Contribution of combined carbohydrates to dissolved and particulate organic carbon after the spring bloom in the northern Bay of Biscay (North-Eastern Atlantic Ocean)
[en] Two cruises were conducted after the diatom spring bloom in the northern Bay of Biscay (2006, 2007), to assess the contribution of combined carbohydrates to organic carbon partitioning. Partitioning of total organic carbon (TOC) into particulate organic carbon (POC) and dissolved organic carbon (DOC) differed between the two years, particularly for depths above 60 m, and was related to the vernal development of the system: a post spring-bloom system in 2007, and a more stratified summer system with higher coccolithophore abundance in 2006. In general, contribution of POC to TOC ranged between 4 and 28% and decreased with depth. Concentration of high molecular weight (>1 kDa) dissolved combined carbohydrates (dCCHO) ranged from 0.6 to 1.4 µmol L−1 and contributed between 4 and 11% to DOC. Concentration of particulate combined carbohydrates (pCCHO) varied between 0.03 and 1.3 µmol L−1. A high contribution of pCCHO to POC was observed in 2007, i.e. 22–60% C compared to 3–10% C in 2006, and coincided with a higher abundance of transparent exopolymer particles (TEP). TEP accounted for 0.4–2.0 µmol C L−1 in 2007 and 0.5–1.5 µmol C L−1 in 2006. Above 60 m, differences in contribution of TEP-C to POC were most pronounced yielding 15.4±3.0% in 2007 compared to relatively low 4.8±1.4%, in 2006. TEP-C could explain about 60% in 2007 and about 40% of pCCHO-C in 2006. Hence, TEP were identified as a substantial component of pCCHO and POC, particularly in the wake of the spring bloom. Molecular composition of CCHO, i.e. HMW-dCCHO+pCCHO, revealed little difference between the years but strong variation over depth. Uronic acids (URA) were identified as a major component of CCHO (20–40%). Our study indicates that the distribution and composition of CCHO in surface seawater are determined by biogeochemical processes on a seasonal scale. A better knowledge of CCHO cycling and molecular signature has therefore a high potential for a better tracing of carbon dynamics in shelf sea ecosystems.
Harlay, Jérôme ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Océanographie chimique
Piontek, Judith; Alfred Wegener Institute (AWI)
Chou, Lei; Université Libre de Bruxelles - ULB > Laboratoire d'Océanographie Chimique et Géochimie des Eaux
Language :
English
Title :
Contribution of combined carbohydrates to dissolved and particulate organic carbon after the spring bloom in the northern Bay of Biscay (North-Eastern Atlantic Ocean)
Publication date :
15 August 2012
Journal title :
Continental Shelf Research
ISSN :
0278-4343
Publisher :
Pergamon Press - An Imprint of Elsevier Science, Oxford, United Kingdom
Alldredge A.L., Passow U., Logan B.E. The abundance and significance of a class of large, transparent organic particles in the ocean. Deep-Sea Research 1993, 40:1131-1140.
Aluwihare L.I., Repeta D.J., Chen R.F. A major biopolymeric component to dissolved organic carbon in surface sea water. Nature 1997, 387:166-169.
Anderson T.R., Williams P.J.leB. A one dimensional model of dissolved organic carbon cycling in the water column incorporating combined biological-photochemical decomposition. Global Biogeochemal Cycles 1999, 13:337-349.
Arnosti C. Speed bumps and barricades in the carbon cycle: substrate structural effects on carbon cycling. Marine Chemistry 2004, 92(1-4):263-273.
Azam F., Fenchel T., Field J.G., Gray J.S., Meyer-Reil L.A., Thingstad F. The ecological role of water column microbes in the sea. Marine Ecology Progress Series 1983, 10:257-263.
Azam F., Hodson R.E. Size distribution and activity of marine microheterotrophs. Limnology and Oceanography 1977, 22:492-501.
Benner R., Pakulski J.D., McCarthy M., Hedges J.I., Hatcher P.G. Bulk chemical characterization of dissolved organic matter in the ocean. Science 1992, 255:1561-1564.
