Abstract
Diversity within marine microbiomes spans the three domains of life: microbial eukaryotes (i.e., protists), bacteria, and archaea. Although protists were the first microbes observed by microscopy, it took the advent of molecular techniques to begin to resolve their complex and reticulate evolutionary history. Symbioses between microbial entities have been key in this journey, and such interactions continue to shape the ecology of marine microbiomes. Nowadays, photosynthetic marine protists are appreciated for their activities as primary producers, rivalling land plant contributions in the global carbon cycle. Predatory protists are known for consuming prokaryotes and other protists, with some combining metabolisms into a mixotrophic lifestyle. Still, much must be learned about specific interactions and lifestyles, especially for uncultured groups recognized just by environmental sequences. With respect to the fate of protists in food webs, there are many paths to consider. Despite being in early stages of identifying interactions, whether mutualistic or death-inducing infections by parasites and viruses, knowledge is advancing rapidly via methods for interrogation in nature without culturing. Here, we review marine protists, their evolutionary histories, diversity, ecological roles, and lifestyles in all layers of the ocean, with reference to how views have shifted over time through extensive investigation.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abrahão J, Silva L, Silva LS et al (2018) Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat Commun 9:749–749
Adl SM, Simpson AGB, Farmer MA et al (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451
Agrawal S, Barrow CJ, Deshmukh SK (2020) Structural deformation in pathogenic bacteria cells caused by marine fungal metabolites: an in vitro investigation. Microb Pathog 146:104248
Alexeev VA, Esau I, Polyakov IV et al (2012) Vertical structure of recent arctic warming from observed data and reanalysis products. Clim Chang 111:215–239
Amato A, Kooistra WHCF, Montresor M (2019) Cryptic diversity: a long-lasting issue for diatomologists. Protist 170:1–7
Amend A, Burgaud G, Cunliffe M et al (2019) Fungi in the marine environment: open questions and unsolved problems. MBio 10:e01189–e01118
Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684
Amin SA, Hmelo LR, van Tol HM et al (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101
Amir A, McDonald D, Navas-Molina JA et al (2017) Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2:e00191–e00116
Andersen KH, Aksnes DL, Berge T et al (2015) Modelling emergent trophic strategies in plankton. J Plankton Res 37:862–868
Anderson SR, Harvey EL (2020) Temporal variability and ecological interactions of parasitic marine Syndiniales in coastal protist communities. mSphere 5:e00209–e00220
Anderson R, Jürgens K, Hansen PJ (2017) Mixotrophic phytoflagellate bacterivory field measurements strongly biased by standard approaches: a case study. Front Microbiol 8:1398
Anderson R, Charvet S, Hansen PJ (2018) Mixotrophy in chlorophytes and haptophytes: effect of irradiance, macronutrient, micronutrient and vitamin limitation. Front Microbiol 9:1704
Apprill A (2017) Marine animal microbiomes: toward understanding host–microbiome interactions in a changing ocean. Front Mar Sci 4:222
Archibald JM (2006) Endosymbiosis: double-take on plastid origins. Curr Biol 16:R690–R692
Archibald JM (2015) Endosymbiosis and eukaryotic cell evolution. Curr Biol 25:R911–R921
Arenovski AL, Lim EL, Caron DA (1995) Mixotrophic nanoplankton in oligotrophic surface waters of the Sargasso Sea may employ phagotrophy to obtain major nutrients. J Plankton Res 17:801–820
Aris R (1990) Vectors, tensors and the basic equations of fluid mechanics. Courier Corporation, Chelmsford
Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192
Arrigo KR, van Dijken G, Pabi S (2008) Impact of a shrinking Arctic ice cover on marine primary production. Geophys Res Lett 35:L19603
Avrahami Y, Frada MJ (2020) Detection of phagotrophy in the marine phytoplankton group of the coccolithophores (Calcihaptophycidae, Haptophyta) during nutrient-replete and phosphate-limited growth. J Phycol 56:1103–1108
Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696
Azam F, Worden AZ (2004) Oceanography. Microbes, molecules, and marine ecosystems. Science 303:1622–1624
Azam F, Fenchel T, Field JG et al (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
Bachy C, Charlesworth CJ, Chan AM et al (2018) Transcriptional responses of the marine green alga Micromonas pusilla and an infecting prasinovirus under different phosphate conditions. Environ Microbiol 20:2898–2912
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann Rev Ecol Evol Syst 34:661–689
Baldauf SL (2003) The deep roots of eukaryotes. Science 300:1703–1706
Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on earth. Proc Natl Acad Sci 115:6506–6511
Barry MT, Rusconi R, Guasto JS, Stocker R (2015) Shear-induced orientational dynamics and spatial heterogeneity in suspensions of motile phytoplankton. J R Soc Interface 12:20150791
Behrenfeld MJ, O’Malley RT, Siegel DA et al (2006) Climate-driven trends in contemporary ocean productivity. Nature 444:752–755
Benoiston A-S, Ibarbalz FM, Bittner L et al (2017) The evolution of diatoms and their biogeochemical functions. Phil Trans R Soc Lond B 372:20160397
Berdjeb L, Parada AE, Needham DM, Fuhrman JA (2018) Short-term dynamics and interactions of marine protist communities during the spring–summer transition. ISME J 12:1907–1917
Bergh O, Børsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468
Bhattacharya D, Roy RS, Price DC, Schliep A (2014) Single-cell genomics of marine plankton: studying the single life of eukaryotic microbes. Biochemist 36:16–22
Bhattacharyya D, Chakraborty S (2018) Chloroplast: the Trojan horse in plant-virus interaction. Mol Plant Pathol 19:504–518
Biecheler B (1936) Observation de la capture et de la digestion des proies chez un Péridinien vert. J Crustacean Biol 122:1173–1175
Billard C, Inouye I (2004) What is new in coccolithophore biology? In: Thierstein HR, Young JR (eds) Coccolithophores: from molecular processes to global impact. Springer, Berlin, Heidelberg, pp 1–29
Bird DF, Kalff J (1986) Bacterial grazing by planktonic lake algae. Science 231:493–495
Blackwell M (2011) The fungi: 1, 2, 3 … 5.1 million species? Am J Bot 98:426–438
Blanc-mathieu R, Krasovec M, Hebrard M et al (2017) Population genomics of picophytoplankton unveils novel chromosome hypervariability. Sci Adv 3:e1700239
Bochdansky AB, Clouse MA, Herndl GJ (2017) Eukaryotic microbes, principally fungi and labyrinthulomycetes, dominate biomass on bathypelagic marine snow. ISME J 11:362–373
Bock NA, Charvet S, Burns J et al (2021) Experimental identification and in silico prediction of bacterivory in green algae. ISME J 15:1987–2000
Boenigk J, Arndt H (2002) Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Ant Leeuwenhoek 81:465–480
Bolaños LM, Karp-Boss L, Choi CJ et al (2020) Small phytoplankton dominate western North Atlantic biomass. ISME J 14:1663–1674
Bowler C, Vardi A, Allen AE (2010) Oceanographic and biogeochemical insights from diatom genomes. Annu Rev Mar Sci 2:333–365
Box JE, Colgan WT, Christensen TR et al (2019) Key indicators of Arctic climate change: 1971–2017. Environ Res Lett 14:045010
Bradley JA, Amend JP, LaRowe DE (2019) Survival of the fewest: microbial dormancy and maintenance in marine sediments through deep time. Geobiology 17(1):43–59
Bradley JA et al (2020) Widespread energy limitation to life in global subseafloor sediments. Sci Adv 6(32):eaba0697
Breitbart M, Bonnain C, Malki K, Sawaya NA (2018) Phage puppet masters of the marine microbial realm. Nat Microbiol 3:754–766
Brocke R, Fatka O, Wilde V (2006) Acritarchs and prasinophytes of the Silurian-Devonian GSSP (Klonk, Barrandian area, Czech Republic). Bull Geosci 81:27–41
Brown RM, Malcolm Brown R (1972) Algal viruses. Adv Virus Res 17:243–277
Brown MW, Heiss AA, Kamikawa R et al (2018) Phylogenomics places orphan protistan lineages in a novel eukaryotic super-group. Genome Biol Evol 10:427–433
Brown JM, Labonté JM, Brown J et al (2020) Single cell genomics reveals viruses consumed by marine protists. Front Microbiol 11:524828
Brumley DR, Rusconi R, Son K, Stocker R (2015) Flagella, flexibility and flow: physical processes in microbial ecology. Eur Phys J Spec Top 224:3119–3140
Brunet T, King N (2017) The origin of animal multicellularity and cell differentiation. Dev Cell 43:124–140
Brunson JK, McKinnie SMK, Chekan JR et al (2018) Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom. Science 361:1356–1358
Brussaard CPD (2004) Viral control of phytoplankton populations--a review. J Eukaryot Microbiol 51:125–138
Brussaard CPD, Kempers RS, Kop AJ et al (1996) Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquat Microb Ecol 10:105–113
Brussaard CPD, Kuipers B, Veldhuis MJW (2005) A mesocosm study of Phaeocystis globosa population dynamics: I. regulatory role of viruses in bloom control. Harmful Algae 4:859–874
Bryant JA, Aylward FO, Eppley JM et al (2016) Wind and sunlight shape microbial diversity in surface waters of the North Pacific subtropical gyre. ISME J 10:1308–1322
Buaya AT, Ploch S, Hanic L et al (2017) Phylogeny of Miracula helgolandica gen. et sp. nov. and Olpidiopsis drebesii sp. nov., two basal oomycete parasitoids of marine diatoms, with notes on the taxonomy of Ectrogella-like species. Mycol Prog 16:1041–1050
Burkholder JM, Glibert PM, Skelton HM (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93
Burki F (2017) The convoluted evolution of eukaryotes with complex plastids. In: Hirakawa Y (ed) Advances in botanical research. Academic Press, London, pp 1–30
