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 Research

Volumn 33, Issue 3, 2011, Pages 357-372

  Engel, Anja ^a   Händel, Nicole ^a   Wohlers, Julia ^b   Lunau, Mirko ^a   Grossart, Hans Peter ^c   Sommer, Ulrich ^c   Riebesell, Ulf ^c  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^c IGB Neuglobsow   (Germany)

Author keywords

amino acids; DOM; mesocosm; microbial loop; phytoplankton; polysaccharides; sea surface warming

Indexed keywords

ALGAL BLOOM; AMINO ACID; BOTTOM-UP CONTROL; CHLOROPHYLL; DIATOM; DISSOLVED ORGANIC MATTER; EXPERIMENTAL STUDY; MARINE ECOSYSTEM; MESOCOSM; MICROBIAL LOOP; PHYTOPLANKTON; POLYSACCHARIDE; SEA SURFACE; SEAWATER; TEMPERATURE EFFECT;

ALGAE; BACILLARIOPHYTA;

EID: 79551711825     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbq122     Document Type: Article

References (76)

1. Alldredge, A. L., Passow, U. and Logan, B. E. (1993) The abundance and significance of a class of large, transparent organic particles in the ocean. Deep-Sea Res., 40, 1131-1140. (Pubitemid 24429273)
2. Anderson, T. R. and Williams, P. J. leB. (1999) A one dimensional model of dissolved organic carbon cycling in the water column incorporating combined biological-photochemical decomposition. Global Biogeochem. Cycles, 13, 337-349.
3. Azam, F. and Hodson, R. E. (1977) Size distribution and activity of marine microheterotrophs. Limnol. Oceanogr., 22, 492-501.
4. Azam, F., Fenchel, T., Field, J. G. et al. (1983) The ecological role of water column microbes in the sea. Mar. Ecol.-Prog. Ser., 10, 257-263.
5. Baines, S. B. and Pace, M. L. (1991) The production of dissolved organic matter by phytoplankton & its importance to bacteria, patterns across marine & freshwater systems. Limnol. Oceanogr., 36, 1078-1090. (Pubitemid 23396254)
6. Benner, R. (2002) Chemical composition and reactivity. In Hansell, D. A. and Carlson, C. (eds), Biogeochemistry of Marine Dissolved Organic Matter. Academic Press, Elsevier Science, San Diego, CA, USA, pp. 59-90.
7. Biddanda, B. and Benner, R. (1997) Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnol. Oceanogr., 42, 506-518. (Pubitemid 27422594)
8. Bronk, D. A. (2002) Dynamics of DON. In Hansell, D. A. and Carlson, C. (eds), Biogeochemistry of Marine Dissolved Organic Matter. Academic Press, Elsevier Science, San Diego, CA, USA, pp. 153-247.
9. Brown, J. H., Gillooly, J. F., Allen, A. P. et al. (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771-1789. (Pubitemid 39188101)
10. Carlson, C. A. (2002) Production and removal processes. In Hansell, D. A. and Carlson, C. (eds), Biogeochemistry of Marine Dissolved Organic Matter. Academic Press, Elsevier Science, San Diego, CA, USA, pp. 59-90.
11. Cho, B. C. and Azam, F. (1988) Major role of bacteria in biogeochemical fluxes in the ocean's interior. Nature, 332, 441-443.
12. Claquin, P., Probert, I., Lefebvre, S. and Véron, B. (2008). Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae. Aquat. Micr. Ecol., 51, 1-11. (Pubitemid 351785223)
13. Copping, A. E. and Lorenzen, C. J. (1980) Carbon budget of marine phytoplankton-herbivore system with carbon-14 as tracer. Limnol. Oceanogr., 25, 873-882.
14. Cowie, G. L. and Hedges, J. I. (1992) Sources and reactivities of amino acids in a coastal marine environment. Limnol. Oceanogr., 37, 703-724. (Pubitemid 23381212)
15. Dauwe, B. and Middelburg, J. J. (1998) Amino acids and hexosamines as indicators of organic matter degradation state in North Sea sediments. Limnol. Oceanogr., 43, 782-798. (Pubitemid 28456363)
