Seasonal variability in phytoplankton stable carbon isotope ratios and bacterial carbon sources in a shallow Dutch lake

Ecosystem metabolism of lakes strongly depends on the relative importance of local vs. allochthonous carbon sources and on microbial food‐web functioning and structure. Over the year ecosystem metabolism varies as a result of seasonal changes in environmental parameters such as nutrient levels, light, temperature, and variability in the food web. This is reflected in isotopic compositions of phytoplankton and bacteria. Here, we present the results of a 17‐month study on carbon dynamics in two basins of Lake Naarden, The Netherlands. One basin was restored after anthropogenic eutrophication, whereas the other basin remained eutrophic. We analyzed natural stable carbon isotope abundances (δ13C) of dissolved inorganic carbon, dissolved organic carbon and macrophytes, and combined these data with compound‐specific δ13C analyses of phospholipid‐derived fatty acids, produced by phytoplankton and bacteria. Isotopic fractionation (ε) between phytoplankton biomass and CO2(aq) was similar for diatoms and other eukaryotic phytoplankton, and differences between sampling sites were small. Highest ε values were observed in winter with values of 23.5 ± 0.6‰ for eukaryotic phytoplankton and 13.6 ± 0.3‰ for cyanobacteria. Lowest ε values were observed in summer: 10.5 ± 0.3‰ for eukaryotic phytoplankton and 2.7 ± 0.1‰ for cyanobacteria. The annual range in δ13Cbact was between 6.9‰ and 8.2‰ for the restored and eutrophic basin, respectively, while this range was between 11.6‰ and 13.1‰ for phytoplankton in the restored and eutrophic basin, respectively. Correlations between δ13Cphyto and δ13Cbact were strong at both sites. During summer and fall, bacterial biomass derives mainly from locally produced organic matter, with minor allochthonous contributions. Conversely, during winter, bacterial dependence on allochthonous carbon was 39–77% at the restored site, and 17–46% at the eutrophic site.

[1]  A. W. Galloway,et al.  Terrestrial carbohydrates support freshwater zooplankton during phytoplankton deficiency , 2016, Scientific Reports.

[2]  Dedmer B. Van de Waal,et al.  CO2-dependent carbon isotope fractionation in dinoflagellates relates to their inorganic carbon fluxes , 2016, Journal of experimental marine biology and ecology.

[3]  E. Peltomaa,et al.  Lake zooplankton δ13C values are strongly correlated with the δ13C values of distinct phytoplankton taxa , 2016 .

[4]  C. Biasi,et al.  Inferring Phytoplankton, Terrestrial Plant and Bacteria Bulk δ¹³C Values from Compound Specific Analyses of Lipids and Fatty Acids , 2015, PloS one.

[5]  G. Reichart,et al.  Stable carbon isotope fractionation of organic cyst-forming dinoflagellates: Evaluating the potential for a CO2 proxy , 2015 .

[6]  E. Jeppesen,et al.  Macrophytes and periphyton carbon subsidies to bacterioplankton and zooplankton in a shallow eutrophic lake in tropical China , 2015 .

[7]  G. Reichart,et al.  Stable carbon isotope fractionation of organic cyst-forming dinoflagellates : Evaluating the potential for a CO 2 proxy , 2015 .

[8]  A. Borges,et al.  Biogeochemistry of a large and deep tropical lake (Lake Kivu, East Africa: insights from a stable isotope study covering an annual cycle , 2014 .

[9]  J. Downing,et al.  Stable carbon isotope biogeochemistry of lakes along a trophic gradient , 2014 .

[10]  M. Brett Are phytoplankton in northern Swedish lakes extremely 13C depleted? , 2014 .

[11]  J. Middelburg Stable isotopes dissect aquatic food webs from the top to the bottom , 2014 .

[12]  A. W. Galloway,et al.  Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in 7 classes by 5 , 2016 .

[13]  Edward G. Stets,et al.  Inorganic carbon loading as a primary driver of dissolved carbon dioxide concentrations in the lakes and reservoirs of the contiguous United States , 2013 .

[14]  M. Pace,et al.  Difficulty in Discerning Drivers of Lake Ecosystem Metabolism with High-Frequency Data , 2011, Ecosystems.