Benner R. Chemical composition and reactivity. Biogeochemistry of Marine Dissolved Organic Matter 2002, Academic Press. D. Hansell, C.A. Carlson (Eds.).
Benz R., Bauer K. Permeation of hydrophilic molecules through the outer membrane of gram-negative bacteria. European Journal of Biochemistry 1988, 176:1-19.
Biddanda B., Benner R. Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnology and Oceanography 1997, 42:506-518.
Borch N.H., Kirchman D.L. Concentration and composition of dissolved combined neutral sugars (combined carbohydrates) in seawater determined by HPLC-PAD. Marine Chemistry 1997, 57:85-95.
Borchard C., Engel A. Organic matter exudation by Emiliania huxleyi under simulated future ocean conditions. Biogeosciences Disc. 2012, 9:1199-1236.
Carlson C.A. Production and removal processes. Biogeochemistry of Marine Dissolved Organic Matter 2002, Academic Press. D. Hansell, C.A. Carlson (Eds.).
Cho B.C., Azam F. Major role of bacteria in biogeochemical fluxes in the ocean's interior. Nature 1988, 332:441-443.
Chin W., Orellana M.V., Verdugo P. Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 1998, 391:568-572.
Copping A.E., Lorenzen C.J. Carbon budget of marine phytoplankton-herbivore system with carbon-14 as tracer. Limnology and Oceanography 1980, 25:873-882.
Decho A.W. Microbial exopolymer secretions in the ocean environments their role(s) in food webs and marine processes. Oceanography and Marine Biology Annual Reviews 1990, 28:73-153.
Engel A., Passow U. Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their Alcian Blue adsorption. Marine Ecology Progress Series 2001, 219:1-10.
Engel A., Thoms S., Riebesell U., Rochelle-Newall E., Zondervan I. Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature 2004, 428:929-932.
Engel A. Determination of Marine Gel Particles, Practical Guidelines for the Analysis of Seawater 2009, 125-142. CRC Press. Oliver Wurl Boca Raton [u.a.] (Ed.).
Engel A., Händel N., Wohlers J., Lunau M., Grossart H.-P., Sommer U., Riebesell U. 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 2011, 33(3):357-372.
Engel A., Händel N. A novel protocol for determining the concentration and composition of sugars in particulate and in high molecular weight dissolved organic matter (HMW-DOM) in seawater. Marine Chemistry 2011, 127:180-191.
Fogg G.E. The extracellular products of algae. Marine Biology Annual Review 1966, 4:195-212.
Fichtinger-Schepman A.M., Kamerling J.P., Vliegenthart J.F.G., de Jong E.W., Bosc L., Westbroek P. Composition of a methylated, acidic polysaccharide associated with coccoliths of Emiliania huxleyi (Lohmann) Kamptner. Carbohydrate Research 1979, 69:181-189.
Fuhrman J.A. Marine viruses and their biogeochemical and ecological effects. Nature 1999, 399:541-548.
Giroldo D., Vieira A.A.H., Paulsen B.S. Extracellular polysaccharides produced by a tropical cryptophyte as a carbon source for natural bacterial populations. European Journal of Phycology 2005, 40(3):241-249.
Godoi R.H.M., Aerts K., Harlay J., Kaegi R., Ro Chul-Un, Chou L., Van Grieken R. Organic surface coating on Coccolithophores-Emiliania huxleyi: its determination and implication in the marine carbon cycle. Microchemical Journal 2009, 91:266-271. 10.1016/j.microc.2008.12.009.
Goldberg S.J., Carlson C.A., Hansell D.A., Nelson N.B., Siegel D.A. Temporal dynamics of dissolved combined neutral sugars and the quality of dissolved organic matter in the Northwestern Sargasso Sea. Deep-Sea Research I 2009, 56:672-685.
Guo L., Hung C.C., Santschi P.H., Walsh I.D. 234Th scavenging and its relationship to acid polysaccharide abundance in the Gulf of Mexico. Marine Chemistry 2002, 78:103-119.
Hansell D.A. DOC in the global ocean carbon cycle. Biogeochemistry of Marine Dissolved Organic Matter 2002, 685-715. Academic Press, San Diego. D.A. Hansell, C.A. Carlson (Eds.).