16. Dauwe, B., Middelburg, J. J., Herman, P. M. J. et al. (1999) Linking diagenetic alteration of amino acids and bulk organic matter reactivity. Limnol. Oceanogr., 44, 1809-1814. (Pubitemid 29514885)
17. Davison, I. R. (1991) Environmental effects on algal photosynthesis: Temperature. J. Phycol., 27, 2-8.
18. del Giorgio, P. A. and Cole, J. J. (1998) Bacterioplankton growth efficiency in aquatic systems. An. Rev. Ecol. System. 29, 503-541. (Pubitemid 29033041)
19. Engel, A., Thoms, S., Riebesell, U. et al. (2004a) Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature, 428, 929-932. (Pubitemid 38560304)
20. Engel, A., Delille, B., Jacquet, S. et al. (2004b) Transparent exopolymer particles and dissolved organic carbon production by Emiliania huxleyi exposed to different CO2 concentrations: a mesocosm experiment. Aquat. Microb. Ecol., 34, 93-104. (Pubitemid 39098358)
21. Fogg, G. E. (1966) The extracellular products of algae. Mar. Biol. Annu. Rev., 4, 195-212.
22. Fuhrman, J. A. (1999) Marine viruses and their biogeochemical and ecological effects. Nature, 399, 541-548.
23. Geider, R. J. (1987) Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol., 106, 1-34.
24. Goldman, J. C. and Dennett, M. R. (1991) Ammonium regeneration and carbon utilization by marine bacteria grown on mixed substrates. Mar. Biol., 109, 369-378.
25. Grossart, H. P. and Simon, M. (2007) Interactions of planktonic algae and specific bacteria: influences on dissolved and particulate organic matter fluxes. Aquat. Microb. Ecol., 47, 163-176. (Pubitemid 350219043)
26. Grossart, H. P., Engel, A., Arnosti, C. et al. (2007) Microbial dynamics in autotrophic and heterotrophic seawater mesocosms: III Organic matter fluxes. Aquat. Microb. Ecol., 49, 143-156. (Pubitemid 351525784)
27. Hansell, D. A. and Carlson, C. A. (1998) Net community production of dissolved organic carbon. Global Biogeochem. Cycles, 12, 443-453.
28. Hansell, D. A., Carlson, C. A., Repeta, D. J. et al. (2009) Dissolved organic matter in the ocean: new insights stimulated by a controversy. Oceanogr., 22, 52-61.
29. Hernes, P. J., Hedges, J. I., Perterson, M. L., Wakeham, S. G. and Lee, C. (1996) Neutral carbohydrate chemistry of particulate matter in the central Equatorial Pacific. Deep-Sea Res. II, 43, 1181-1204.
30. Hopkinson, C. S. and Vallino, J. J. (2005) Efficient export of carbon to the deep ocean through dissolved organic matter. Nature, 433, 142-145.
31. Hoppe, H. G., Breithaupt, P., Walther, K. et al. (2008) Climate warming during winter affects the coupling between phytoplankton and bacteria during the spring bloom: results from a mesocosm study. Aquat. Microb. Ecol., 51, 105-115. (Pubitemid 351959710)
32. Kaiser, K. and Benner, R. (2009). Biochemical composition and size distribution of organic matter at the Pacific and Atlantic times-series stations. Mar. Chem., 113, 63-77.
33. Kawasaki, N. and Benner, R. (2006) Bacterial release of dissolved organic matter during cell growth and decline: molecular origin and composition. Limnol. Oceanogr., 51, 2170-2180. (Pubitemid 44520913)
34. Keil, R. G. and Kirchman, D. L. (1993) Abiotic transformation of labile protein to refractory protein in sea water. Mar. Chem., 45, 187-196.
35. Kerner, M., Hohenberg, H., Ertl, S. et al. (2003) Self-organization of dissolved organic matter to micelle-like microparticles in river water. Nature, 422, 150-154. (Pubitemid 36362744)
36. Kirchman, D. L. (2000) Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria. In Kirchman, D. L. (ed.), Microbial Ecology of the Oceans. Wiley, New York, pp. 261-288.
37. Kirchman, D. L., Keil, R. G. and Wheeler, P. A. (1990) Carbon limitation of ammonium uptake by heterotrophic bacteria in the sub-Arctic pacific. Limnol. Oceanogr., 35, 1258-1266.