[15]  S. Carpenter,et al.  Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen , 2011, Proceedings of the National Academy of Sciences.

[16]  J. Middelburg,et al.  Phytoplankton-bacteria coupling under elevated CO 2 levels: a stable isotope labelling study , 2010 .

[17]  Jonathan J. Cole,et al.  Lake metabolism and the diel oxygen technique: State of the science , 2010 .

[18]  Hari Seshan,et al.  Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production , 2009, Proceedings of the National Academy of Sciences.

[19]  John M. Melack,et al.  Lakes and reservoirs as regulators of carbon cycling and climate , 2009 .

[20]  R. Evershed,et al.  A simple modification of a silicic acid lipid fractionation protocol to eliminate free fatty acids from glycolipid and phospholipid fractions. , 2009, Journal of microbiological methods.

[21]  J. Middelburg,et al.  Autochthonous and allochthonous contributions to mesozooplankton diet in a tidal river and estuary: Integrating carbon isotope and fatty acid constraints , 2009 .

[22]  J. Cole,et al.  Dissolved CO 2 , 2009 .

[23]  Gene E. Likens,et al.  Encyclopedia of Inland Waters , 2009 .

[24]  J. Middelburg,et al.  A versatile method for stable carbon isotope analysis of carbohydrates by high-performance liquid chromatography/isotope ratio mass spectrometry. , 2008, Rapid communications in mass spectrometry : RCM.

[25]  Aaron I. Packman,et al.  Biophysical controls on organic carbon fluxes in fluvial networks , 2008 .

[26]  J. Marty,et al.  Comparison of methods to determine algal δ13C in freshwater , 2008 .

[27]  S. Carpenter,et al.  Does terrestrial organic carbon subsidize the planktonic food web in a clear‐water lake? , 2007 .

[28]  K. Sand‐Jensen,et al.  Temporal dynamics and regulation of lake metabolism , 2007 .

[29]  J. Downing,et al.  Plumbing the Global Carbon Cycle: Integrating Inland Waters into the Terrestrial Carbon Budget , 2007, Ecosystems.

[30]  J. Kromkamp,et al.  Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition , 2006 .

[31]  A. Sessions,et al.  Isotope-ratio detection for gas chromatography. , 2006, Journal of separation science.

[32]  S. Carpenter,et al.  Differential support of lake food webs by three types of terrestrial organic carbon. , 2006, Ecology letters.

[33]  Stefan Schouten,et al.  Seasonal Variation in the Stable Carbon Isotopic Composition of Algal Lipids in a Shallow Anoxic Fjord: Evaluation of the Effect of Recycling of Respired CO2 on the δ13C of Organic Matter , 2006, American Journal of Science.

[34]  J. Cole,et al.  Impact of chemically enhanced diffusion on dissolved inorganic carbon stable isotopes in a fertilized lake , 2006 .

[35]  B. Ibelings,et al.  The effects of biomanipulation on the biogeochemistry, carbon isotopic composition and pelagic food web relations of a shallow peat lake , 2005 .

[36]  R. Pel,et al.  Analysis of planktonic community structure and trophic interactions using refined isotopic signatures determined by combining fluorescence‐activated cell sorting and isotope‐ratio mass spectrometry , 2004 .

[37]  J. Finlay Patterns and controls of lotic algal stable carbon isotope ratios , 2004 .

[38]  S. Carpenter,et al.  Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs , 2004, Nature.

[39]  D. White,et al.  Determination of the sedimentary microbial biomass by extractible lipid phosphate , 2004, Oecologia.

[40]  M. Salkinoja-Salonen,et al.  Cellular fatty acids as chemotaxonomic markers of the genera Anabaena, Aphanizomenon, Microcystis, Nostoc and Planktothrix (cyanobacteria). , 2002, International journal of systematic and evolutionary microbiology.

[41]  J. Middelburg,et al.  Stable isotopes and biomarkers in microbial ecology. , 2002, FEMS microbiology ecology.

[42]  H. Cypionka,et al.  Phospholipid analysis as a tool to study complex microbial communities in marine sediments. , 2002, Journal of microbiological methods.

[43]  U. Riebesell,et al.  Light‐dependent carbon isotope fractionation in the coccolithophorid Emiliania huxleyi , 2002 .

