Skip to main content

Advertisement

SpringerLink
Log in

Chemical Mediation of Ternary Interactions Between Marine Holobionts and Their Environment as Exemplified by the Red Alga Delisea pulchra

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The need for animals and plants to control microbial colonization is important in the marine environment with its high densities of microscopic propagules and seawater that provides an ideal medium for their dispersal. In contrast to the traditional emphasis on antagonistic interactions of marine organisms with microbes, emerging studies lend support to the notion that health and performance of many marine organisms are functionally regulated and assisted by associated microbes, an ecological concept defined as a holobiont. While antimicrobial activities of marine secondary metabolites have been studied in great depth ex-situ, we are beginning to understand how some of these compounds function in an ecological context to maintain the performance of marine holobionts. The present article reviews two decades of our research on the red seaweed Delisea pulchra by addressing: the defense chemistry of this seaweed; chemically-mediated interactions between the seaweed and its natural enemies; and the negative influence of elevated seawater temperature on these interactions. Our understanding of these defense compounds and the functional roles they play for D. pulchra extends from molecular interactions with bacterial cell signaling molecules, to ecosystem-scale consequences of chemically-controlled disease and herbivory. Delisea pulchra produces halogenated furanones that antagonize the same receptor as acylated homoserine lactones (AHL)—a group of widespread intercellular communication signals among bacteria. Halogenated furanones compete with and inhibit bacterial cell-to-cell communication, and thus interfere with important bacterial communication-regulated processes, such as biofilm formation. In a predictable pattern that occurs at the ecological level of entire populations, environmental stress interferes with the production of halogenated furanones, causing downstream processes that ultimately result in disease of the algal holobiont.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amsler, C. D. (ed.) 2008. Algal Chemical Ecology. Springer, Berlin.

    Google Scholar 

  • Atkinson, S. and Williams, P. 2009. Quorum sensing and social networking in the microbial world. J. R. Soc. Interface 6:959–978.

    Article  PubMed  CAS  Google Scholar 

  • Barott, K. L., Rodriguez-Brito, B., Janouskovec, J., Marhaver, K. L., Smith, J. E., Keeling, P., and Rohwer, F. L. 2011. Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ. Microbiol. 13:1192–1204.

    Article  PubMed  CAS  Google Scholar 

  • Bourne, D. G., Garren, M., Work, T. M., Rosenberg, E., Smith, G. W., and Harvell, C. D. 2009. Microbial disease and the coral holobiont. Trends Microbiol. 17:554–562.

    Article  PubMed  CAS  Google Scholar 

  • Breitbart, M., Bhagooli, R., Griffin, S., Johnston, I., and Rohwer, F. 2005. Microbial communities associated with skeletal tumors on Porites compressa. FEMS Microbiol. Lett. 243:431–436.

    Article  PubMed  CAS  Google Scholar 

  • Burke, C., Steinberg, P., Rusch, D., Kjelleberg, S., and Thomas, T. 2011a. Bacterial community assembly based on functional genes rather than species. Proc. Natl. Acad. Sci. U.S.A. 108:14288–14293.

    Article  PubMed  CAS  Google Scholar 

  • Burke, C., Thomas, T., Lewis, M., Steinberg, P., and Kjelleberg, S. 2011b. Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J. 5:590–600.

    Article  PubMed  CAS  Google Scholar 

  • Campbell, A. H. 2011. The ecology of bacterially-mediated bleaching in a chemically-defended seaweed. PhD dissertation. University of New South Wales, Sydney.

    Google Scholar 

  • Campbell, A. H., Harder, T., Nielsen, S., Kjelleberg, S., and Steinberg, P. D. 2011. Climate change and disease: bleaching of a chemically defended seaweed. Glob. Chang. Biol. 17:2958–2970.

    Article  Google Scholar 

  • Case, R. J., Longford, S. R., Campbell, A. H., Low, A., Tujula, N., Steinberg, P. D., and Kjelleberg, S. 2011. Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environ. Microbiol. 13:529–537.

    Article  PubMed  CAS  Google Scholar 

  • CEBRIAN, E., URIZ, M. J., GARRABOU, J., and BALLESTEROS, E. 2011. Sponge mass mortalities in a warming mediterranean sea: are cyanobacteria-harboring species worse off? Plos One 6.

  • Cole, R. G. and Babcock, R. C. 1996. Mass mortality of a dominant kelp (Laminariales) at Goat Island, North-eastern New Zealand. Mar. Freshw. Res. 47:907–911.