38. Kirchman, D. L., Moran, X. A. G. and Ducklow, H. (2009) Microbial growth in the polar oceans-role of temperature and potential impact of climate change. Nat. Rev. Microbiol., 7, 451-459.
39. Koroleff, F. and Grasshoff, K. (1983) Determination of nutrients. In Grasshof, K., Erhardt, M. and Kremling, K. (eds), Methods of Seawater Analyses, Vol. 2. Verlag Chemie, Weinheim, Germany, pp. 125-188.
40. Kritzberg, E. S., Arrieta, J. M. and Duarte, C. M. (2010) Temperature and phosphorus regulating carbon flux through bacteria in a coastal marine system. Aquat. Microb. Ecol., 58, 141-151.
41. Kroer, N. (1993) Bacterial growth efficiencies on natural dissolved organic matter. Limnol. Oceanogr., 38, 1281-1290.
42. Laws, E. A., Falkowski, P. G., Smith, W. O. et al. (2000) Temperature effects on export production in the open ocean. Global Biogeochem. Cycles, 14, 231-1246.
43. Lee, C. and Cronin, C. (1984) Particulate amino acids in the sea: effects of primary productivity and biological decomposition. J. Mar. Res., 42, 1075-1097. (Pubitemid 15455792)
44. Leppard, G. G. (1995) The characterization of algal and microbial mucilages and their aggregates in aquatic ecosystems. Sci. Total Environ., 165, 103-131.
45. Lindroth, P. and Mopper, K. (1979) High performance liquid chromatography determination of subpicomole amounts of amino acids by precolumn fluorescence derivatisation with OPA. Anal. Chem., 51, 1667-1674.
46. Middelboe, M., Søndergaard, M., Letarte, Y. et al. (1995) Attached and free-living bacteria: production and polymer hydrolysis during a diatom bloom. Microb. Ecol., 29, 231-248.
47. Mopper, K., Zhou, X., Kieber, R. J. et al. (1991) Photochemical degradation of dissolved organic carbon and its impact on the oceanic carbon cycle. Nature, 353, 60-62. (Pubitemid 21912454)
48. Moran, X. A., Sebastian, M., Pedros-Alio, C. et al. (2006) Response of Southern Ocean phytoplankton and bacterioplankton to short-term experimental warming. Limnol. Oceanogr., 51, 1791-1800. (Pubitemid 44185730)
49. Myklestad, S., Haug, A. and Larsen, B. (1972) Production of carbohydrates by the marine diatom Chaetoceros affinis var Willei (Gran). In Hustedt II: preliminary investigation of the extracellular polysaccharide. J. Exp. Mar. Biol. Ecol., 9, 137-144.
50. Nagata, T. (2000) Production mechanisms of dissolved matter. In Kirchmann, D. L. (ed.), Microbial Ecology of the Oceans. Wiley-Liss, New York, pp. 121-152.
51. Ogawa, H., Amagai, Y., Koike, I. et al. (2001) Production of refractory dissolved organic matter by bacteria. Science, 292, 917-920. (Pubitemid 32422486)
52. Pakulski, J. D. and Benner, R. (1994) Abundance and distribution of carbohydrates in the ocean. Limnol. Oceanogr., 39, 930-940. (Pubitemid 2117875)
53. Palenik, B. and Morel, F. M. M. (1990) Cell-surface oxidation of amino acids in seawater. Mar. Ecol.-Prog. Ser., 59, 195-201.
54. Piontek, J., Händel, N., Langer, G. et al. (2009) Effects of rising temperature on the formation and microbial degradation of marine diatom aggregates. Aquat. Microb. Ecol., 54, 305-318.
55. Piontek, J., Lunau, M., Händel, N. et al. (2010) Acidification increases microbial polysaccharide degradation in the ocean. Biogeosciences, 7, 1615-1624.
56. Pomeroy, L. R. and Wiebe, W. J. (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat. Microb. Ecol., 23, 187-204. (Pubitemid 34253481)
57. Rich, J. H., Ducklow, H. W. and Kirchman, D. L. (1996) Concentrations and uptake of neutral monosaccharides along 140 degrees W in the equatorial Pacific: contribution of glucose to heterotrophic bacterial activity and the DOM flux. Limnol. Oceanogr., 41, 595-604. (Pubitemid 26324521)
