Accumulation of Gel Particles in the Sea-Surface Microlayer during an Experimental Study with the Diatom Thalassiosira weissflogii

Abstract

Since the early 80’s, the sea-surface microlayer (SML) has been hypothesized as being a gelatinous film. Recent studies have confirmed this characteristic, which confers properties that mediate mass and energy fluxes between ocean and atmosphere, including the emission of primary organic aerosols from marine systems. We investigated SML thickness and composition in five replicate indoor experiments between September and December 2010. During each experiment, the SML and underlying seawater were sampled from four seawater tanks: one served as control, and three were inoculated with Thalassiosira weissflogii grown in chemostats at 180, 380 and 780 ppm pCO2. We examined organic material enrichment factors in each tank, paying particular attention to gel particles accumulation such as polysaccharidic Transparent Exopolymer Particles (TEP) and the proteinaceous Coomassie Stainable Particles (CSP). While previous studies have observed carbohydrates and TEP enrichment in the microlayer, little is yet known about proteinaceous gel particles in the SML. Our experiments show that CSP dominate the gelatinous composition of the SML. We believe that the enrichment in CSP points to the importance of bacterial activity in the microlayer. Bacteria may play a pivotal role in mediating processes at the air-sea interface thanks to their exudates and protein content that can be released through cell disruption.

Share and Cite:

L. Galgani and A. Engel, "Accumulation of Gel Particles in the Sea-Surface Microlayer during an Experimental Study with the Diatom Thalassiosira weissflogii," International Journal of Geosciences, Vol. 4 No. 1, 2013, pp. 129-145. doi: 10.4236/ijg.2013.41013.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] O. Wurl and J. P. Obbard, “A Review of Pollutants in the Sea-Surface Microlayer (SML): A Unique Habitat for Marine Organisms,” Marine Pollution Bulletin, Vol. 48, No. 11, 2004, pp. 1016-1030. doi:10.1016/j.marpolbul.2004.03.016
[2] P. S. Liss and R. A. Duce, “The Sea Surface and Global Change,” Cambridge University Press, Cambridge, 2005.
[3] E. S. Van Vleet and P. M. Williams, “Sampling Sea Sur face Films: A Laboratory Evaluation of Techniques and Collecting Materials,” Limnology and Oceanography, Vol. 25, No. 4, 1980, pp. 764-770. doi:10.4319/lo.1980.25.4.0764
[4] E. S. Van Vleet and P. M. Williams, “Surface Potential and Film Pressure Measurements in Seawater Systems,” Limnology and Oceanography, Vol. 28, No. 3, 1983, pp. 401-414. doi:10.4319/lo.1983.28.3.0401
[5] Z. Zhang, “Studies on the Sea Surface Microlayer II. The Layer of Sudden Change of Physical and Chemical Properties,” Journal of Colloid and Interface Science, Vol. 264, No. 1, 2003, pp. 148-159. doi:10.1016/S0021-9797(03)00390-4
[6] Z. Zhang, C. Liu and L. Liu, “Physicochemical Studies of the Sea-Surface Microlayer,” Frontiers of Chemistry in China, Vol. 1, No. 1, 2006, pp. 1-14. doi:10.1007/s11458-005-0003-8
[7] Z. Zhang, L. Liu, Z. Wu, J. Li and H. Ding, “Physicochemical Studies of the Sea Surface Microlayer: I. Thickness of the Sea Surface Microlayer and Its Experimental Determination,” Journal of Colloid and Interface Science, Vol. 204, No. 2, 1998, pp. 294-299.