    Article  Google Scholar 

  • Coleman, M. A., Kelaher, B. P., Steinberg, P. D., and MILLAR, A. J. K. 2008. Absence of a large brown macroalga on urbanised reefs around Sydney, Australia and evidence for historical decline. J. Phycol. 44:897–901.

    Article  Google Scholar 

  • Connell, S. D., Russel, B. D., Turner, D. J., Sheperd, S. A., Kildea, T., Miller, D., Airoldi, L., and Cheshire, A. 2008. Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar. Ecol. Prog. Ser. 36:63–72.

    Article  Google Scholar 

  • Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J., and Smith, A. G. 2005. Algae acquire vitamin B-12 through a symbiotic relationship with bacteria. Nature 438:90–93.

    Article  PubMed  CAS  Google Scholar 

  • Davis, A., Targett, N., McConnell, O., and Young, C. 1989. Epibiosis of marine algae and benthic invertebrates: natural products chemistry and other mechanisms inhibiting settlement and overgrowth, in P. Scheuer (ed.), Bioorganic Marine Chemistry. Springer, Heidelberg, Berlin, New York.

    Google Scholar 

  • de Nys, R., Wright, A. D., Konig, G. M., and Sticher, O. 1993. New halogenated furanones from the marine alga Delisea pulchra (Cf fimbrata). Tetrahedron 49:11213–11220.

    Article  Google Scholar 

  • de Nys, R., Steinberg, P. D., Willemsen, P., Dworjanyn, S. A., Gabelish, C. L., and King, R. J. 1995. Broad-spectrum effects of secondary metabolites from the red alga Delisea pulchra in antifouling assays. Biofouling 8:259–271.

    Article  Google Scholar 

  • Dobretsov, S., Teplitski, M., Bayer, M., Gunasekera, S., Proksch, P., and Paul, V. J. 2011. Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling 27:893–905.

    Article  PubMed  CAS  Google Scholar 

  • Dworjanyn, S. A., de Nys, R., and Steinberg, P. D. 1999. Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra. Mar. Biol. 133:727–736.

    Article  CAS  Google Scholar 

  • Dworjanyn, S. A., de Nys, R., and Steinberg, P. D. 2006. Chemically mediated antifouling in the red alga Delisea pulchra. Mar. Ecol. Prog. Ser. 318:153–163.

    Article  CAS  Google Scholar 

  • Edwards, M. S. and Estes, J. A. 2006. Catastrophe, recovery and range limitation in NE Pacific kelp forests: a large-scale perspective. Mar. Ecol. Prog. Ser. 320:79–87.

    Article  Google Scholar 

  • Ellison, A. M., Bank, M. S., Clinton, B. D., Colburn, E. A., Elliott, K., Ford, C. R., Foster, D. R., Kloeppel, B. D., Knoepp, J. D., Lovett, G. M., Mohan, J., Orwig, D. A., Rodenhouse, N. L., Sobczak, W. V., Stinson, K. A., Stone, J. K., Swan, C. M., Thompson, J., von Holle, B., and Webster, J. R. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front. Ecol. Environ. 3:479–486.

    Article  Google Scholar 

  • Engel, S., Jensen, P. R., and Fenical, W. 2002. Chemical ecology of marine microbial defense. J. Chem. Ecol. 28:1971–1985.

    Article  PubMed  CAS  Google Scholar 

  • FERNANDES, N. 2011. Molecular studies on the role of bacteria in a marine algal disease. PhD dissertation. Sydney: University of New South Wales.

  • Fernandes, N., Case, R. J., Longford, S. R., Seyedsayamdost, M. R., Steinberg, P. D., Kjelleberg, S., and Thomas, T. 2011. Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red alga delisea pulchra. PLoS One 6:e27387.

    Article  PubMed  CAS  Google Scholar 

  • Fuqua, W. C., Winans, S. C., and Greenberg, E. P. 1994. Quorum sensing in bacteria—the LuxR-LuxI family of cell density-responsive trabnscriptional regulators. J. Bacteriol. 176:269–275.

    PubMed  CAS  Google Scholar 

  • Gachon, C. M. M., Sime-Ngando, T., Strittmatter, M., Chambouvet, A., and Kim, G. H. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15:633–640.

    Article  PubMed  CAS  Google Scholar 

  • Gao, M. S., Teplitski, M., Robinson, J. B., and Bauer, W. D. 2003. Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol. Plant Microbe Interact. 16:827–834.