Burki F, Kaplan M, Tikhonenkov DV et al (2016) Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc Biol Sci 283:20152802
Burki F, Roger AJ, Brown MW, Simpson AGB (2020) The new tree of eukaryotes. Trends Ecol Evol 35:43–55
Cachon M, Caram B (1979) A symbiotic green alga, Pedinomonas symbiotica sp. nov. (Prasinophyceae), in the radiolarian Thalassolampe margarodes. Phycologia 18:177–184
Cahoon L (2016) Tychoplankton. In: Kennish MJ (ed) Encyclopedia of estuaries. Springer Netherlands, Dordrecht, pp 721–721
Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49:51–57
Callahan BJ, Mcmurdie PJ, Rosen MJ et al (2016) DADA2: high resolution sample inference from amplicon data. Nat Methods 13:581–583
Carlile M (1982) Prokaryotes and eukaryotes: strategies and successes. Trends Biochem Sci 7:128–130
Caron DA, Alexander H, Allen AE et al (2017) Probing the evolution, ecology and physiology of marine protists using transcriptomics. Nat Rev Microbiol 15:6–20
Carradec Q, Pelletier E, Da Silva C et al (2018) A global ocean atlas of eukaryotic genes. Nat Commun 9:373
Casteleyn G, Leliaert F, Backeljau T et al (2010) Limits to gene flow in a cosmopolitan marine planktonic diatom. Proc Natl Acad Sci 107:12952–12957
Castillo YM, Mangot J-F, Benites LF et al (2019) Assessing the viral content of uncultured picoeukaryotes in the global-ocean by single cell genomics. Mol Ecol 28:4272–4289
Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? Biosystems 14:461–481
Cavalier-Smith T (2018) Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences. Protoplasma 255:297–357
Cavalier-Smith T, von der Heyden S (2007) Molecular phylogeny, scale evolution and taxonomy of centrohelid heliozoa. Mol Phylogenet Evol 44:1186–1203
Cavalier-Smith T, Chao EE, Lewis R (2015) Multiple origins of Heliozoa from flagellate ancestors: new cryptist subphylum Corbihelia, superclass Corbistoma, and monophyly of Haptista, Cryptista, Hacrobia and Chromista. Mol Phylogenet Evol 93:331–362
Cavalier-Smith T, Chao EE, Lewis R (2016) 187-gene phylogeny of protozoan phylum Amoebozoa reveals a new class (Cutosea) of deep-branching, ultrastructurally unique, enveloped marine Lobosa and clarifies amoeba evolution. Mol Phylogenet Evol 99:275–296
Cavicchioli R, Ripple WJ, Timmis KN et al (2019) Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17:569–586
Ceballos G, Ehrlich PR, Barnosky AD et al (2015) Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci Adv 1:e1400253
Cermeño P (2016) The geological story of marine diatoms and the last generation of fossil fuels. Perspect Phycol 3:53–60
Chambouvet A, Morin P, Marie D, Guillou L (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322:1254–1257
Chambouvet A, Monier A, Maguire F et al (2019) Intracellular infection of diverse diatoms by an evolutionary distinct relative of the fungi. Curr Biol 29:4093–4101
Chan CX, Ragan MA (2013) Next-generation phylogenomics. Biol Direct 8:3
Choi CJ, Bachy C, Jaeger GS et al (2017) Newly discovered deep-branching marine plastid lineages are numerically rare but globally distributed. Curr Biol 27:R15–R16
Choi CJ, Jimenez V, Needham DM et al (2020) Seasonal and geographical transitions in eukaryotic phytoplankton community structure in the Atlantic and Pacific oceans. Front Microbiol 11:542372
Chrismas N, Cunliffe M (2020) Depth-dependent mycoplankton glycoside hydrolase gene activity in the open ocean-evidence from the Tara oceans eukaryote metatranscriptomes. ISME J 14:2361–2365
Cooney EC, Okamoto N, Cho A et al (2020) Single-cell transcriptomics of Abedinium reveals a new early-branching dinoflagellate lineage. Genome Biol Evol 12:2417–2428
Corliss JO (1984) The kingdom Protista and its 45 phyla. Biosystems 17:87–126
Cram JA, Chow C-ET, Sachdeva R et al (2014) Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J 9:563–563
Cunliffe M, Hollingsworth A, Bain C et al (2017) Algal polysaccharide utilisation by saprotrophic planktonic marine fungi. Fungal Ecol 30:135–138
Cuvelier ML, Allen AE, Monier A et al (2010) Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc Natl Acad Sci 107:14679–14684
Daugbjerg N, Jensen MH, Hansen PJ (2013) Using nuclear-encoded LSU and SSU rDNA sequences to identify the eukaryotic endosymbiont in Amphisolenia bidentata (Dinophyceae). Protist 164:411–422
De Luca D, Piredda R, Sarno D, Kooistra WHCF (2021) Resolving cryptic species complexes in marine protists: phylogenetic haplotype networks meet global DNA metabarcoding datasets. ISME J 15:1931–1942
de Mendoza A, Suga H, Permanyer J et al (2015) Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals. elife 4:e08904
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886
de Vargas C, Audic S, Henry N et al (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605
de Wit R, Bouvier T (2006) “Everything is everywhere, but, the environment selects”; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758
DeAngelis KM, Silver WL, Thompson AW, Firestone MK (2010) Microbial communities acclimate to recurring changes in soil redox potential status. Environ Microbiol 12:3137–3149
Decelle J (2013) New perspectives on the functioning and evolution of photosymbiosis in plankton: mutualism or parasitism? Commun Integr Biol 6:e24560
Decelle J, Martin P, Paborstava K et al (2013) Diversity, ecology and biogeochemistry of cyst-forming acantharia (radiolaria) in the oceans. PLoS One 8:e53598
Decelle J, Colin S, Foster RA (2015) Photosymbiosis in marine planktonic protists. In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N, Not F (eds) Marine Protists: diversity and dynamics. Springer, Tokyo, pp 465–500
Decelle J, Stryhanyuk H, Gallet B et al (2019) Algal remodeling in a ubiquitous planktonic photosymbiosis. Curr Biol 29:968–978.e4
Deeg CM, Zimmer MM, George EE et al (2019) Chromulinavorax destructans, a pathogen of microzooplankton that provides a window into the enigmatic candidate phylum Dependentiae. PLoS Pathog 15:e1007801
del Campo J, Massana R (2011) Emerging diversity within chrysophytes, choanoflagellates and bicosoecids based on molecular surveys. Protist 162:435–448
del Giorgio PA, Gasol JM, Vaqué D et al (1996) Bacterioplankton community structure: Protists control net production and the proportion of active bacteria in a coastal marine community. Limnol Oceanogr 41:1169–1179
Delaroque N, Boland W (2008) The genome of the brown alga Ectocarpus siliculosus contains a series of viral DNA pieces, suggesting an ancient association with large dsDNA viruses. BMC Evol Biol 8:110
Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6:361–375
Demir-Hilton E, Sudek S, Cuvelier ML et al (2011) Global distribution patterns of distinct clades of the photosynthetic picoeukaryote Ostreococcus. ISME J 5:1095–1107
Derelle R, López-García P, Timpano H, Moreira D (2016) A phylogenomic framework to study the diversity and evolution of stramenopiles (= heterokonts). Mol Biol Evol 33:2890–2898
Deshmukh SK, Prakash V, Ranjan N (2017) Marine fungi: A source of potential anticancer compounds. Front Microbiol 8:2536
Diamond LS, Mattern CF (1976) Protozoal viruses. Adv Virus Res 20:87–112
Diamond LS, Mattern CF, Bartgis IL (1972) Viruses of Entamoeba histolytica. I Identification of transmissible virus-like agents. J Virol 9:326–341
Diekmann Y, Pereira-Leal JB (2013) Evolution of intracellular compartmentalization. Biochem J 449:319–331
Díez B, Pedrós-Alió C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941
Dittami SM, Arboleda E, Auguet J-C et al (2021) A community perspective on the concept of marine holobionts: state-of-the-art, challenges, and future directions. PeerJ 9:e10911
Dixon AK, Needham DM, Al-Horani FA, Chadwick NE (2013) Microhabitat use and photoacclimation in the clownfish sea anemone Entacmaea quadricolor. J Mar Biol Assoc 94:473–480
do Rosário Gomes H, Goes JI, Matondkar SGP et al (2014) Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia. Nat Commun 5:4862
do Rosário Gomes H, McKee K, Mile A et al (2018) Influence of light availability and prey type on the growth and photo-physiological rates of the mixotroph Noctiluca scintillans. Front Mar Sci 5:374
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192
Doney SC, Ruckelshaus M, Duffy JE et al (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37
Doolittle WF (1998a) A paradigm gets shifty. Nature 392:15–16
Doolittle WF (1998b) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311
Dorrell RG, Drew J, Nisbet RER, Howe CJ (2014) Evolution of chloroplast transcript processing in plasmodium and its chromerid algal relatives. PLoS Genet 10:e1004008
Dorrell RG, Gile G, McCallum G et al (2017) Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. elife 6:e23717
Droop MR (1957) Auxotrophy and organic compounds in the nutrition of marine phytoplankton. J Gen Microbiol 16:286–293
Duanmu D, Bachy C, Sudek S et al (2014) Marine algae and land plants share conserved phytochrome signaling systems. Proc Natl Acad Sci 111:15827–15832
Ducklow HW, Steinberg DK, Buesseler KO (2001) Upper Ocean carbon export and the biological pump. Oceanography 14:50–58
Dupont CL, McCrow JP, Valas R et al (2015) Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities. ISME J 9:1076–1092
Eckford-Soper L, Daugbjerg N (2016) The ichthyotoxic genus Pseudochattonella (Dictyochophyceae): distribution, toxicity, enumeration, ecological impact, succession and life history – a review. Harmful Algae 58:51–58
Edgar GJ, Stuart-Smith RD, Willis TJ et al (2014) Global conservation outcomes depend on marine protected areas with five key features. Nature 506:216–220
Edgcomb VP (2016) Marine protist associations and environmental impacts across trophic levels in the twilight zone and below. Curr Op Microbiol 31:169–175
Edgcomb VP, Leadbetter ER, Bourland W et al (2011) Structured multiple endosymbiosis of bacteria and archaea in a ciliate from marine sulfidic sediments: a survival mechanism in low oxygen, sulfidic sediments? Front Microbiol 2:55