[8] C. Stolle, K. Nagel, M. Labrenz and K. Jürgens, “Bacterial Activity in the Sea-Surface Microlayer: In Situ Investigations in the Baltic Sea and the Influence of Sampling Devices,” Aquatic Microbial Ecology, Vol. 58, No. 1, 2009, pp. 67-78. doi:10.3354/ame01351
[9] H. Agogué, E.O. Casamayor, F. Joux, I. Obernosterer, C. Dupuy, F. Lantoine, P. Catala, M. G. Weinbauer, T. Re inthaler, G. J. Herndl and P. Lebaron, “Comparison of Samplers for the Biological Characterization of the Sea Surface Microlayer,” Limnology and Oceanography: Methods, Vol. 2, 2004, pp. 213-225. doi:10.4319/lom.2004.2.213
[10] O. Wurl and M. Holmes, “The Gelatinous Nature of the Sea-Surface Microlayer,” Marine Chemistry, Vol. 110, No. 1, 2008, pp. 89-97. doi:10.1016/j.marchem.2008.02.009
[11] A. Engel, “Determination of Marine Gel Particles,” In: Practical Guidelines for the Analysis of Seawater, CRC Press, Boca Raton, 2009. doi:10.1201/9781420073072.ch7
[12] M. Cunliffe and J. C. Murrell, “The Sea-Surface Micro layer Is a Gelatinous Biofilm,” The ISME Journal, Vol. 3, No. 9, 2009, pp. 1001-1003. doi:10.1038/ismej.2009.69
[13] A. L. Alldredge, U. Passow and B. E. Logan, “The Abundance and Significance of a Class of Large, Transparent Organic Particles in the Ocean,” Deep Sea Research, Vol. 40, No. 6, 1993, pp. 1131-1140. doi:10.1016/0967-0637(93)90129-Q
[14] H.-P. Grossart, G. Czub and M. Simon, “Algae-Bacteria Interactions and Their Effects on Aggregation and Organic Matter Flux in the Sea,” Environmental Microbiology, Vol. 8, No. 6, 2006, pp. 1074-1084. doi:10.1111/j.1462-2920.2006.00999.x
[15] U. Passow, R. F. Shipe, A. Murray, D. K. Pak, M. A. Brzezinski and A. L. Alldredge, “The Origin of Trans parent Exopolymer Particles (TEP) and Their Role in the Sedimentation of Particulate Matter,” Continental Shelf Research, Vol. 21, No. 4, 2001, pp. 327-346. doi:10.1016/S0278-4343(00)00101-1
[16] J. M. Sieburth, “Microbiological and Organic-Chemical Processes in the Surface and Mixed Layers—Air-Sea Exchange of Gases and Particles,” D. Reidel Publishing Company, Boston, 1983.
[17] O. Wurl, E. Wurl, L. Miller, K. Johnson and S. Vagle, “Formation and Global Distribution of Sea-Surface Microlayers,” Biogeosciences, Vol. 8, No. 1, 2011, pp. 121 135. doi:10.5194/bg-8-121-2011
[18] W.-C. Chin, M. V. Orellana and P. Verdugo, “Spontane ous Assembly of Marine Dissolved Organic Matter into Polymer Gels,” Nature, Vol. 391, No. 6667, 1998, pp. 568-572. doi:10.1038/35345
[19] A. Engel, S. Thoms, U. Riebesell, E. Rochelle-Newall and I. Zondervan, “Polysaccharide Aggregation as a Potential Sink of Marine Dissolved Organic Carbon,” Nature, Vol. 428, No. 6986, 2004, pp. 929-932. doi:10.1038/nature02453
[20] P. Verdugo, A. L. Alldredge, F. Azam, D. L. Kirchman, U. Passow and P. H. Santschi, “The Oceanic Gel Phase: A Bridge in the DOM-POM Continuum,” Marine Chemistry, Vol. 92, No. 1-4, 2004, pp. 67-85. doi:10.1016/j.marchem.2004.06.017
[21] R. Benner, “Chemical Composition and Reactivity,” In: D. A. Hansell and D. J. Carlson, Eds., Biogeochemistry of Marine Dissolved Organic Matter, Academic Press, Waltham, 2002, pp. 59-90. doi:10.1016/B978-012323841-2/50005-1
[22] R. A. Long and F. Azam, “Abundant Protein-Containing Particles in the Sea,” Aquatic Microbial Ecology, Vol. 10, No. 3, 1996, pp. 213-221. doi:10.3354/ame010213
[23] M. Kuznetsova, C. Lee and J. Aller, “Enrichment of Ami no Acids in the Sea Surface Microlayer at Coastal and Open Ocean Sites in the North Atlantic Ocean,” Limnology and Oceanography, Vol. 49, No. 5, 2004, pp. 1605 1619. doi:10.4319/lo.2004.49.5.1605
[24] M. Kuznetsova and C. Lee, “Dissolved Free and Combined Amino Acids in Nearshore Seawater, Sea Surface Microlayers and Foams: Influence of Extracellular Hydrolysis,” Aquatic Sciences—Research Across Boundaries, Vol. 64, 2002, pp. 252-268.