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni, S. and Rappe, M. 2000. Evolution, diversity, and molecular ecology of marine prokaryotes, in D. Kirchman (ed.), Microbial Ecology of the Oceans. Wiley-Liss, New York.

    Google Scholar 

  • Givskov, M., de Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P. D., and Kjelleberg, S. 1996. Eukaryotic interference with homoserine lactone-mediated prokaryotic signaling. J. Bacteriol. 178:6618–6622.

    PubMed  CAS  Google Scholar 

  • Glynn, P. W. 1996. Coral reef bleaching: Facts, hypotheses and implications. Glob. Chang. Biol. 2:495–509.

    Article  Google Scholar 

  • Goecke, F., Labes, A., Wiese, J., and Imhoff, J. F. 2010. Chemical interactions between marine macroalgae and bacteria. Mar. Ecol. Prog. Ser. 409:267–299.

    Article  CAS  Google Scholar 

  • HARDER, T. 2008. Marine epibiosis: concepts, ecological consequences and host defence, pp. 219–232, in H. Flemming, R. Venkatesan, and S. Murthy (eds.), Marine and Industrial Biofouling. Springer, Heidelberg, New York.

    Google Scholar 

  • Harvell, C. D. and Hewson, I. 2010. Climate change and invertebrate microbial interactions. Integr. Comp. Biol. 50:E69.

    Google Scholar 

  • Harvell, D., Altizer, S., Cattadori, I. M., Harrington, L., and Weil, E. 2009. Climate change and wildlife diseases: When does the host matter the most? Ecology 90:912–920.

    Article  PubMed  Google Scholar 

  • Hay, M. E. 2009. Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annu. Rev. Mar. Sci. 1:193–212.

    Article  Google Scholar 

  • Hughes, D. T. and Sperandio, V. 2008. Inter-kingdom signalling: communication between bacteria and their hosts. Nat. Rev. Microbiol. 6:111–120.

    Article  PubMed  CAS  Google Scholar 

  • IPCC. 2007. Climate change 2007: the physical science basis, in S. Solomon, D. Qin, M. Manning (eds.), Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel Onclimate Change. Cambridge.

  • Joint, I., Tait, K., and Wheeler, G. 2007. Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos. Trans. R. Soc. B 362:1223–1233.

    Article  CAS  Google Scholar 

  • Konkel, M. E. and Tilly, K. 2000. Temperature-regulated expression of bacterial virulence genes. Microbes Infect. 2:157–166.

    Article  PubMed  CAS  Google Scholar 

  • Kushmaro, A., Loya, Y., Fine, M., and Rosenberg, E. 1996. Bacterial infection and coral bleaching. Nature 380:396.

    Article  CAS  Google Scholar 

  • Lachnit, T., Wahl, M., and Harder, T. 2010. Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling 26:247–255.

    Article  PubMed  CAS  Google Scholar 

  • Lachnit, T., Meske, D., Wahl, M., Harder, T., and Schmitz, R. 2011. Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ. Microbiol. 13:655–665.

    Article  PubMed  Google Scholar 

  • Lafferty, K. D., Porter, J. W., and Ford, S. E. 2004. Are diseases increasing in the ocean? Annu. Rev. Ecol. Syst. 35:31–54.

    Article  Google Scholar 

  • Lane, A. L., Nyadong, L., Galhena, A. S., Shearer, T. L., Stout, E. P., Parry, R. M., Kwasnik, M., Wang, M. D., Hay, M. E., Fernandez, F. M., and Kubanek, J. 2009. Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed. Proc. Natl. Acad. Sci. U.S.A. 106:7314–7319.

    Article  PubMed  CAS  Google Scholar 

  • Littler, M. M. and Littler, D. S. 1995. Impact of CLOD pathogen on Pacific coral reefs. Science 267:1356–1360.

    Article  PubMed  CAS  Google Scholar 

  • Longford, S. R., Tujula, N. A., Crocetti, G. R., Holmes, A. J., Holmstrom, C., Kjelleberg, S., Steinberg, P. D., and Taylor, M. W. 2007. Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat. Microb. Ecol. 48:217–229.

    Article  Google Scholar 

  • Manefield, M., de Nys, R., Kumar, N., Read, R., Givskov, M., Steinberg, P., and Kjelleberg, S. A. 1999. Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiol-UK 145:283–291.

    Article  CAS  Google Scholar 

  • Manefield, M., Harris, L., Rice, S. A., de Nys, R., and Kjelleberg, S. 2000. Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl. Environ. Microbiol. 66:2079–2084.