Hansell D.A., Carlson C.A., Repeta J.D., Schlitzer R. Dissolved organic matter in the ocean. A controversy stimulates new insights. Oceanography 2009, 22:202-211.
Harlay J., De Bodt C., Engel A., Jansen S., d'Hoop Q., Piontek J., Van Oostende N., Groom S., Sabbe K., Chou L. Abundance and size distribution of transparent exopolymer particles (TEP) in a coccolithophorid bloom in the northern Bay of Biscay. Deep-Sea Research I 2009, 56:1251-1265.
Harlay J., Chou L., De Bodt C., Van Oostende N., Piontek J., Suykens K., Engel A., Sabbe K, Groom S., Delille B., Borges A.V. Biogeochemistry and carbon mass balance of a coccolithophore bloom in the northern Bay of Biscay (June 2006). Deep-Sea Research I 2010, 58:111-127.
Hopkinson C.S., Vallino J.J. Efficient export of carbon to the deep ocean through dissolved organic matter. Nature 2005, 433:142-145.
Hydes D.J., Le Gall A.C., Miller A.E.J., et al. Supply and demand of nutrients and dissolved organic matter at and across the NW European shelf break in relation to hydrography and biogeochemical activity. Deep-Sea Research II 2001, 48(14-15):3023-3047.
Ittekkot V., Brockmann U., Michaelis W., Degens E.T. Dissolved Free and Combined Carbohydrates during a Phytoplankton Bloom in the Northern North Sea. Marine Ecology Progress Series 1981, 4:299-305.
Jiao N., Herndl G.J., Hansell D.A., et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Reviews Microbiology 2010, 8:593-599.
Kaiser K., Benner R. Biochemical composition and size distribution of organic matter at the Pacific and Atlantic time series stations. Marine Chemistry 2009, 119:63-77.
Keir R.S., Rehder G., Frankignoulle M. Partial pressure and air-sea flux of CO 2 in the Northeast Atlantic during September 1995. Deep-Sea Research II 2001, 48(14-15):3179-3189.
Kirchman D.L., Meon B., Ducklow H.W., Carlson C.A., Hansell D.A., Steward G.F. Glucose fluxes and concentrations of dissolved combined neutral sugars (polysaccharides) in the Ross Sea and Polar Front Zone, Antarctica. Deep Sea Research Part II, Topical Studies in Oceanography 2001, 48(19-20):4179-4197.
Leppard G.G. The characterization of algal and microbial mucilage's and their aggregates in aquatic ecosystems. Science of the Total Environment 1995, 165:103-131.
Mann K.H., Lazier J.R.N. Dynamics of Marine Ecosystems. Biological-Physical Interactions in the Oceans 1991, Blackwell Scientific Publications, Cambridge, 466 pp.
Mari X., Burd A. Seasonal size spectra of transparent exopolymeric particles (TEP) in a coastal sea and comparison with those predicted using coagulation theory. Marine Ecology Progress Series 1998, 163:63-76.
Mari X. Carbon content and C:N ratio of transparent exopolymeric particles (TEP) produced by bubbling exudates of diatoms. Marine Ecology Progress Series 1999, 183:59-71.
Mopper K., Zhou J., Ramana K.S., Passow U., Dam H.G., Drapeau D.T. The role of surface-active carbohydrates in the flocculation of a diatom bloom in a mesocosm. Deep-Sea Research II 1995, 42:47-73.
Myklestad S. Production of carbohydrates by marine planktonic diatoms. II Influence of the N/P ratio in the growth medium on the assimilation ratio, growth rate and production of cellular and extracellular carbohydrates by Chaetoceros affinis var Willei (Gran) Hustedt and Skeletonema costatum (Grev) Cleve. Journal of Experimental Marine Biology and Ecology 1977, 29:161-179.
Nagata T. Production mechanisms of dissolved matter. Microbial Ecology of the Oceans 2000, 121-152. Wiley-Liss, New York. D.L. Kirchmann (Ed.).
Ogawa H., Amagai Y., Koike I., Kaiser K., Benner R. Production of refractory dissolved organic matter by bacteria. Science 2001, 292:917-920.