[25] M. Kuznetsova and C. Lee, “Enhanced Extracellular En zymatic Peptide Hydrolysis in the Sea-Surface Micro layer,” Marine Chemistry, Vol. 73, No. 3-4, 2001, pp. 319-332. doi:10.1016/S0304-4203(00)00116-X
[26] M. Kuznetsova, C. Lee and J. Aller, “Characterization of the Proteinaceous Matter in Marine Aerosols,” Marine Chemistry, Vol. 96, No. 3-4, 2005, pp. 359-377. doi:10.1016/j.marchem.2005.03.007
[27] C. Borchard, A. V. Borges, N. H?ndel and A. Engel, “Biogeochemical Response of Emiliania Huxleyi (PML B92/11) to Elevated CO2 and Temperature under Phos phorous Limitation: A Chemostat Study,” Journal of Experimental Marine Biology and Ecology, Vol. 410, 2011, pp. 61-71. doi:10.1016/j.jembe.2011.10.004
[28] C. Stolle, K. Nagel, M. Labrenz and K. Jürgens, “Succes sion of the Sea-Surface Microlayer in the Coastal Baltic Sea under Natural and Experimentally Induced Low Wind Conditions,” Biogeosciences, Vol. 7, No. 9, 2010, pp. 2975-2988. doi:10.5194/bg-7-2975-2010
[29] M. Cunliffe, A. Engel, S. Frka, B. Ga?parovi?, C. Guitart, J. C. Murrell, M. Salter, C. Stolle, R. Upstill-Goddard and O. Wurl, “Sea Surface Microlayers: A Unified Physico chemical and Biological Perspective of the Air-Ocean Interface,” Progress in Oceanography, 2012, in Press.
[30] G. W. Harvey and L. A. Burzell, “A Simple Microlayer Method for Small Samples,” Limnology and Oceanogra phy, Vol. 11, No. 4, 1972, pp. 608-614. doi:10.4319/lo.1966.11.4.0608
[31] P. S. Liss and R. A. Duce, “The Sea Surface and Global Change,” Cambridge University Press, Cambridge, 1997. doi:10.1017/CBO9780511525025
[32] B. E. Logan, H.-P. Grossart and M. Simon, “Direct Ob servation of Phytoplankton, TEP and Aggregates on Poly carbonate Filters Using Brightfield Microscopy,” Journal of Plankton Research, Vol. 16, No. 12, 1994, pp. 1811-1815. doi:10.1093/plankt/16.12.1811
[33] E. J. Rochelle-Newall, X. Mari and O. Pringault, “Sticking Properties of Transparent Exopolymeric Particles (TEP) during Aging and Biodegradation,” Journal of Plankton Research, Vol. 32, No. 10, 2010, pp. 1433-1442. doi:10.1093/plankt/fbq060
[34] X. Mari and A. Burd, “Seasonal Size Spectra of Trans parent Exopolymeric Particles (TEP) in a Coastal Sea and Comparison with Those Predicted Using Coagulation The ory,” Marine Ecology Progress Series, Vol. 163, 1998, pp. 63-76. doi:10.3354/meps163063
[35] A. Engel and N. H?ndel, “A Novel Protocol for Deter mining the Concentration and Composition of Sugars in Particulate and in High Molecular Weight Dissolved Organic Matter (HMW-DOM) in Seawater,” Marine Chemistry, Vol. 127, No. 1-4, 2011, pp. 180-191. doi:10.1016/j.marchem.2011.09.004
[36] M. Cunliffe, M. Salter, P. J. Mann, A. S. Whiteley, R. C. Upstill-Goddard and J. C. Murrell, “Dissolved Organic Carbon and Bacterial Populations in the Gelatinous Sur face Microlayer of a Norwegian Fjord Mesocosm,” FEMS Microbiology Letters, Vol. 299, No. 2, 2009, pp. 248-254. doi:10.1111/j.1574-6968.2009.01751.x
[37] U. Passow, “Transparent Exopolymer Particles (TEP) in Aquatic Environments,” Progress in Oceanography, Vol. 55, No. 3-4, 2002, pp. 287-333. doi:10.1016/S0079-6611(02)00138-6
[38] U. Passow, “Formation of Transparent Exopolymer Particles, TEP, from Dissolved Precursor Material,” Marine Ecology Progress Series, Vol. 192, 2000, pp. 1-11. doi:10.3354/meps192001
[39] O. Wurl, L. Miller and S. Vagle, “Production and Fate of Transparent Exopolymer Particles in the Ocean,” Journal of Geophysical Research, Vol. 116, 2011, Article ID: C00H13. doi:10.1029/2011JC007342
[40] K. M. Crocker and U. Passow, “Differential Aggregation of Diatoms,” Marine Ecology Progress Series, Vol. 117, 1995, pp. 249-257. doi:10.3354/meps117249
[41] A. Gardes, M. H. Iversen, H.-P. Grossart, U. Passow and M. S. Ullrich, “Diatom-Associated Bacteria Are Required for Aggregation of Thalassiosira weissflogii,” The ISME Journal, Vol. 5, No. 3, 2011, pp. 436-445.
