The utilization of polysaccharides by heterotrophic bacterioplankton in the Bay of Biscay (North Atlantic Ocean)

This study investigates the turnover of polysaccharides by heterotrophic bacterioplankton in the northern Bay of Biscay, a productive marine system on the continental margin of the temperate Atlantic Ocean. Bacterial biomass production (BBP) near the surface ranged from 0.5 to 25.7 nmol C L−1 h−1 during small phytoplankton blooms in May and June that occurred after the main spring bloom. A direct relationship between BBP and total polysaccharides strongly suggests the dependence of bacterial growth on the availability of semi-labile organic matter. Concentrations of combined glucose as well as rate constants of extracellular glucosidase activity and glucose uptake were determined to estimate the actual carbon fluxes from bacterial polysaccharide turnover. Results reveal that the degradation of polysaccharides in the upper 100 m of the water column sustained a glucose flux of 15.2–32.3 mg C m−2 d−1 that was available for bacterial consumption. The mean turnover time for polysaccharides was 170 and 165 days for α- and β-glycosidic linked polymers, respectively. Incorporation of free glucose supported 0.4–19.6% of BBP. The availability of nitrate plus nitrite (NOx) was identified as one factor increasing bacterial incorporation of glucose in most samples. Our results demonstrate that the bacterial recycling of polysaccharides generated a significant flux of organic carbon in microbial food-webs and biogeochemical processes.

[1]  U. Sommer,et al.  Effects of sea surface warming on the production and composition of dissolved organic matter during phytoplankton blooms: results from a mesocosm study , 2011 .

[2]  S. Doney,et al.  Oceanic heterotrophic bacterial nutrition by semilabile DOM as revealed by data assimilative modeling , 2010 .

[3]  L. Chou,et al.  Pelagic calcification and fate of carbonate production in marine systems , 2010 .

[4]  A. Engel,et al.  Acidification increases microbial polysaccharide degradation in the ocean , 2009 .

[5]  K. Sabbe,et al.  Abundance and size distribution of transparent exopolymer particles (TEP) in a coccolithophorid bloom in the northern Bay of Biscay , 2009 .

[6]  U. Riebesell,et al.  Effects of rising temperature on the formation and microbial degradation of marine diatom aggregates , 2009 .

[7]  Karl Kaiser,et al.  Biochemical Composition and Size Distribution of Organic Matter at the Pacific and Atlantic Time-Series Stations , 2009 .

[8]  M. Tedetti,et al.  Distribution and bacterial availability of dissolved neutral sugars in the South East Pacific , 2008 .

[9]  G. Kraus,et al.  Changing bacterioplankton growth characteristics on a large spatial scale: oligotrophic versus mesotrophic ocean , 2006 .

[10]  C. Duarte,et al.  Growth and grazing losses of prokaryotes in the central Atlantic Ocean , 2005 .

[11]  E. Laws,et al.  Global carbon cycle (communication arising): Metabolic balance of the open sea , 2003, Nature.

[12]  R. Anadón,et al.  Carbon flux through the microbial community in a temperate sea during summer: role of bacterial metabolism , 2003 .

[13]  K. Caldeira,et al.  Oceanography: Anthropogenic carbon and ocean pH , 2003, Nature.

[14]  K. Whitehead,et al.  Microbial glucose uptake and growth along a horizontal nutrient gradient in the North Pacific , 2002 .

[15]  M. Simon,et al.  Bacterioplankton dynamics in the Gulf of Aqaba and the northern Red Sea in early spring , 2002 .

[16]  G. Herndl,et al.  Changes in bacterial β‐glucosidase diversity during a coastal phytoplankton bloom , 2002 .

[17]  P. B. Duffy,et al.  Anthropogenic carbon and ocean pH , 2001 .

[18]  B. Biddanda,et al.  Bacterial utilization of dissolved glucose in the upper water column of the Gulf of Mexico , 1999 .

[19]  R. Anadón,et al.  Seasonal compensation of microbial production and respiration in a temperate sea , 1999 .

[20]  H. Ducklow.  The bacterial component of the oceanic euphotic zone , 1999 .

[21]  Manfred Ehrhardt,et al.  Methods of seawater analysis , 1999 .

[22]  Lei Chou,et al.  Distribution and Fluxes of Calcium Carbonatealong the Continental Margin in the Gulf of Biscay , 1998 .

[23]  D. Karl,et al.  ECTOAMINOPEPTIDASE SPECIFICITY AND REGULATION IN ANTARCTIC MARINE PELAGIC MICROBIAL COMMUNITIES , 1998 .

[24]  A. Bode,et al.  Abundance and production of pelagic bacteria in the southern Bay of Biscay during summer , 1998 .

[25]  Farooq Azam,et al.  Microbial Control of Oceanic Carbon Flux: The Plot Thickens , 1998, Science.

[26]  R. Benner,et al.  Aldoses in various size fractions of marine organic matter: Implications for carbon cycling , 1997 .

[27]  S. Wakeham,et al.  Molecular indicators of diagenetic status in marine organic matter , 1997 .

[28]  D. Kirchman,et al.  Concentration and composition of dissolved combined neutral sugars (polysaccharides) in seawater determined by HPLC−PAD , 1997 .

[29]  J. Vallino,et al.  Modeling bacterial utilization of dissolved organic matter: Optimization replaces Monod growth kinetics , 1996 .