Edwards KF (2019) Mixotrophy in nanoflagellates across environmental gradients in the ocean. Proc Natl Acad Sci 116:6211–6220
Eren AM, Morrison HG, Lescault PJ et al (2015) Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J 9:968–979
Faktorová D, Nisbet RER, Fernández Robledo JA et al (2020) Genetic tool development in marine protists: emerging model organisms for experimental cell biology. Nat Methods 17:481–494
Falkowski P (2012) Ocean science: the power of plankton. Nature 483:17–20
Febvre-Chevalier C, Febvre J (1994) Buoyancy and swimming in marine planktonic protists. In: Maddock L, Bone Q, Rayner JMV (eds) Mechanics and physiology of animal swimming. Cambridge University Press, Cambridge, pp 13–26
Field MC, Dacks JB (2009) First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr Op Cell Biol 21:4–13
Field CB, Behrenfeld MJ, Randerson JT et al (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240
Filée J (2014) Multiple occurrences of giant virus core genes acquired by eukaryotic genomes: the visible part of the iceberg? Virology 466–467:53–59
Finkel ZV, Beardall J, Flynn KJ et al (2009) Phytoplankton in a changing world: cell size and elemental stoichiometry. J Plankton Res 32:119–137
Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063
Fitzsimmons JN, Hayes CT, Al-Subiai SN et al (2015) Daily to decadal variability of size-fractionated iron and iron-binding ligands at the Hawaii Ocean Time-Series Station ALOHA. Geochim Cosmochim Acta 171:303–324
Flannagan RS, Jaumouillé V, Grinstein S (2012) The cell biology of phagocytosis. Annu Rev Pathol 7:61–98
Flegontova O, Flegontov P, Malviya S et al (2016) Extreme diversity of diplonemid eukaryotes in the ocean. Curr Biol 26:3060–3065
Flombaum P, Gallegos JL, Gordillo RA et al (2013) Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci 110:9824–9829
Flynn KJ, Stoecker DK, Mitra A et al (2012) Misuse of the phytoplankton–zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J Plankton Res 35:3–11
Flynn KJ, Mitra A, Glibert PM, Burkholder JM (2018) Mixotrophy in harmful algal blooms: by whom, on whom, when, why, and what next. In: Glibert PM, Berdalet E, Burford MA et al (eds) Global ecology and oceanography of harmful algal blooms. Springer International Publishing, Cham, pp 113–132
Flynn KJ, Mitra A, Anestis K et al (2019) Mixotrophic protists and a new paradigm for marine ecology: where does plankton research go now? J Plankton Res 41:375–391
Forster D, Dunthorn M, Mahé F et al (2016) Benthic protists: the under-charted majority. FEMS Microbiol Ecol 92:fiw120
Foster RA, Zehr JP (2006) Characterization of diatom–cyanobacteria symbioses on the basis of nifH, hetR and 16S rRNA sequences. Environ Microbiol 8:1913–1925
Foster RA, Kuypers MMM, Vagner T et al (2011) Nitrogen fixation and transfer in open ocean diatom–cyanobacterial symbioses. ISME J 5:1484–1484
Foulon E, Not F, Jalabert F et al (2008) Ecological niche partitioning in the picoplanktonic green alga Micromonas pusilla: evidence from environmental surveys using phylogenetic probes. Environ Microbiol 10:2433–2443
Frias-Lopez J, Thompson A, Waldbauer J, Chisholm SW (2009) Use of stable isotope-labelled cells to identify active grazers of picocyanobacteria in ocean surface waters. Environ Microbiol 11:512–525
Fuhrman JA, Cram JA, Needham DM (2015) Marine microbial community dynamics and their ecological interpretation. Nat Rev Microbiol 13:133–146
Gaines G, Taylor FJR (1984) Extracellular digestion in marine dinoflagellates. J Plankton Res 6:1057–1061
Gallot-Lavallée L, Blanc G (2017) A glimpse of Nucleo-cytoplasmic large DNA virus biodiversity through the eukaryotic genomics window. Viruses 9:17
Gardner MJ, Hall N, Fung E et al (2002) Genome sequence of the human malaria parasite plasmodium falciparum. Nature 419:498–511
Garvetto A, Badis Y, Perrineau M-M et al (2019) Chytrid infecting the bloom-forming marine diatom Skeletonema sp.: morphology, phylogeny and distribution of a novel species within the Rhizophydiales. Fungal Biol 123:471–480
Gastrich MD, Leigh-Bell JA, Gobler CJ et al (2004) Viruses as potential regulators of regional brown tide blooms caused by the alga, Aureococcus anophagefferens. Estuaries 27:112–119
Gawryluk RMR, Tikhonenkov DV, Hehenberger E et al (2019) Non-photosynthetic predators are sister to red algae. Nature 572:240–243
Genitsaris S, Monchy S, Viscogliosi E et al (2015) Seasonal variations of marine protist community structure based on taxon-specific traits using the eastern English Channel as a model coastal system. FEMS Microbiol Ecol 91:fiv034
Gibbs A, Skotnicki AH, Gardiner JE et al (1975) A tobamovirus of a green alga. Virology 64:571–574
Gilbert C, Cordaux R (2017) Viruses as vectors of horizontal transfer of genetic material in eukaryotes. Curr Op Virol 25:16–22
Giovannoni SJ, Vergin KL (2012) Seasonality in ocean microbial communities. Science 335:671–676
Glassman SI, Martiny JBH (2018) Broadscale ecological patterns are robust to use of exact sequence variants versus operational taxonomic units. mSphere 3:e00148–e00118
Glibert PM (2017) Eutrophication, harmful algae and biodiversity - challenging paradigms in a world of complex nutrient changes. Mar Pollut Bull 124:591–606
Glücksman E, Snell EA, Berney C et al (2011) The novel marine gliding zooflagellate genus Mantamonas (Mantamonadida Ord. N.: Apusozoa). Protist 162:207–221
Gobler CJ, Anderson OR, Gastrich MD, Wilhelm SW (2007) Ecological aspects of viral infection and lysis in the harmful brown tide alga Aureococcus anophagefferens. Aquat Microb Ecol 47:25–36
Gobler CJ, Berry DL, Dyhrman ST et al (2011) Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc Natl Acad Sci 108:4352–4357
Gonzáez JM, Sherr EB, Sherr BF (1993) Differential feeding by marine flagellates on growing versus starving, and on motile versus nonmotile, bacterial prey. Mar Ecol Prog Ser 102:257–267
Gooday AJ, Schoenle A, Dolan JR, Arndt H (2020) Protist diversity and function in the dark ocean – challenging the paradigms of deep-sea ecology with special emphasis on foraminiferans and naked protists. Eur J Protistol 75:125721
Goodenough U, Heitman J (2014) Origins of eukaryotic sexual reproduction. Cold Spring Harb Perspect Biol 6:a016154
Goodenough U, Lin H, Lee J-H (2007) Sex determination in Chlamydomonas. Semin Cell Dev Biol 18:350–361
Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517
Grant CR, Wan J, Komeili A (2018) Organelle formation in bacteria and archaea. Annu Rev Cell Dev Biol 34:217–238
Graversen RG, Mauritsen T, Tjernström M et al (2008) Vertical structure of recent Arctic warming. Nature 451:53–56
Griffiths DJ (2001) Endogenous retroviruses in the human genome sequence. Genome Biol 2:reviews1017.1
Grigoriev IV, Hayes RD, Calhoun S et al (2021) PhycoCosm, a comparative algal genomics resource. Nucleic Acids Res 49:D1004–D1011
Grimsley N, Péquin B, Bachy C et al (2010) Cryptic sex in the smallest eukaryotic marine green alga. Mol Biol Evol 27:47–54
Grossart H-P, Van den Wyngaert S, Kagami M et al (2019) Fungi in aquatic ecosystems. Nat Rev Microbiol 17:339–354
Gsell AS, de Senerpont Domis LN, Verhoeven KJF et al (2013) Chytrid epidemics may increase genetic diversity of a diatom spring-bloom. ISME J 7:2057–2059
Guadayol Ò, Peters F, Marrasé C et al (2009) Episodic meteorological and nutrient-load events as drivers of coastal planktonic ecosystem dynamics: a time-series analysis. Mar Ecol Prog Ser 381:139–155
Guidi L, Chaffron S, Bittner L et al (2016) Plankton networks driving carbon export in the oligotrophic ocean. Nature 532:465–465
Guillou L, Viprey M, Chambouvet A et al (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10:3349–3365
Gustavsen JA, Winget DM, Tian X, Suttle CA (2014) High temporal and spatial diversity in marine RNA viruses implies that they have an important role in mortality and structuring plankton communities. Front Microbiol 5:703
Gutiérrez MH, Jara AM, Pantoja S (2016) Fungal parasites infect marine diatoms in the upwelling ecosystem of the Humboldt current system off Central Chile. Environ Microbiol 18:1646–1653
Gutowska MA, Shome B, Sudek S et al (2017) Globally important haptophyte algae use exogenous pyrimidine compounds more efficiently than thiamin. MBio 8:e01459–e01417
Hadariová L, Vesteg M, Hampl V, Krajčovič J (2018) Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists. Curr Genet 64:365–387
Haeckel E (1887) Report on the Radiolaria collected by HMS challenger during the years 1873–1876. Report of the voyage of HMS challenger. Zoology 18:i–clxxxviii
Haeckel EHPA, Ernst Heinrich Philipp (1862) Die Radiolarien (Rhizopoda radiaria): eine Monographie
Hallock P (1999) Symbiont-bearing foraminifera. In: Modern foraminifera. Springer, Berlin, pp 123–139
Han KY, Maciszewski K, Graf L et al (2019) Dictyochophyceae plastid genomes reveal unusual variability in their organization. J Phycol 55:1166–1180
Händeler K, Grzymbowski YP, Krug PJ, Wägele H (2009) Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life. Front Zool 6:28
Hanic LA, Sekimoto S, Bates SS (2009) Oomycete and chytrid infections of the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae) from Prince Edward Island, Canada. Botany 87:1096–1105
Hansen PJ (2011) The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J Eukaryot Microbiol 58:203–214
Hansen PJ, Calado AJ (1999) Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J Eukaryot Microbiol 46:382–389
Hansen PJ, Hjorth M (2002) Growth and grazing responses of Chrysochromulina ericina (Prymnesiophyceae): the role of irradiance, prey concentration and pH. Mar Biol 141:975–983
Hartmann M, Grob C, Tarran GA et al (2012) Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc Natl Acad Sci 109:5756–5760