    Article  PubMed  CAS  Google Scholar 

  • Matsuo, Y., Imagawa, H., Nishizawa, M., and Shizuri, Y. 2005. Isolation of an algal morphogenesis inducer from a marine bacterium. Science 307:1598.

    Article  PubMed  CAS  Google Scholar 

  • Maximilien, R., de Nys, R., Holmstrom, C., Gram, L., Givskov, M., Crass, K., Kjelleberg, S., and Steinberg, P. D. 1998. Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat. Microb. Ecol. 15:233–246.

    Article  Google Scholar 

  • Miller, M. B. and Bassler, B. L. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165–199.

    Article  PubMed  CAS  Google Scholar 

  • PETTUS, J. A., WING, R. M., and SIMS, J. J. 1977. Marine natural products.12. Isolation of a family of multi-halogenated gamma-methylene lactones from red seaweed Delisea fimbriata. Tetrahedron Let. :41–44.

  • Pantos, O. and Bythell, J. C. 2006. Bacterial community structure associated with white band disease in the elkhorn coral Acropora palmata determined using culture-independent 16S rRNA techniques. Dis. Aquat. Org. 69:79–88.

    Article  PubMed  CAS  Google Scholar 

  • Paul, V. J., Arthur, K. E., Ritson-Williams, R., Ross, C., and Sharp, K. 2007. Chemical defenses: From compounds to communities. Biol. Bull. 213:226–251.

    Article  PubMed  CAS  Google Scholar 

  • Paul, V. J., Ritson-Williams, R., and Sharp, K. 2011. Marine chemical ecology in benthic environments. Nat. Prod. Rep. 28:345–387.

    Google Scholar 

  • Pawlik, J. R. 1993. Marine invertebrate chemical defenses. Chem. Rev. 93:1911–1922.

    Article  CAS  Google Scholar 

  • Persson, F., Svensson, R., Nylund, G. M., Fredriksson, N. J., Pavia, H., and Hermansson, M. 2011. Ecological role of a seaweed secondary metabolite for a colonizing bacterial community. Biofouling 27:579–588.

    Article  PubMed  CAS  Google Scholar 

  • Phelan, V., Liu, W., Pogliano, K., and Dorrestein, P. 2012. Microbial metabolic exchange—the chemotype-to-phenotype link. Nat. Chem. Biol. 8:26–35.

    Article  CAS  Google Scholar 

  • Rice, S. A., McDougald, D., Givskov, M., and Kjelleberg, S. 2007. Detection and inhibition of bacterial cell–cell communication, pp. 55–68, in F. DeLeo and M. Otto (eds.), Bacterial Pathogenesis Methods and Protocols. Springer, New Jersey.

    Google Scholar 

  • Rohwer, F., Seguritan, V., Azam, F., and Knowlton, N. 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1–10.

    Article  Google Scholar 

  • Rosenberg, E. and Zilber-Rosenberg, I. 2011. Symbiosis and development: the hologenome concept. Birth Defects Res. Part C-Embryo Today-Rev. 93:56–66.

    Article  CAS  Google Scholar 

  • Rumbaugh, K. 2004. The language of bacteria … and just about everything else. Scientist 18:26–27.

    Google Scholar 

  • Short, F. T. and Neckles, H. A. 1999. The effects of global climate change on seagrasses. Aquat. Bot. 63:169–196.

    Article  Google Scholar 

  • Short, F. T., Muehlstein, L. K., and Porter, D. 1987. Eelgrass wasting disease—cause and recurrence of a marine epidemic. Biol. Bull. 173:557–562.

    Article  Google Scholar 

  • Simon, C. and Daniel, R. 2011. Metagenomic analyses: past and future trends. Appl. Environ. Microbiol. 77:1153–1161.

    Article  PubMed  CAS  Google Scholar 

  • Skindersoe, M. E., Ettinger-Epstein, P., Rasmussen, T. B., Bjarnsholt, T., de Nys, R., and Givskov, M. 2008. Quorum sensing antagonism from marine organisms. Mar. Biotechnol. 10:56–63.

    Article  PubMed  CAS  Google Scholar 

  • Stachowicz, J. J. 2001. Mutualisms, positive interactions, and the structure of ecological communities. BioScience 51:235–246.

    Article  Google Scholar 

  • Steinberg, P. D. and van Altena, I. 1992. Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temparate Australasia. Ecol. Monogr. 62:189–222.