Pakulski J.D., Benner R. Abundance and distribution of carbohydrates in the ocean. Limnology and Oceanography 1994, 39:930-940.
Panagiotopoulos C., Sempéré R. Analytical methods for the determination of sugars in marine samples, a historical perspective and future directions. Limnology and Oceanography Methods 2005, 3:419-453.
Parsons T.R., Takahashi M., Hargrave B. Biological Oceanographic Processes 1983, Pergamon Press, Oxford, UK. third ed.
Passow U. Transparent exopolymer particles (TEP) in aquatic environments. Progress in Oceanography 2002, 55:287-333.
Piontek J., Händel N., de Bodt C., Harlay J., Chou L., Engel A. The utilization of polysaccharides by heterotrophic bacterioplankton in the Bay of Biscay (North Atlantic Ocean). Journal of Plankton Research 2011, 33:1719-1735.
Qian J., Mopper K. An automated, high performance, high temperature combustion dissolved organic carbon analyzer. Analytical Chemistry 1996, 68:3090-3097.
Quigley M.S., Santschi P.H., Hung C.-C., Guo L., Honeyman B.D. Importance of acid polysaccharides for 234Th complexation to marine organic matter. Limnology and Oceanography 2002, 47:367-377.
Ramus J. Alcian Blue, a quantitative aqueous assay for algal acid and sulfated polysaccharides. Journal of Phycology 1977, 13:345-348.
Skoog A., Benner R. Aldoses in various size fractions of marine organic matter, implications for carbon cycling. Limnology and Oceanography 1997, 42:1803-1813.
Skoog A., Alldredge A., Passow U., Dunne J., Murray J. Neutral aldoses as source indicators for marine snow. Marine Chemistry 2008, 108:195-206.
Simon M, Grossart HP, Schweitzer B, et al. Microbial ecology of organic aggregates in aquatic ecosystems. Aquatic Microbial Ecology 2002, 28(2):175-211.
Smith D.C., Simon M., Alldredge A.L., Azam F. Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 1992, 359:139-142.
Steigenberger S., Statham P.J., Voelker C., Passow U. The role of polysaccharides and diatom exudates in the redox cycling of Fe and the photoproduction of hydrogen peroxide in coastal seawaters. Biogeosciences 2010, 7(1):109-119.
Strom S.L., Benner R., Ziegler S., Dagg M.J. Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnology and Oceanography 1997, 42(6):1364-1374.
Suárez I., Marañon E. Photosynthate allocation in a temperate sea over an annual cycle, the relationship between protein synthesis and phytoplankton physiological state. Journal of Sea Research 2003, 50:285-299.
Tomshich S.V., Komandrova N.A., Widmalm G, Nedashkovskaya O.I., Shashkov A.S., Perepelov A.V. Structure of acidic o-specific polysaccharide from the marine bacterium Cellulophaga baltica. Russian Journal of Bioorganic Chemistry 2007, 33(1):83-87.
van Oostende, N., Harlay, J., Vanelslander, B., Chou, L., Sabbe, K. Phytoplankton community dynamics during late spring coccolithophore blooms at the continental margin of the Celtic Sea (North East Atlantic, 2006-2008). Progress in Oceanography, forthcoming.
Verdugo P., Santschi P.H. Polymer dynamics of DOC networks and gel formation in seawater. Deep-Sea Research II 2010, 57(16):1486-1493.
Wakeham S.G., Lee C., Hedges J.I., Hernes P.J., Peterson M.L. Molecular indicators of diagenetic status in marine organic matter. Geochimica et Cosmochimica Acta 1997, 61:5363-5369.
Weiss M.S., Abele U., Weckesser J., Welte W., Schiltz E., Schulz G.E. Molecular architecture and electrostatic properties of a bacterial porin. Science 1991, 254:1627-1630.
Yentsch C.S., Menzel D.W. A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Research and Oceanographic Abstracts 1963, 10:221-231.
Zhou J., Mopper K., Passow U. The role of surface active carbohydrates in the formation of transparent exopolymer particles by bubble adsorption of seawater. Limnology and Oceanography 1998, 43:1860-1871.