Hartmann M, Zubkov MV, Scanlan DJ, Lepère C (2013) In situ interactions between photosynthetic picoeukaryotes and bacterioplankton in the Atlantic Ocean: evidence for mixotrophy. Environ Microbiol Rep 5:835–840
Harvey EL, Jeong HJ, Menden-Deuer S (2013) Avoidance and attraction: chemical cues influence predator-prey interactions of planktonic protists. Limnol Oceanogr 58:1176–1184
Hassett BT, Borrego EJ, Vonnahme TR et al (2019) Arctic marine fungi: biomass, functional genes, and putative ecological roles. ISME J 13:1484–1496
Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. In: Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, NAR G (eds) The fungal Kingdom. American Society for Microbiology, Washington, DC. https://doi.org/10.1128/9781555819583.ch4
Hehenberger E, Tikhonenkov DV, Kolisko M et al (2017) Novel predators reshape Holozoan phylogeny and reveal the presence of a two-component signaling system in the ancestor of animals. Curr Biol 27:2043–2050
Hehenberger E, Gast RJ, Keeling PJ (2019) A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Proc Natl Acad Sci 116:17934–17942
Heintze C, Formanek P, Pohl D et al (2020) An intimate view into the silica deposition vesicles of diatoms. BMC Materials 2:11
Hildebrand M, Lerch SJL (2015) Diatom silica biomineralization: parallel development of approaches and understanding. Semin Cell Dev Biol 46:27–35
Hoehler TM, Alperin MJ, Albert DB, Martens CS (1998) Thermodynamic control on hydrogen concentrations in anoxic sediments. Geochim Cosmochim Acta 62:1745–1756
Hu SK, Connell PE, Mesrop LY, Caron DA (2018) A hard day’s night: diel shifts in microbial eukaryotic activity in the North Pacific subtropical gyre. Front Mar Sci 5:351
Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145
Hyman P, Abedon ST (2012) Smaller fleas: viruses of microorganisms. Scientifica 2012:734023
Ibarbalz FM, Henry N, Brandão MC et al (2019) Global trends in marine plankton diversity across kingdoms of life. Cell 179:1084–1097
Ibelings BW, De Bruin A, Kagami M et al (2004) Host parasite interactions between freshwater phytoplankton and chytrid fungi (Chytridiomycota). J Phycol 40:437–453
Imachi H, Nobu MK, Nakahara N et al (2020) Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577:519–525
Inagaki F, Hinrichs K-U, Kubo Y, The IODP Expedition 337 Scientists (2016) IODP expedition 337: deep coalbed biosphere off Shimokita – microbial processes and hydrocarbon system associated with deeply buried coalbed in the ocean. Sci Drill 21:17–28
Jahson S, Rai AN, Bergman B (1995) Intracellular cyanobiont Richelia intracellularis: ultrastructure and immuno-localisation of phycoerythrin, nitrogenase, rubisco and glutamine synthetase. Mar Biol 124:1–8
James TY, Stajich JE, Hittinger CT, Rokas A (2020) Toward a fully resolved fungal tree of life. Annu Rev Microbiol 74:291–313
Janouskovec J, Horák A, Oborník M et al (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci 107:10949–10954
Janouškovec J, Tikhonenkov DV, Burki F et al (2015) Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc Natl Acad Sci 112:10200–10207
Janouškovec J, Tikhonenkov DV, Burki F et al (2017) A new lineage of eukaryotes illuminates early mitochondrial genome reduction. Curr Biol 27:3717–3724
Jardillier L, Zubkov MV, Pearman J, Scanlan DJ (2010) Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical Northeast Atlantic Ocean. ISME J 4:1180–1192
Jephcott TG, Alves-de-Souza C, Gleason FH et al (2016) Ecological impacts of parasitic chytrids, syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates. Fungal Ecol 19:47–58
Jiang H, Kulis DM, Brosnahan ML, Anderson DM (2018) Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum. Harmful Algae 77:43–54
John U, Lu Y, Wohlrab S et al (2019) An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome. Sci Adv 5:eaav1110
Johnson AR, Omand MM (2021) Evolution of a subducted carbon-rich filament on the edge of the North Atlantic gyre. J Geophys Res C: Oceans 49:438–460
Johnson MD, Oldach D, Delwiche CF, Stoecker DK (2007) Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426–428
Johnson WM, Alexander H, Bier RL et al (2020) Auxotrophic interactions: a stabilizing attribute of aquatic microbial communities? FEMS Microbiol Ecol 96:fiaa115
Jones RI (2000) Mixotrophy in planktonic protists: an overview: Mixotrophy in planktonic protists. Freshw Biol 45:219–226
Jones EBG (2011) Are there more marine fungi to be described? Bot Mar 54:343–354
Jørgensen BB, Kasten S (2006) Sulfur cycling and methane oxidation. In: Schulz HD, Zabel M (eds) Marine Geochemistry. Springer, Berlin, Heidelberg, pp 271–309
Jürgens K, Massana R (2008) Protistan grazing on marine bacterioplankton. In: Kirchman DL (ed) Microbial ecology of the oceans. John Wiley & Sons, Inc., Hoboken, NJ, pp 383–441
Jürgens K, Matz C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Ant Leeuwenhoek 81:413–434
Kallmeyer J, Pockalny R, Adhikari RR et al (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci 109:16213–16216
Kamennaya NA, Kennaway G, Fuchs BM, Zubkov MV (2018) “Pomacytosis”—semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae. PLoS Biol 16:e2003502
Kamp A, Høgslund S, Risgaard-Petersen N, Stief P (2015) Nitrate storage and dissimilatory nitrate reduction by eukaryotic microbes. Front Microbiol 6:1492
Kaneko H, Blanc-Mathieu R, Endo H et al (2021) Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean. iScience 24:102002
Karlusich JJP, Ibarbalz FM, Bowler C (2020) Exploration of marine phytoplankton: from their historical appreciation to the omics era. J Plankton Res 42:595–612
Karnkowska A, Vacek V, Zubáčová Z et al (2016) A eukaryote without a mitochondrial organelle. Curr Biol 26:1274–1284
Karpov SA, Mamkaeva MA, Aleoshin VV et al (2014) Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Front Microbiol 5:112
Kawachi M, Inouye I, Maeda O, Chihara M (1991) The haptonema as a food-capturing device: observations on Chrysochromulina hirta (Prymnesiophyceae). Phycologia 30:563–573
Kawachi M, Nakayama T, Kayama M et al (2021) Rappemonads are haptophyte phytoplankton. Curr Biol 31:2395–2403
Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607
Keeling PJ, Burki F (2019) Progress towards the tree of eukaryotes. Curr Biol 29:R808–R817
Keeling PJ, Campo JD (2017) Marine protists are not just big bacteria. Curr Biol 27:R541–R549
Keeling PJ, Burger G, Durnford DG et al (2005) The tree of eukaryotes. Trends Ecol Evol 20:670–676
Keeling PJ, Burki F, Wilcox HM et al (2014) The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol 12:e1001889
Kerszberg M (2000) The survival of slow reproducers. J Theor Biol 206:81–89
Kilias ES, Junges L, Šupraha L et al (2020) Chytrid fungi distribution and co-occurrence with diatoms correlate with sea ice melt in the Arctic Ocean. Commun Biol 3:183
Kim E, Harrison JW, Sudek S et al (2011a) Newly identified and diverse plastid-bearing branch on the eukaryotic tree of life. Proc Natl Acad Sci 108:1496–1500
Kim E, Harrison JW, Sudek S et al (2011b) Newly identified and diverse plastid-bearing branch on the eukaryotic tree of life. Proc Natl Acad Sci 108:1496–1500
Kim DY, Countway PD, Jones AC et al (2013) Monthly to interannual variability of microbial eukaryote assemblages at four depths in the eastern North Pacific. ISME J 8:515–530
King N, Westbrook MJ, Young SL et al (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788
Kiørboe T, Visser A, Andersen KH (2018) A trait-based approach to ocean ecology. ICES J Mar Sci 75:1849–1863
Kleindienst S, Grim S, Sogin M et al (2016) Diverse, rare microbial taxa responded to the Deepwater horizon deep-sea hydrocarbon plume. ISME J 10:400–415
Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60:115–138
Knight-Jones EW, Walne PR (1951) Chromulina pusilla butcher; a dominant member of the ultraplankton. Nature 167:445–446
Kolb A, Strom S (2013) An inducible antipredatory defense in haploid cells of the marine microalga Emiliania huxleyi (Prymnesiophyceae). Limnol Oceanogr 58:932–944
Krabberød AK, Orr RJS, Bråte J et al (2017) Single cell transcriptomics, mega-phylogeny, and the genetic basis of morphological innovations in Rhizaria. Mol Biol Evol 34:1557–1573
Kristiansen J, Škaloud P (2017) Chrysophyta. In: Archibald JM, Simpson AGB, Slamovits CH (eds) Handbook of the protists. Springer International Publishing, Cham, pp 331–366
Ku C, Nelson-Sathi S, Roettger M et al (2015) Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524:427–432
Kudryavtsev A, Pawlowski J, Smirnov A (2018) More amoebae from the deep-sea: two new marine species of Vexillifera (Amoebozoa, Dactylopodida) with notes on taxonomy of the genus. Eur J Protistol 66:9–25
La Scola B, Audic S, Robert C et al (2003) A giant virus in amoebae. Science 299:2033
Labarre A, López-Escardó D, Latorre F et al (2021) Comparative genomics reveals new functional insights in uncultured MAST species. ISME J 15:1767–1781
Lam P, Kuypers MMM (2011) Microbial nitrogen cycling processes in oxygen minimum zones. Annu Rev Mar Sci 3:317–345
Lambert S, Tragin M, Lozano J-C et al (2019) Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations. ISME J 13:388–401
Lane N (2011) Energetics and genetics across the prokaryote-eukaryote divide. Biol Direct 6:35
Lane CE, Archibald JM (2008) The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol Evol 23:268–275
Lane N, Martin W (2010) The energetics of genome complexity. Nature 467:929–934
Lax G, Eglit Y, Eme L et al (2018) Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes. Nature 564:410–414
Leadbeater BSC (2015) The choanoflagellates. Cambridge University Press, Cambridge
Leander BS (2008) Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends Parasitol 24:60–67
Leander BS (2020) Predatory protists. Curr Biol 30:R510–R516
Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130