[44]  Roger Jones,et al.  Seasonal changes in the importance of the source of organic matter to the diet of zooplankton in Loch Ness, as indicated by stable isotope analysis , 2001 .

[45]  W. Vermaas Photosynthesis and Respiration in Cyanobacteria , 2001 .

[46]  J. Hayes Fractionation of Carbon and Hydrogen Isotopes in Biosynthetic Processes , 2001 .

[47]  C. Heip,et al.  The fate of intertidal microphytobenthos carbon: An in situ 13C‐labeling study , 2000 .

[48]  Aat Barendregt,et al.  Effectiveness of reducing external nutrient load entering a eutrophicated shallow lake ecosystem in the Naardermeer nature reserve, The Netherlands , 1999 .

[49]  U. Riebesell,et al.  Stable carbon isotope fractionation by marine phytoplankton in response to daylength, growth rate, and CO2 availability , 1999 .

[50]  F. Morel,et al.  A model of carbon isotopic fractionation and active carbon uptake in phytoplankton , 1999 .

[51]  J. Keeley Photosynthetic pathway diversity in a seasonal pool community , 1999 .

[52]  C. Hopkinson,et al.  13C/12C composition of marine dissolved organic carbon , 1998 .

[53]  K. Grice,et al.  Biosynthetic effects on the stable carbon isotopic compositions of algal lipids: implications for deciphering the carbon isotopic biomarker record , 1998 .

[54]  R. Parkes,et al.  Direct linking of microbial populations to specific biogeochemical processes by 13C-labelling of biomarkers , 1998, Nature.

[55]  K. L. Hanson,et al.  Effect of Phytoplankton Cell Geometry on Carbon Isotopic Fractionation , 1998 .

[56]  M. I C H A E,et al.  The role of highly unsaturated fatty acids in aquatic foodweb processes , 1997 .

[57]  M. Sierszen,et al.  Analysis of a Lake Superior coastal food web with stable isotope techniques , 1996 .

[58]  Stephen A. Macko,et al.  Dependence of phytoplankton carbon isotopic composition on growth rate and [CO2)aq: Theoretical considerations and experimental results , 1995 .

[59]  G. Kling,et al.  Carbon Dioxide Supersaturation in the Surface Waters of Lakes , 1994, Science.

[60]  L. Forney,et al.  Accuracy, Reproducibility, and Interpretation of Fatty Acid Methyl Ester Profiles of Model Bacterial Communities , 1994, Applied and environmental microbiology.

[61]  Paul J. Harrison,et al.  Estimating carbon, nitrogen, protein, and chlorophyll a from volume in marine phytoplankton , 1994 .

[62]  G. Kling,et al.  Stable Isotopes and Planktonic Trophic Structure in Arctic Lakes , 1992 .

[63]  T. Kaneda Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance , 1991 .

[64]  T. Kaneda,et al.  Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. , 1991, Microbiological reviews.

[65]  J. Ehleringer,et al.  Carbon Isotope Discrimination and Photosynthesis , 1989 .

[66]  M. O'Leary,et al.  Carbon Isotopes in PhotosynthesisFractionation techniques may reveal new aspects of carbon dynamics in plants , 1988 .

[67]  M. Pace,et al.  Bacterial production in fresh and saltwater ecosystems: a cross-system overview , 1988 .

[68]  B. Peterson,et al.  STABLE ISOTOPES IN ECOSYSTEM , 1987 .

[69]  B. Peterson,et al.  STABLE ISOTOPES IN ECOSYSTEM STUDIES , 1987 .

[70]  J. Patton,et al.  The effect of organic matter and oxygen on the degradation of bacterial membrane lipids in marine sediments , 1986 .

[71]  W. J. Lucas,et al.  Inorganic carbon transport in aquatic photosynthetic organisms , 1985 .

[72]  H. Buser,et al.  Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts , 1983 .

[73]  W. G. Mook,et al.  CARBON ISOTOPE FRACTIONATION BETWEEN DISSOLVED BICARBONATE AND GASEOUS CARBON-DIOXIDE , 1974 .

[74]  R. Guillard,et al.  Metabolic fractionation of carbon isotopes in marine plankton—I. Temperature and respiration experiments , 1968 .

[75]  M. Keller,et al.  Photosynthesis and respiration , 2020, The Science of Grapevines.