[30]  K. Mopper,et al.  Automated High-Performance, High-Temperature Combustion Total Organic Carbon Analyzer , 1996 .

[31]  David C. Smith,et al.  Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea , 1996 .

[32]  H. Ducklow,et al.  Concentrations and uptake of neutral monosaccharides along 14°W in the equatorial Pacific: Contribution of glucose to heterotrophic bacterial activity and the DOM flux , 1996 .

[33]  D. Karl,et al.  Bacterial ectoenzymes in marine waters : activity ratios and temperature responses in three oceanographic provinces , 1995 .

[34]  P. Williams.  Evidence for the seasonal accumulation of carbon-rich dissolved organic material, its scale in comparison with changes in particulate material and the consequential effect on net CN assimilation ratios , 1995 .

[35]  D. Caron,et al.  The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda , 1995 .

[36]  J. Russell,et al.  Energetics of bacterial growth: balance of anabolic and catabolic reactions. , 1995, Microbiological reviews.

[37]  H. Ducklow,et al.  Annual flux of dissolved organic carbon from the euphotic zone in the northwestern Sargasso Sea , 1994, Nature.

[38]  David C. Smith,et al.  Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution , 1992, Nature.

[39]  T. Nakatsuka,et al.  Vertical fluxes and ecological significance of organic materials during the phytoplankton bloom during austral summer in Breid Bay, Antarctica , 1992 .

[40]  G. Schulz,et al.  Molecular architecture and electrostatic properties of a bacterial porin. , 1991, Science.

[41]  Michael L. Pace,et al.  The production of dissolved organic matter by phytoplankton and its importance to bacteria : patterns across marine and freshwater systems , 1991 .

[42]  R. Anadón,et al.  A persistent upwelling off the Central Cantabrian Coast (Bay of Biscay) , 1990 .

[43]  R. Benz,et al.  Permeation of hydrophilic molecules through the outer membrane of gram‐negativ bacteria , 1988 .

[44]  Sang-Jin Kim,et al.  Microbial Decomposition in Aquatic Environments: Combined Process of Extracellular Enzyme Activity and Substrate Uptake , 1988, Applied and environmental microbiology.

[45]  G. Cowie,et al.  Carbohydrate sources in a coastal marine environment , 1984 .

[46]  R. Y. Morita,et al.  Observations on microbial percent respiration values in arctic and subarctic marine waters and sediments , 1984, Microbial Ecology.

[47]  P. Holligan,et al.  Celtic Sea and Armorican current structure and the vertical distributions of temperature and chlorophyll , 1982 .

[48]  L. Pomeroy.  The Ocean's Food Web, A Changing Paradigm , 1974 .

[49]  S. A. Gross.  Storage of products , 1974 .

[50]  C. Yentsch,et al.  A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence , 1963 .

[51]  R. Lewin,et al.  Physiology and Biochemistry of Algae. , 1963 .

[52]  H. Bolhuis,et al.  Characterization of marine bacteria and the activity of their enzyme systems involved in degradation of the algal storage glucan laminarin. , 2007, FEMS microbiology ecology.

[53]  S. Schiavon,et al.  Climate Change 2007: Impacts, Adaptation and Vulnerability. , 2007 .

[54]  R. Benner.  Chapter 3 – Chemical Composition and Reactivity , 2002 .

[55]  Dennis A. Hansell,et al.  Biogeochemistry of marine dissolved organic matter , 2002 .

[56]  Dennis A. Hansell,et al.  Glucose fluxes and concentrations of dissolved combined neutral sugars (polysaccharides) in the Ross Sea and Polar Front Zone, Antarctica , 2001 .

[57]  J. Huthnance,et al.  Physical structures, advection and mixing in the region of Goban spur , 2001 .

[58]  L. Chou,et al.  The Carbon cycle at the Ocean Margin in the Northern Gulf of Biscay: The OMEX-I Project , 2000 .

[59]  A. Bianchi,et al.  Bacterial utilization of glucose in the water column from eutrophic to oligotrophic pelagic areas in the eastern North Atlantic Ocean , 1998 .

[60]  M. Gosselin,et al.  High bacterial production, uptake and concentrations of dissolved organic matter in the Central Arctic Ocean , 1997 .

[61]  R. Benner,et al.  Bacterial utilization of different size classes of dissolved organic matter , 1996 .

[62]  David C. Smith,et al.  A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine , 1992 .

[63]  D. Kirchman.  Incorporation of thymidine and leucine in the subarctic Pacific application to estimating bacterial production , 1992 .

[64]  G. Bratbak,et al.  Incorporation of viruses into the budget of microbial C-transfer A first approach , 1992 .

[65]  R. Chróst.  Environmental Control of the Synthesis and Activity of Aquatic Microbial Ectoenzymes , 1991 .

[66]  R. Chróst.  Microbial Enzymes in Aquatic Environments , 1991, Brock/Springer Series in Contemporary Bioscience.

[67]  J. Fuhrman,et al.  Nanomolar concentrations and rapid turnover of dissolved free amino acids in seawater: agreement between chemical and microbiological measurements , 1986 .

[68]  H. Hoppe.  Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates , 1983 .

[69]  T. Painter.  4 – Algal Polysaccharides , 1983 .