Leray M, Knowlton N (2016) Censusing marine eukaryotic diversity in the twenty-first century. Phil Trans R Soc Lond B 371:20150331
Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556
Li WKW, McLaughlin F, Lovejoy C, Carmack EC (2009) Smallest algae thrive as the Arctic Ocean freshens. Science 326:539–539
Li Q, Edwards KF, Schvarcz CR et al (2021) Plasticity in the grazing ecophysiology of Florenciella (Dichtyochophyceae), a mixotrophic nanoflagellate that consumes Prochlorococcus and other bacteria. Limnol Oceanogr 66:47–60
Lie AAY, Kim DY, Schnetzer A, Caron DA (2013) Small-scale temporal and spatial variations in protistan community composition at the San Pedro Ocean time-series station off the coast of southern California. Aquat Microb Ecol 70:93–110
Lima-Mendez G, Faust K, Henry N et al (2015) Ocean plankton. Determinants of community structure in the global plankton interactome. Science 348:1262073–1262073
Limardo AJ, Sudek S, Choi CJ et al (2017) Quantitative biogeography of picoprasinophytes establishes ecotype distributions and significant contributions to marine phytoplankton. Environ Microbiol 19:3219–3234
Lin Y-C, Campbell T, Chung C-C et al (2012) Distribution patterns and phylogeny of marine stramenopiles in the North Pacific Ocean. Appl Environ Microbiol 78:3387–3399
Lindell D, Jaffe JD, Johnson ZI et al (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86–89
Ling Y-C, Gan HM, Bush M et al (2018) Time-resolved microbial guild responses to tidal cycling in a coastal acid-sulfate system. Environ Chem 15:2–17
Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639
Litchman E, Ohman MD, Kiørboe T (2013) Trait-based approaches to zooplankton communities. J Plankton Res 35:473–484
Liu H, Probert I, Uitz J et al (2009) Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. Proc Natl Acad Sci U S A 106:12803–12808
Liu H, Aris-Brosou S, Probert I, de Vargas C (2010) A time line of the environmental genetics of the haptophytes. Mol Biol Evol 27:161–176
Liu H, Stephens TG, González-Pech RA, et al (2018) Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun Biol 1:95
Livermore JA, Mattes TE (2013) Phylogenetic detection of novel Cryptomycota in an Iowa (United States) aquifer and from previously collected marine and freshwater targeted high-throughput sequencing sets. Environ Microbiol 15:2333–2341
Lomas MW, Bates NR, Johnson RJ et al (2013) Two decades and counting: 24-years of sustained open ocean biogeochemical measurements in the Sargasso Sea. Deep Sea Res Part 2 Top Stud Oceanogr 93:16–32
López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607
López-García P, Eme L, Moreira D (2017) Symbiosis in eukaryotic evolution. J Theor Biol 434:20–33
Lowe CD, Minter EJ, Cameron DD, Brockhurst MA (2016) Shining a light on exploitative host control in a photosynthetic endosymbiosis. Curr Biol 26:207–211
Lundholm N, Hasle GR (2010) Fragilariopsis (Bacillariophyceae) of the Northern Hemisphere – morphology, taxonomy, phylogeny and distribution, with a description of F. pacifica sp. nov. Phycologia 49:438–460
Luo G, Ono S, Beukes NJ et al (2016) Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago. Sci Adv 2:e1600134
Luo E, Eppley JM, Romano AE et al (2020) Double-stranded DNA virioplankton dynamics and reproductive strategies in the oligotrophic open ocean water column. ISME J 14:1304–1315
Lynch M, Marinov GK (2017) Membranes, energetics, and evolution across the prokaryote-eukaryote divide. elife 6:e20437
Lyons TW, Reinhard CT, Planavsky NJ (2014) The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506:307–315
Maamar A, Lucchesi M-E, Debaets S et al (2020) Highlighting the crude oil bioremediation potential of marine fungi isolated from the port of Oran (Algeria). Diversity 12:196
Madin LP, Horgan EF, Steinberg DK (2001) Zooplankton at the Bermuda Atlantic time-series study (BATS) station: diel, seasonal and interannual variation in biomass, 1994–1998. Deep Sea Res Part 2 Top Stud Oceanogr 48:2063–2082
Mafra LL Jr, Nagai S, Uchida H et al (2016) Harmful effects of Dinophysis to the ciliate Mesodinium rubrum: implications for prey capture. Harmful Algae 59:82–90
Malviya S, Scalco E, Audic S et al (2016) Insights into global diatom distribution and diversity in the world’s ocean. Proc Natl Acad Sci 113:E1516–E1525
Margulis L (1990) Words as battle cries—symbiogenesis and the new field of endocytobiology. Bioscience 40:673–677
Marin B, Melkonian M (2010) Molecular phylogeny and classification of the Mamiellophyceae class. Nov. (Chlorophyta) based on sequence comparisons of the nuclear- and plastid-encoded rRNA operons. Protist 161:304–336
Martini S, Larras F, Boyé A et al (2020) Functional trait-based approaches as a common framework for aquatic ecologists. Limnol Oceanogr 66:965–994
Martin-Platero AM, Cleary B, Kauffman K et al (2018) High resolution time series reveals cohesive but short-lived communities in coastal plankton. Nat Commun 9:266
Massana R, Pedrós-Alió C (2008) Unveiling new microbial eukaryotes in the surface ocean. Curr Op Microbiol 11:213–218
Massana R, Guillou L, Díez B, Pedrós-Alió C (2002) Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol 68:4554–4558
Massana R, Balagué V, Guillou L, Pedrós-Alió C (2004) Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiol Ecol 50:231–243
Massana R, Terrado R, Forn I et al (2006) Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ Microbiol 8:1515–1522
Massana R, Unrein F, Rodríguez-Martínez R et al (2009) Grazing rates and functional diversity of uncultured heterotrophic flagellates. ISME J 3:588–596
Massana R, del Campo J, Sieracki ME et al (2014) Exploring the uncultured microeukaryote majority in the oceans: reevaluation of ribogroups within stramenopiles. ISME J 8:854–866
Massana R, Gobet A, Audic S et al (2015) Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing. Environ Microbiol 17:4035–4049
Mast SO (1947) The food-vacuole in paramecium. Biol Bull 92:31–72
Matz C, Boenigk J, Arndt H, Jürgens K (2002) Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat Microb Ecol 27:137–148
Maumus F, Epert A, Nogué F, Blanc G (2014) Plant genomes enclose footprints of past infections by giant virus relatives. Nat Commun 5:4268
Mayer JA, Taylor FJR (1979) A virus which lyses the marine nanoflagellate Micromonas pusilla. Nature 281:299–301
Mayr E (1996) What is a species, and what is not? Phil Sci 63:262–277
McClanahan TR, Marnane MJ, Cinner JE, Kiene WE (2006) A comparison of marine protected areas and alternative approaches to coral-reef management. Curr Biol 16:1408–1413
McFadden GI, Reith ME, Munholland J, Lang-Unnasch N (1996) Plastid in human parasites. Nature 381:482
McFall-Ngai MJ (2014) The importance of microbes in animal development: lessons from the squid-vibrio symbiosis. Annu Rev Microbiol 68:177–194
McRose D, Guo J, Monier A et al (2014) Alternatives to vitamin B 1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages. ISME J 8:2517–2529
Medina LE, Taylor CD, Pachiadaki MG et al (2017) A review of protist grazing below the photic zone emphasizing studies of oxygen-depleted water columns and recent applications of in situ approaches. Front Mar Sci 4:105
Medlin LK, Sáez AG, Young JR (2008) A molecular clock for coccolithophores and implications for selectivity of phytoplankton extinctions across the K/T boundary. Mar Micropaleontol 67:69–86
Meints RH, Ivey RG, Lee AM, Choi T-J (2008) Identification of two virus integration sites in the brown alga Feldmannia chromosome. J Virol 82:1407–1413
Mendes CRB, Tavano VM, Dotto TS et al (2018) New insights on the dominance of cryptophytes in Antarctic coastal waters: A case study in Gerlache Strait. Deep Sea Res Part 2 Top Stud Oceanogr 149:161–170
Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biologisches Centralblatt 25:293–604
Meyen FJF (1834) Reise um die Erde: ausgeführt auf dem königlich preussischen Seehandlungs-Schiffe Prinzess Louise, commandirt von Captain W. Wendt, in den Jahren 1830, 1831 und 1832. Sander’sche buchhandlung
Meyer-Abich A (1943) I. Das typologische Grundgesetz und seine Folgerungen für Phylogenie und Entwicklungsphysiologie. Acta Biotheor 7:1–80
Mihara T, Koyano H, Hingamp P et al (2018) Taxon richness of “Megaviridae” exceeds those of bacteria and archaea in the ocean. Microbes Environ 33:162–171
Mitra A, Flynn KJ, Burkholder JM et al (2014) The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11:995–1005
Mitra A, Flynn KJ, Tillmann U et al (2016) Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: incorporation of diverse mixotrophic strategies. Protist 167:106–120
Mock T, Otillar RP, Strauss J et al (2017) Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature 541:536–540
Moeller HV, Neubert MG, Johnson MD (2019) Intraguild predation enables coexistence of competing phytoplankton in a well-mixed water column. Ecology 100:e02874
Mojica KDA, Huisman J, Wilhelm SW, Brussaard CPD (2016) Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean. ISME J 10:500–513
Monger BC, Landry MR (1991) Prey-size dependency of grazing by free-living marine flagellates. Mar Ecol Prog Ser 74:239–248
Monier A, Worden AZ, Richards TA (2016) Phylogenetic diversity and biogeography of the Mamiellophyceae lineage of eukaryotic phytoplankton across the oceans. Environ Microbiol Rep 8:461–469
Monier A, Chambouvet A, Milner DS et al (2017) Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton. Proc Natl Acad Sci 114:E7489–E7498
Monteil CL, Vallenet D, Menguy N et al (2019) Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist. Nat Microbiol 4:1088–1095
Monteiro FM, Follows MJ, Dutkiewicz S (2010) Distribution of diverse nitrogen fixers in the global ocean. Global Biogeochem Cycles 24:GB3017
Moodley L, Middelburg JJ, Boschker HTS et al (2002) Bacteria and foraminifera: key players in a short-term deep-sea benthic response to phytodetritus. Mar Ecol Prog Ser 236:23–29