58. Rosenstock, B. and Simon, M. (1993) Use of dissolved combined and free amino acids by planktonic bacteria in Lake Constance. Limnol. Oceanogr., 38, 1521-1531. (Pubitemid 2015286)
59. Sachs, L. (1974) Angewandte Statistik. Springer-Verlag, Berlin, Heidelberg, New York, pp. 329-333.
60. Schartau, M., Engel, A., Schröter, J. et al. (2007) Modelling carbon overconsumption and the formation of extracellular particulate organic carbon. Biogeosciences, 4, 433-454. (Pubitemid 47158264)
61. Schofield, O., Grzymski, J., Moline, M. M. A. et al. (1998) Impact of temperature on photosynthesis in the toxic red-tide dinoflagellate Alexandrium fundyense. J. Plankton Res., 20, 1241-1258. (Pubitemid 28362077)
62. Simon, M. and Rosenstock, B. (2007) Different coupling of dissolved amino acid, protein, and carbohydrate turnover to heterotrophic picoplankton production in the Southern Ocean in austral summer and fall. Limnol. Oceanogr., 52, 85-95. (Pubitemid 46972125)
63. Skoog, A., Whitehead, K., Sperling, F. et al. (2002) Microbial glucose uptake and growth along a horizontal nutrient gradient in the North Pacific. Limnol. Oceanogr., 47, 1676-1683. (Pubitemid 36016826)
64. Smith, D. C., Simon, M., Alldredge, A. L. et al. (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature, 359, 139-142. (Pubitemid 23374905)
65. Solomon, S. et al. (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK; New York, NY, USA.
66. Sommer, U., Aberle, N., Engel, A. et al. (2007) An indoor mesocosm system to study the effect of climate change on the late winter and spring succession of Baltic Sea phyto- and zooplankton. Oecologia, 150, 655-666.
67. Søndergaard, M., Williams, P. J. leB., Cauwet, G. et al. (2000) Net accumulation and flux of dissolved organic carbon and dissolved organic nitrogen in marine plankton communities. Limnol. Oceanogr., 45, 1097-1111. (Pubitemid 30597390)
68. Thingstad, T. F., Bellerby, R. G. J., Bratbak, G. et al. (2008) Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature, 455, 387-391.
69. Vazquez-Dominguez, E., Vaque, D. and Gasol, A. M. (2007) Ocean warming enhances respiration and carbon demand of coastal microbial plankton. Global Change Biol., 13, 1327-1334. (Pubitemid 47082271)
70. Verdugo, P., Alldredge, A., Azam, F. et al. (2004) The oceanic gel phase: a bridge in the DOM-POM continuum. Mar. Chem., 92, 67-85. (Pubitemid 39568987)
71. Verity, P. G. (1981) Effects of temperature, irradiance, and daylength on the marine diatom Leptocylindrus danicus Cleve. I. Photosynthesis and cellular composition. J. Exp. Mar. Biol. Ecol., 55, 79-91.
72. Verity, P. G. (1982) Effects of temperature, irradiance, and daylength on the marine diatom Leptocylindrus danicus Cleve. III. Dark respiration. J. Exp. Mar. Biol. Ecol., 60, 197-207.
73. Wakeham, S. G., Lee, C., Hedges, J. I. et al. (1997) Molecular indicators of diagenetic status in marine organic matter. Geochim. Cosmochim. Acta, 61, 5363-5369.
74. Wohlers, J., Engel, A., Zöllner, E. et al. (2009) Changes in biogenic carbon flow in response to sea surface warming. Proc. Natl Acad. Sci., 106, 7067-7072.
75. Wolfstein, K., Brouwer, J. F. C. and Stal, L. J. (2002) Biochemical partitioning of photosynthetically fixed carbon by benthic diatoms during short-term incubations at different irradiances. Mar. Ecol.-Prog. Ser., 245, 21-31. (Pubitemid 36108075)
76. Wood, M. A. and Van Valen, L. M. (1990) Paradox lost? On the release of energy-rich compounds by phytoplankton. Mar. Microb. Food Webs, 4, 103-116.