[42] U. Passow and A. L. Alldredge, “Aggregation of a Diatom Bloom in a Mesocosm: The Role of Transparent Exopolymer Particles (TEP),” Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 42, No. 1, 1995, pp. 99-109. doi:10.1016/0967-0645(95)00006-C
[43] J. Zhou, K. Mopper and U. Passow, “The Role of Sur face-Active Carbohydrates in the Formation of Transparent Exopolymer Particles by Bubble Adsorption of Sea Water,” Limnology and Oceanography, Vol. 43, No. 8, 1998, pp. 1860-1871.
[44] U. Passow, “Production of Transparent Exopolymer Par ticles (TEP) by Phyto and Bacterioplankton,” Marine Ecology Progress Series, Vol. 236, 2002, pp. 1-12. doi:10.3354/meps236001
[45] I. Obernosterer, P. Catala, T. Reinthaler, G. J. Herndl and P. Lebaron, “Enhanced Heterotrophic Activity in the Sur face Microlayer of the Mediterranean Sea,” Aquatic Microbial Ecology, Vol. 39, No. 3, 2005, pp. 293-302. doi:10.3354/ame039293
[46] H.-P. Grossart, F. Levold, M. Allgaier, M. Simon and T. Brinkhoff, “Marine Diatom Species Harbour Distinct Bacterial Communities,” Environmental Microbiology, Vol. 7, No. 6, 2005, pp. 860-873. doi:10.1111/j.1462-2920.2005.00759.x
[47] T. Reinthaler, E. Sintes and G. J. Herndl, “Dissolved Organic Matter and Bacterial Production and Respiration in the Sea-Surface Microlayer of the Open Atlantic and the Western Mediterranean Sea,” Limnology and Oceanography, Vol. 53, No. 1, 2008, pp. 122-136. doi:10.4319/lo.2008.53.1.0122
[48] S. M. Henrichs and P. M. Williams, “Dissolved and Particulate Amino Acids and Carbohydrates in the Sea Sur face Microlayer,” Marine Chemistry, Vol. 17, No. 2, 1985, pp. 141-163. doi:10.1016/0304-4203(85)90070-2
[49] A. F. Carlucci, D. M. Wolgast and D. B. Craven, “Micro bial Populations in Surface Films: Amino Acid Dynamics in Nearshore and Offshore Waters off Southern Califor nia,” Journal of Geophysical Research, Vol. 97, No. C4, 1992, pp. 5271-5280. doi:10.1029/91JC02614
[50] A. F. Carlucci, D. B. Craven, K. J. Robertson and P. M. Williams, “Surface-Film Microbial Populations: Diel Amino Acid Metabolism, Carbon Utilization, and Growth Rates,” Marine Biology, Vol. 92, No. 2, 1986, pp. 289 297. doi:10.1007/BF00392847
[51] K. Mopper, R. Dawson, G. Liebezeit and V. Ittekkot, “The Monosaccharide Spectra of Natural Waters,” Marine Chemistry, Vol. 10, No. 1, 1980, pp. 55-66. doi:10.1016/0304-4203(80)90058-4
[52] A. Skoog and R. Benner, “Aldoses in Various Size Fractions of Marine Organic Matter: Implications for Carbon Cycling,” Limnology and Oceanography, Vol. 42, No. 8, 1997, pp. 1803-1813. doi:10.4319/lo.1997.42.8.1803
[53] K. Mopper, “Sugars and Uronic Acids in Sediment and Water from the Black Sea and North Sea with Emphasis on Analytical Techniques,” Marine Chemistry, Vol. 5, No. 4-6, 1977, pp. 585-603. doi:10.1016/0304-4203(77)90044-5