Moon-van der Staay SY, De Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607–610
Moore RB, Oborník M, Janouskovec J et al (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963
Mordret S, Romac S, Henry N et al (2016) The symbiotic life of Symbiodinium in the open ocean within a new species of calcifying ciliate (Tiarina sp.). ISME J 10:1424–1436
Moreau H, Verhelst B, Couloux A et al (2012) Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage. Genome Biol 13:R74
Moreira D, López-García P (2014) The rise and fall of Picobiliphytes: how assumed autotrophs turned out to be heterotrophs. BioEssays 36:468–474
Mougari S, Sahmi-Bounsiar D, Levasseur A et al (2019) Virophages of giant viruses: an update at eleven. Viruses 11:733
Murphy LS, Haugen EM (1985) The distribution and abundance of phototrophic ultraplankton in the North Atlantic. Limnol Oceanogr 30:47–58
Needham DM, Fuhrman JA (2016) Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nature Microbiol 1:16005–16005
Needham DM, Sachdeva R, Fuhrman JA (2017) Ecological dynamics and co-occurrence among marine phytoplankton, bacteria and myoviruses shows microdiversity matters. ISME J 11:1614–1629
Needham DM, Fichot EB, Wang E et al (2018) Dynamics and interactions of highly resolved marine plankton via automated high frequency sampling. ISME J 12:2417–2432
Needham DM, Poirier C, Hehenberger E et al (2019a) Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes. Phil Trans R Soc Lond B 374:20190086
Needham DM, Yoshizawa S, Hosaka T et al (2019b) A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. Proc Natl Acad Sci 116:20574–20583
Neuer S, Cowles TJ (1994) Protist herbivory in the Oregon upwelling system. Mar Ecol Prog Ser 113:147–162
Nielsen LT, Kiørboe T (2021) Foraging trade-offs, flagellar arrangements, and flow architecture of planktonic protists. Proc Natl Acad Sci 118:e2009930118
Nielsen LT, Asadzadeh SS, Dölger J et al (2017) Hydrodynamics of microbial filter feeding. Proc Natl Acad Sci 114:9373–9378
Nöel M-H, Kawachi M, Inouye I (2004) Induced dimorphic life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea (Prymnesiophyceae, Haptophyta). J Phycol 40:112–129
Not F, Gausling R, Azam F et al (2007a) Vertical distribution of picoeukaryotic diversity in the Sargasso Sea. Environ Microbiol 9:1233–1252
Not F, Valentin K, Romari K et al (2007b) Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science 315:253–255
Nowack ECM, Melkonian M, Glöckner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18:410–418
Nyholm SV, McFall-Ngai M (2004) The winnowing: establishing the squid–vibrio symbiosis. Nat Rev Microbiol 2:632–642
O’Malley MA (2007) The nineteenth century roots of “everything is everywhere.”. Nat Rev Microbiol 5:647–651
O’Malley MA, Leger MM, Wideman JG, Ruiz-Trillo I (2019) Concepts of the last eukaryotic common ancestor. Nat Ecol Evol 3:338–344
Oikonomou CM, Chang Y-W, Jensen GJ (2016) A new view into prokaryotic cell biology from electron cryotomography. Nat Rev Microbiol 14:205–220
Ollison GA, Hu SK, Mesrop LY et al (2021) Come rain or shine: depth not season shapes the active protistan community at station ALOHA in the North Pacific subtropical gyre. Deep-Sea Res I Oceanogr Res Pap 170:103494
Olson MB, Strom SL (2002) Phytoplankton growth, microzooplankton herbivory and community structure in the southeast Bering Sea: insight into the formation and temporal persistence of an Emiliania huxleyi bloom. Deep Sea Res Part 2 Top Stud Oceanogr 49:5969–5990
Omand MM, D’Asaro EA, Lee CM et al (2015) Eddy-driven subduction exports particulate organic carbon from the spring bloom. Science 348:222–225
Orcutt BN, Sylvan JB, Knab NJ, Edwards KJ (2011) Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol Mol Biol Rev 75:361–422
Orsi W, Song YC, Hallam S, Edgcomb V (2012) Effect of oxygen minimum zone formation on communities of marine protists. ISME J 6:1586–1601
Orsi WD, Wilken S, Del Campo J et al (2018) Identifying protist consumers of photosynthetic picoeukaryotes in the surface ocean using stable isotope probing. Environ Microbiol 20:815–827
Paasche E (2001) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40:503–529
Paerl RW, Sundh J, Tan D et al (2018) Prevalent reliance of bacterioplankton on exogenous vitamin B1 and precursor availability. Proc Natl Acad Sci 115:E10447–E10456
Palenik B, Morel FMM (1990) Amino acid utilization by marine phytoplankton: A novel mechanism. Limnol Oceanogr 35:260–269
Pančić M, Kiørboe T (2018) Phytoplankton defence mechanisms: traits and trade-offs. Biol Rev Camb Philos Soc 93:1269–1303
Pančić M, Torres RR, Almeda R, Kiørboe T (2019) Silicified cell walls as a defensive trait in diatoms. Proc Biol Sci 286:20190184
Parfrey LW, Lahr DJG (2013) Multicellularity arose several times in the evolution of eukaryotes (response to DOI https://doi.org/10.1002/bies.201100187). BioEssays 35:339–347
Park MG, Kim S, Kim HS et al (2006) First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat Microb Ecol 45:101–106
Parke M, Manton I (1967) The specific identity of the algal symbiont in Convoluta roscoffensis. J Mar Biol Assoc 47:445–464
Pasulka AL, Landry MR, Taniguchi DAA et al (2013) Temporal dynamics of phytoplankton and heterotrophic protists at station ALOHA. Deep Sea Res Part 2 Top Stud Oceanogr 93:44–57
Patron NJ, Waller RF (2007) Transit peptide diversity and divergence: A global analysis of plastid targeting signals. BioEssays 29:1048–1058
Patyshakuliyeva A, Falkoski DL, Wiebenga A et al (2019) Macroalgae derived fungi have high abilities to degrade algal polymers. Microorganisms 8:52
Paulmier A, Ruiz-Pino D (2009) Oxygen minimum zones (OMZs) in the modern ocean. Prog Oceanogr 80:113–128
Pernice MC, Forn I, Gomes A et al (2015) Global abundance of planktonic heterotrophic protists in the deep ocean. ISME J 9:782–792
Pernice MC, Giner CR, Logares R et al (2016) Large variability of bathypelagic microbial eukaryotic communities across the world’s oceans. ISME J 10:945–958
Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3:537–546
Peter KH, Sommer U (2013) Phytoplankton cell size reduction in response to warming mediated by nutrient limitation. PLoS One 8:e71528
Pettitt ME, Orme BAA, Blake JR, Leadbeater BSC (2002) The hydrodynamics of filter feeding in choanoflagellates. Eur J Protistol 38:313–332
Philippe H, Brinkmann H, Lavrov DV et al (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602
Piganeau G, Eyre-Walker A, Jancek S et al (2011) How and why DNA barcodes underestimate the diversity of microbial eukaryotes. PLoS One 6:e16342
Pita L, Rix L, Slaby BM et al (2018) The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46
Pitta P, Karakassis I (2005) Size distribution in ultraphytoplankton: a comparative analysis of counting methods. Environ Monit Assess 102:85–101
Piwosz K, Mukherjee I, Salcher MM et al (2021) CARD-FISH in the sequencing era: opening a new universe of protistan ecology. Front Microbiol 12:397
Pizay M-D, Lemée R, Simon N et al (2009) Night and day morphologies in a planktonic dinoflagellate. Protist 160:565–575
Planavsky NJ, Crowe SA, Fakhraee M et al (2021) Evolution of the structure and impact of Earth’s biosphere. Nature Rev Earth Environment 2:123–139
Pomeroy LR (1974) The ocean’s food web, a changing paradigm. Bioscience 24:499–504
Pontasch S, Scott A, Hill R et al (2014) Symbiodinium diversity in the sea anemone Entacmaea quadricolor on the east Australian coast. Coral Reefs 33:537–542
Preisig HR (1994) Siliceous structures and silicification in flagellated protists. In: Wetherbee R, Pickett-Heaps JD, Andersen RA (eds) The Protistan cell surface. Springer Vienna, Vienna, pp 29–42
Pride DT, Sun CL, Salzman J et al (2010) Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 21:126–136
Priest T, Fuchs B, Amann R, Reich M (2021) Diversity and biomass dynamics of unicellular marine fungi during a spring phytoplankton bloom. Environ Microbiol 23:448–463
Pringsheim EG (1958) Über Mixotrophie bei Flagellaten. Planta 52:405–430
Proctor LM, Fuhrman JA (1990) Viral mortality of marine bacteria and cyanobacteria. Nature 343:60–62
Raghukumar S (2002) Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Eur J Protistol 38:127–145
Raina J-B, Fernandez V, Lambert B et al (2019) The role of microbial motility and chemotaxis in symbiosis. Nat Rev Microbiol 17:284–294
Raoult D, Audic S, Robert C et al (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306:1344–1350
Raven JA (1998) The twelfth Tansley lecture. Small is beautiful: the picophytoplankton. Funct Ecol 12:503–513
Raven J, Caldeira K, Elderfield H, et al. (2005) Ocean acidification due to increasing atmospheric carbon dioxide The Royal Society Policy Document 12/05
Read BA, Kegel J, Klute MJ et al (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–213
Record NR, Pershing AJ, Maps F (2013) The paradox of the “paradox of the plankton.”. ICES J Mar Sci 71:236–240
Reynolds N (1973) The estimation of the abundance of ultraplankton. Br Phycol J 8:135–146
Richards TA, Talbot NJ (2018) Osmotrophy. Curr Biol 28:R1179–R1180
Richards TA, Dacks JB, Jenkinson JM et al (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 16:1857–1864
Richards TA, Jones MDM, Leonard G, Bass D (2012) Marine fungi: their ecology and molecular diversity. Annu Rev Mar Sci 4:495–522
Richards TA, Leonard G, Mahé F et al (2015) Molecular diversity and distribution of marine fungi across 130 European environmental samples. Proc Biol Sci 282:20152243
Richter DJ, Fozouni P, Eisen M, King N (2018) Gene family innovation, conservation and loss on the animal stem lineage. elife 7:e34226–e34226
Roberts EC, Legrand C, Steinke M, Wootton EC (2011) Mechanisms underlying chemical interactions between predatory planktonic protists and their prey. J Plankton Res 33:833–841