    Article  Google Scholar 

  • Steneck, R. S., Graham, M. H., Bourque, B. J., Corbett, D., Erlandson, J. M., Estes, J. A., and Tegner, M. J. 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29:436–459.

    Article  Google Scholar 

  • Teplitski, M., Robinson, J. B., and Bauer, W. D. 2000. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant Microbe Interact. 13:637–648.

    Article  PubMed  CAS  Google Scholar 

  • Teplitski, M., Chen, H. C., Rajamani, S., Gao, M. S., Merighi, M., Sayre, R. T., Robinson, J. B., Rolfe, B. G., and Bauer, W. D. 2004. Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol. 134:137–146.

    Article  PubMed  CAS  Google Scholar 

  • Thibaut, T., Pinedo, S., Torras, X., and Ballesteros, E. 2005. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Alberes coast (France, North-western Mediterranean). Mar. Pollut. Bull. 50:1472–1489.

    Article  PubMed  CAS  Google Scholar 

  • Thomas, T., Rusch, D., Demaere, M. Z., Yung, P. Y., Lewis, M., Halpern, A., Heidelberg, K. B., Egan, S., Steinberg, P. D., and Kjelleberg, S. 2010. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 4:1557–1567.

    Article  PubMed  CAS  Google Scholar 

  • Vairappan, C. S., Suzuki, M., Motomura, T., and Ichimura, T. 2001. Pathogenic bacteria associated with lesions and thallus bleaching symptoms in the Japanese kelp Laminaria religiosa Miyabe (Laminariales, Phaeophyceae). Hydrobiologia 445:183–191.

    Article  Google Scholar 

  • van Oppen, M. J. H., Leong, J. A., and Gates, R. D. 2009. Coral-virus interactions: A double-edged sword? Symbiosis 47:1–8.

    Article  Google Scholar 

  • Vargas-Angel, B. 2010. Crustose coralline algal diseases in the US-Affiliated Pacific Islands. Coral Reefs 29:943–956.

    Article  Google Scholar 

  • von Bodman, S. B., Bauer, W. D., and Coplin, D. L. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41:455–482.

    Article  Google Scholar 

  • Webster, N. S., Cobb, R. E., and Negri, A. P. 2008. Temperature thresholds for bacterial symbiosis with a sponge. ISME J. 2:830–842.

    Article  PubMed  CAS  Google Scholar 

  • Webster, N. S., Taylor, M. W., Behnam, F., Lucker, S., Rattei, T., Whalan, S., Horn, M., and Wagner, M. 2010. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12:2070–2082.

    PubMed  CAS  Google Scholar 

  • Webster, N. S., Soo, R., Cobb, R., and Negri, A. P. 2011. Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae. ISME J. 5:759–770.

    Article  PubMed  CAS  Google Scholar 

  • Williams, W. M., Viner, A. B., and Broughton, W. J. 1987. Nitrogen-fixation (acetylene reduction) associated with the living coral Acropora variabilis. Mar. Biol. 94:531–535.

    Article  Google Scholar 

  • Williamson, J. E., Carson, D. G., de Nys, R., and Steinberg, P. D. 2004. Demographic consequences of an ontogenetic shift by a sea urchin in response to host plant chemistry. Ecology 85:1355–1371.

    Article  Google Scholar 

  • Wright, J. T., de Nys, R., Poore, A. G. B., and Steinberg, P. D. 2004. Chemical defense in a marine alga: Heritability and the potential for selection by herbivores. Ecology 85:2946–2959.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centre for Marine Bio-Innovation and School of Biological, Earth and Environmental Science, University of New South Wales, Sydney, NSW, Australia, 2052

    Tilmann Harder, Alexandra H. Campbell & Peter D. Steinberg

  2. Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia, 2052

    Suhelen Egan

  3. Sydney Institute of Marine Science, 2 Chowder Bay Rd., Mosman, NSW, Australia, 2088

    Peter D. Steinberg

Authors
  1. Tilmann Harder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandra H. Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suhelen Egan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter D. Steinberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tilmann Harder.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harder, T., Campbell, A.H., Egan, S. et al. Chemical Mediation of Ternary Interactions Between Marine Holobionts and Their Environment as Exemplified by the Red Alga Delisea pulchra . J Chem Ecol 38, 442–450 (2012). https://doi.org/10.1007/s10886-012-0119-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0119-5

Keywords

Search

Navigation