[54] S. M. Myklestad, E. Skkanoy and S. Hestmann, “A Sensitive and Rapid Method for Analysis of Dissolved Mono and Polysaccharides in Seawater,” Marine Chemistry, Vol. 56, No. 3-4, 1997, pp. 279-286. doi:10.1016/S0304-4203(96)00074-6
[55] A. Engel, J. R. M. Harlay, J. Piontek and L. Chou, “Contribution of Combined Carbohydrates to Dissolved and Particulate Organic Carbon after the Spring Bloom in the Northern Bay of Biscay (North-Eastern Atlantic Ocean),” Continental Shelf Research, Vol. 45, 2012, pp. 42-53. doi:10.1016/j.csr.2012.05.016
[56] A. Engel, N. H?ndel, J. Wohlers, M. Lunau, H. P. Gros sart, U. Sommer and U. Riebesell, “Effects of Sea Surface Warming on the Production and Composition of Dissolved Organic Matter during Phytoplankton Blooms: Results from a Mesocosm Study,” Journal of Plankton Re search, Vol. 33, 2010, pp. 357-372. doi:10.1093/plankt/fbq122
[57] C. Borchard and A. Engel, “Organic Matter Exudation by Emiliania huxleyi under Simulated Future Ocean Conditions,” Biogeosciences, Vol. 9, 2012, pp. 3405-3423. doi:10.5194/bg-9-3405-2012
[58] S. M. Myklestad, “Dissolved Organic Carbon from Phy toplankton,” In: P. Wangersky, Ed., Springer, Berlin, Hei delberg, 2000, pp. 111-148.
[59] R. Benner, K. Kaiser, “Abundance of Amino Sugars and Peptidoglycan in Marine Particulate and Dissolved Orga nic Matter,” Limnology and Oceanography, Vol. 48, No. 1, 2003, pp. 118-128. doi:10.4319/lo.2003.48.1.0118
[60] P. M. Williams, A. F. Carlucci, S. M. Henrichs, E. S. Van Vleet, S. G. Horrigan, F. M. H. Reid and K. J. Robertson, “Chemical and Microbiological Studies of Sea-Surface Films in the Southern Gulf of California and off the West Coast of Baja California,” Marine Chemistry, Vol. 19, No. 1, 1986, pp. 17-98. doi:10.1016/0304-4203(86)90033-2
[61] A. L. Santos, C. Mendes, N. C. M. Gomes, I. Henriques, A. N. Correia, A. Almeida and ?. Cunha, “Short-Term Variability of Abundance, Diversity and Activity of Estuarine Bacterioneuston and Bacterioplankton,” Journal of Plankton Research, Vol. 31, No. 12, 2009, pp. 1545 1555. doi:10.1093/plankt/fbp083
[62] G. C. Hays, A. J. Richardson and C. Robinson, “Climate Change and Marine Plankton,” Trends in Ecology & Evo lution, Vol. 20, No. 6, 2005, pp. 337-344. doi:10.1016/j.tree.2005.03.004
[63] A. Engel, “Direct Relationship between CO2 Uptake and Transparent Exopolymer Particles Production in Natural Phytoplankton,” Journal of Plankton Research, Vol. 24, No. 1, 2002, pp. 49-53. doi:10.1093/plankt/24.1.49
[64] I. Joint, S. C. Doney and D. M. Karl, “Will Ocean Acidification Affect Marine Microbes?” The ISME Journal, Vol. 5, 2011, pp. 1-7. doi:10.1038/ismej.2010.79

Journals Menu
Follow SCIRP
Contact us
+1 323-425-8868
customer@scirp.org
WhatsApp +86 18163351462(WhatsApp)
Click here to send a message to me 1655362766
Paper Publishing WeChat

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.