Rocke E, Pachiadaki MG, Cobban A et al (2015) Protist community grazing on prokaryotic prey in deep ocean water masses. PLoS One 10:e0124505
Rodríguez-Martínez R, Leonard G, Milner DS et al (2020) Controlled sampling of ribosomally active protistan diversity in sediment-surface layers identifies putative players in the marine carbon sink. ISME J 14:984–998
Roger Anderson O, Be AWH (1976) The ultrastructure of a planktonic foraminifer, Globigerinoides sacculifer (Brady), and its symbiotic dinoflagellates. J Foraminiferal Res 6:1–21
Ros-Rocher N, Pérez-Posada A, Leger MM, Ruiz-Trillo I (2021) The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition. Open Biol 11:200359
Rothhaupt KO (1996a) Utilization of substitutable carbon and phosphorus sources by the mixotrophic chrysophyte Ochromonas sp. Ecology 77:706–715
Rothhaupt KO (1996b) Laboratorary experiments with a mixotrophic chrysophyte and obligately phagotrophic and photographic competitors. Ecology 77:716–724
Roy S, Chattopadhyay J (2007) Towards a resolution of “the paradox of the plankton”: A brief overview of the proposed mechanisms. Ecol Complex 4:26–33
Ruardij P, Veldhuis MJW, Brussaard CPD (2005) Modeling the bloom dynamics of the polymorphic phytoplankter Phaeocystis globosa: impact of grazers and viruses. Harmful Algae 4:941–963
Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:225–274
Sala E, Mayorga J, Bradley D et al (2021) Protecting the global ocean for biodiversity, food and climate. Nature 592:297–402
Samadi S, Barberousse A (2006) The tree, the network, and the species. Biol J Linn Soc Lond 89:509–521
Sánchez-Baracaldo P, Cardona T (2020) On the origin of oxygenic photosynthesis and cyanobacteria. New Phytol 225:1440–1446
Sarno D, Kooistra WHCF, Medlin LK et al (2005) Diversity in the genus Skeletonema (Bacillariophyceae). An assessment of the taxonomy of Costatum-like species with the description of four new species. J Phycol 41:151–176
Schaffelke B, Heimann K, Marshall PA, Ayling AM (2004) Blooms of Chrysocystis fragilis on the great barrier reef. Coral Reefs 23:514–514
Schmoker C, Hernández-León S, Calbet A (2013) Microzooplankton grazing in the oceans: impacts, data variability, knowledge gaps and future directions. J Plankton Res 35:691–706
Schoemann V, Becquevort S, Stefels J, et al. (2005) Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res 53:43–66
Scholz B, Küpper FC, Vyverman W, Karsten U (2014) Eukaryotic pathogens (Chytridiomycota and Oomycota) infecting marine microphytobenthic diatoms – a methodological comparison. J Phycol 50:1009–1019
Scholz B, Vyverman W, Küpper FC et al (2017) Effects of environmental parameters on chytrid infection prevalence of four marine diatoms: a laboratory case study. Bot Mar 60:419–431
Schroeder DC, Oke J, Hall M et al (2003) Virus succession observed during an Emiliania huxleyi bloom. Appl Environ Microbiol 69:2484–2490
Schulz F, Yutin N, Ivanova NN et al (2017) Giant viruses with an expanded complement of translation system components. Science 356:82–85
Schvarcz CR, Steward GF (2018) A giant virus infecting green algae encodes key fermentation genes. Virology 518:423–433
Seeleuthner Y, Mondy S, Lombard V et al (2018) Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans. Nat Commun 9:310
Seenivasan R (2013) Identification of a new eukaryotic phylum “Picozoa” in the oceanic environment. Doctoral Thesis, Universität zu Köln
Seenivasan R, Sausen N, Medlin LK, Melkonian M (2013) Picomonas judraskeda gen. et sp. nov.: the first identified member of the Picozoa phylum nov., a widespread group of picoeukaryotes, formerly known as “picobiliphytes.” PLoS ONE 8:e59565
Sellers CG, Gast RJ, Sanders RW (2014) Selective feeding and foreign plastid retention in an Antarctic dinoflagellate. J Phycol 50:1081–1088
Ševčíková T, Horák A, Klimeš V et al (2015) Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci Rep 5:10134
Seymour JR, Amin SA, Raina J-B, Stocker R (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2:17065
Sharma V, Colson P, Giorgi R et al (2014) DNA-dependent RNA polymerase detects hidden giant viruses in published databanks. Genome Biol Evol 6:1603–1610
Sharon I, Alperovitch A, Rohwer F et al (2009) Photosystem I gene cassettes are present in marine virus genomes. Nature 461:258–262
Sherr E, Sherr B (1988) Role of microbes in pelagic food webs: A revised concept. Limnol Oceanogr 33:1225–1227
Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Ant Leeuwenhoek 81:293–308
Sherr EB, Sherr BF (2007) Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar Ecol Prog Ser 352:187–197
Short SM (2012) The ecology of viruses that infect eukaryotic algae. Environ Microbiol 14:2253–2271
Sibbald SJ, Archibald JM (2020) Genomic insights into plastid evolution. Genome Biol Evol 12:978–990
Sieburth JM, Smetacek V, Lenz J (1978) Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol Oceanogr 23:1256–1263
Sieracki ME, Poulton NJ, Jaillon O et al (2019) Single cell genomics yields a wide diversity of small planktonic protists across major ocean ecosystems. Sci Rep 9:6025
Silva PC (2008) Historical review of attempts to decrease subjectivity in species identification, with particular regard to algae. Protist 159:153–161
Simmons MP, Bachy C, Sudek S et al (2015) Intron invasions trace algal speciation and reveal nearly identical Arctic and Antarctic Micromonas populations. Mol Biol Evol 32:2219–2235
Simmons MP, Sudek S, Monier A et al (2016) Abundance and biogeography of picoprasinophyte ecotypes and other phytoplankton in the eastern North Pacific Ocean. Appl Environ Microbiol 82:1693–1705
Simon M, López-García P, Deschamps P et al (2015) Marked seasonality and high spatial variability of protist communities in shallow freshwater systems. ISME J 9:1941–1953
Simon J-C, Marchesi JR, Mougel C, Selosse M-A (2019) Host-microbiota interactions: from holobiont theory to analysis. Microbiome 7:5
Simpson AGB, Roger AJ (2004) The real “kingdoms” of eukaryotes. Curr Biol 14:R693–R696
Smetacek V (1999) Revolution in the ocean. Nature 401:647–647
Sogin ML (2015) Evolution of eukaryotic microorganisms and their small subunit ribosomal RNAs1. Integr Comp Biol 29:487–499
Sogin ML, Morrison HG, Huber JA et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere.”. Proc Natl Acad Sci 103:12115–12120
Soucy SM, Huang J, Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482
Sournia A, Chrdtiennot-Dinet M-J, Ricard M (1991) Marine phytoplankton: how many species in the world ocean? J Plankton Res 13:1093–1099
Spang A, Saw JH, Jørgensen SL et al (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179
Stanier RY, Van Niel CB (1962) The concept of a bacterium. Arch Mikrobiol 42:17–35
Steele JA, Countway PD, Xia LC et al (2011) Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J 5:1414–1425
Steinberg DK, Landry MR (2017) Zooplankton and the ocean carbon cycle. Annu Rev Mar Sci 9:413–444
Steinberg DK, Carlson CA, Bates NR et al (2001) Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep Sea Res Part 2 Top Stud Oceanogr 48:1405–1447
Steward GF, Culley AI, Mueller JA et al (2013) Are we missing half of the viruses in the ocean? ISME J 7:672–679
Stiller JW, Schreiber J, Yue J et al (2014) The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat Commun 5:5764
Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol 34:281–290
Stoecker DK, Silver MW, Michaels AE, Davis LH (1988) Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, oligo trichida). Mar Microb Food Webs 3:79–100
Stoecker DK, Hansen PJ, Caron DA, Mitra A (2017) Mixotrophy in the marine plankton. Annu Rev Mar Sci 9:311–335
Strassert JFH, Karnkowska A, Hehenberger E et al (2018) Single cell genomics of uncultured marine alveolates shows paraphyly of basal dinoflagellates. ISME J 12:304–308
Strassert JFH, Jamy M, Mylnikov AP et al (2019) New phylogenomic analysis of the enigmatic phylum Telonemia further resolves the eukaryote tree of life. Mol Biol Evol 36:757–765
Suda S, Watanabe MM, Inouye I (1989) Evidence for sexual reproduction in the primitive green alga Nephroselmis olivacea (Prasinophyceae). J Phycol 25:596–600
Suttle CA, Chan AM, Cottrell MT (1990) Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467–469
Sweeney BM (1976) Pedinomonas noctilucae (Prasinophyceae), the flagellate symbiotic in Noctiluca flagellate symbiotic in Noctiluca (Dinophyceae) in Southeast Asia. J Phycol 12:460–464
Takahashi M, Bienfang PK (1983) Size structure of phytoplankton biomass and photosynthesis in subtropical Hawaiian waters. Mar Biol 76:203–211
Taylor FJRM (2003) The collapse of the two-kingdom system, the rise of protistology and the founding of the International Society for Evolutionary Protistology (ISEP). Int J Syst Evol Microbiol 53:1707–1714
Taylor DL, Lee CC (1971) A new cryptomonad from Antarctica: Cryptomonas cryophila sp. nov. Arch Mikrobiol 75:269–280
Taylor BP, Cortez MH, Weitz JS (2014) The virus of my virus is my friend: ecological effects of virophage with alternative modes of coinfection. J Theor Biol 354:124–136
Taylor AR, Brownlee C, Wheeler G (2017) Coccolithophore cell biology: chalking up progress. Annu Rev Mar Sci 9:283–310
Taylor BP, Weitz JS, Brussaard CPD, Fischer MG (2018) Quantitative infection dynamics of cafeteria Roenbergensis virus. Viruses 10:468
Teeling H, Fuchs BM, Becher D et al (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611
Thines M (2018) Oomycetes. Curr Biol 28:R812–R813
Thompson JR, Rivera HE, Closek CJ, Medina M (2014) Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol 4:176
Tikhonenkov DV (2020) Predatory flagellates – the new recently discovered deep branches of the eukaryotic tree and their evolutionary and ecological significance. Protistology 14:15–22
Tikhonenkov DV, Hehenberger E, Esaulov AS et al (2020a) Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals. BMC Biol 18:39
Tikhonenkov DV, Strassert JFH, Janouškovec J et al (2020b) Predatory colponemids are the sister group to all other alveolates. Mol Phylogenet Evol 149:106839
Tikhonenkov DV, Gawryluk RMR, Mylnikov AP, Keeling PJ (2021) First finding of free-living representatives of Prokinetoplastina and their nuclear and mitochondrial genomes. Sci Rep 11:2946
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135
Tischler AH, Hodge-Hanson KM, Visick KL (2019) Vibrio fischeri–squid symbiosis. Encyclopedia Life Sci. https://doi.org/10.1002/9780470015902.a0028395
Tizard TH, Moseley HN, Buchanan JY, Murray J (1885) Narrative of the cruise of HMS challenger with a general account of the scientific results of the expedition. Report on the scientific results of the voyage of HMS challenger during the years 1873-76. Narrative 1:511–1110
Tragin M, Vaulot D (2018) Green microalgae in marine coastal waters: the ocean sampling day (OSD) dataset. Sci Rep 8:14020
Tragin M, Lopes dos Santos A, Christen R, Vaulot D (2016) Diversity and ecology of green microalgae in marine systems: an overview based on 18S rRNA gene sequences. Perspect Phycol 3:141–154
Treusch AH, Vergin KL, Finlay LA et al (2009) Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3:1148–1163
Treusch AH, Demir-Hilton E, Vergin KL et al (2011) Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids. ISME J 6:481–492
Unrein F, Massana R, Alonso-Sáez L, Gasol JM (2007) Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Oceanogr 52:456–469
Unrein F, Gasol JM, Not F et al (2014) Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters. ISME J 8:164–176
Urayama S-I, Takaki Y, Nishi S et al (2018) Unveiling the RNA virosphere associated with marine microorganisms. Mol Ecol Resources 18:1444–1455
van de Guchte M, Blottière HM, Doré J (2018) Humans as holobionts: implications for prevention and therapy. Microbiome 6:81
Van Donk E, Ianora A, Vos M (2011) Induced defences in marine and freshwater phytoplankton: a review. Hydrobiologia 668:3–19
Van Etten JL, Agarkova I, Dunigan DD et al (2017) Chloroviruses have a sweet tooth. Viruses 9:88
Van Leeuwenhoek A (1677) Observations, communicated to the publisher by Mr. Antony van Leewenhoeck, in a dutch letter of the 9th Octob. 1676. Here English’d: concerning little animals by him observed in rain-well-sea-and snow water; as also in water wherein pepper had lain infused. Philos Trans R Soc Lond 12:821–831
Van Steenkiste NWL, Stephenson I, Herranz M et al (2019) A new case of kleptoplasty in animals: marine flatworms steal functional plastids from diatoms. Sci Adv 5:eaaw4337
van Tatenhove-Pel RJ, Rijavec T, Lapanje A et al (2021) Microbial competition reduces metabolic interaction distances to the low μm-range. ISME J 15:688–701
Vannier T, Leconte J, Seeleuthner Y et al (2016) Survey of the green picoalga Bathycoccus genomes in the global ocean. Sci Rep 6:37900
Vardi A, Haramaty L, Van Mooy BAS et al (2012) Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proc Natl Acad Sci 109:19327–19332
Vellai T, Vida G (1999) The origin of eukaryotes: the difference between prokaryotic and eukaryotic cells. Proc Biol Sci 266:1571–1577
Villa Martín P, Buček A, Bourguignon T, Pigolotti S (2020) Ocean currents promote rare species diversity in protists. Sci Adv 6:eaaz9037
von Linné C (1735) Systema naturae; sive, Regna tria naturae: systematice proposita per classes, ordines, genera & species. Haak
Waller RF, Kořený L (2017) Plastid complexity in dinoflagellates: a picture of gains, losses, replacements and revisions. In: Hirakawa Y (ed) Advances in botanical research. Academic Press, Oxford, pp 105–143
Wang AL, Wang CC (1991) Viruses of the protozoa. Annu Rev Microbiol 45:251–263
Wang L, Lin X, Goes JI, Lin S (2016) Phylogenetic analyses of three genes of Pedinomonas noctilucae, the green endosymbiont of the marine dinoflagellate Noctiluca scintillans, reveal its affiliation to the order Marsupiomonadales (Chlorophyta, Pedinophyceae) under the reinstated name Protoeuglena noctilucae. Protist 167:205–216
Wang Y, Fan X, Gao G et al (2020) Decreased motility of flagellated microalgae long-term acclimated to CO2-induced acidified waters. Nature Clim Change 10:561–567
Ward BA, Follows MJ (2016) Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc Natl Acad Sci 113:2958–2963
Wassmann P (2015) Overarching perspectives of contemporary and future ecosystems in the Arctic Ocean. Prog Oceanogr 139:1
Wessenberg H, Antipa G (1970) Capture and ingestion of Paramecium by Didinium nasutum. J Protozool 17:250–270
Wetherbee R, Bringloe TT, Costa JF et al (2020) New pelagophytes show a novel mode of algal colony development and reveal a perforated theca that may define the class. J Phycol 57:396–411
Weynberg KD (2018) Viruses in marine ecosystems: from open waters to coral reefs. Adv Virus Res 101:1–38
Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci 95:6578–6583
Whittaker RH (1969) New concepts of kingdoms or organisms. Evolutionary relations are better represented by new classifications than by the traditional two kingdoms. Science 163:150–160
Wideman JG, Lax G, Leonard G et al (2019) A single-cell genome reveals diplonemid-like ancestry of kinetoplastid mitochondrial gene structure. Phil Trans R Soc Lond B 374:20190100
Wideman JG, Monier A, Rodríguez-Martínez R et al (2020) Unexpected mitochondrial genome diversity revealed by targeted single-cell genomics of heterotrophic flagellated protists. Nat Microbiol 5:154–165
Wilken S, Verspagen JMH, Naus-Wiezer S et al (2014) Comparison of predator-prey interactions with and without intraguild predation by manipulation of the nitrogen source. Oikos 123:423–432
Wilken S, Yung CCM, Hamilton M et al (2019) The need to account for cell biology in characterizing predatory mixotrophs in aquatic environments. Phil Trans R Soc Lond B 374:20190090
Wilken S, Choi CJ, Worden AZ (2020) Contrasting mixotrophic lifestyles reveal different ecological niches in two closely related marine protists. J Phycol 56:52–67
Wiltshire KH, Malzahn AM, Wirtz K et al (2008) Resilience of North Sea phytoplankton spring bloom dynamics: an analysis of long-term data at Helgoland roads. Limnol Oceanogr 53:1294–1302
Wolf YI, Silas S, Wang Y et al (2020) Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome. Nat Microbiol 5:1262–1270
Worden AZ, Nolan JK, Palenik B (2004) Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnol Oceanogr 49:168–179
Worden AZ, Lee J-H, Mock T et al (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272
Worden AZ, Janouskovec J, McRose D et al (2012) Global distribution of a wild alga revealed by targeted metagenomics. Curr Biol 22:R675–R677
Worden AZ, Follows MJ, Giovannoni SJ et al (2015) Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347:1257594–1257594
Woznica A, Cantley AM, Beemelmanns C et al (2016) Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc Natl Acad Sci 113:7894–7899
Woznica A, Gerdt JP, Hulett RE et al (2017) Mating in the closest living relatives of animals is induced by a bacterial chondroitinase. Cell 170:1175–1183
Wright D (2017) Swells, soundings, and sustainability, but…“here be monsters.”. Oceanography 30:209–221
Wu W, Huang B (2019) Protist diversity and community assembly in surface sediments of the South China Sea. Microbiol Open 8:e891
Yau S, Lauro FM, DeMaere MZ et al (2011) Virophage control of antarctic algal host–virus dynamics. Proc Natl Acad Sci 108:6163–6168
Yoon HS, Price DC, Stepanauskas R et al (2011) Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332:714–717
Yutin N, Koonin EV (2012) Proteorhodopsin genes in giant viruses. Biol Direct 7:34–34
Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358
Zavarzina NB, Protsenko AE (1958) On lysis of cultures Chlorella pyrenoidosa Pringsheim. Dokl Akad Nauk SSSR
Zeigler Allen L, McCrow JP, Ininbergs K et al (2017) The Baltic Sea virome: diversity and transcriptional activity of DNA and RNA viruses. mSystems 2:e00125–e00116
Zimmerman AE, Howard-Varona C, Needham DM et al (2020) Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat Rev Microbiol 18:21–34
Zoccarato L, Pallavicini A, Cerino F et al (2016) Water mass dynamics shape Ross Sea protist communities in mesopelagic and bathypelagic layers. Prog Oceanogr 149:16–26
Zubkov MV, Tarran GA (2008) High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455:224–226
Acknowledgements
We thank our various mentors and lab colleagues over the years who have inspired and challenged us to take on new ways of thinking. We thank the funding sources that have supported our research and time in writing this book chapter, especially the Dutch Research Council (NWO) Vidi grant VI.Vidi.193.101 (to SW), Gordon and Betty Moore Foundation 3788 and NSF DEB-1639033 (to AZW) and availability of data generated under the Simons Foundation International’s BIOS-SCOPE program. AZW thanks the Hanse Wissenschaftskolleg (Delmenhorst Germany) and the Radcliffe Institute for Advanced Studies at Harvard (Cambridge, MA, USA) for fellowships that have facilitated thought on these topics. We also thank Lucas J. Stal, Mariana Silvia Cretoiu, and other chapter authors for their understanding of the challenges posed in completing this work with young children at home during the COVID epidemic, as was the case for multiple authors.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Bachy, C. et al. (2022). Marine Protists: A Hitchhiker’s Guide to their Role in the Marine Microbiome. In: Stal, L.J., Cretoiu, M.S. (eds) The Marine Microbiome. The Microbiomes of Humans, Animals, Plants, and the Environment, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-030-90383-1_4
Download citation
DOI: https://doi.org/10.1007/978-3-030-90383-1_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-90382-4
Online ISBN: 978-3-030-90383-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)