Abstract
Under higher atmospheric CO2 concentrations, increases in soil moisture and, hence in terrestrial-aquatic carbon transfer are probable. In a coupled terrestrial-aquatic experiment we examined the direct (e.g. through changes in the CO2 water concentration) and indirect (e.g. through changes in the quality and quantity of soil leachates) effects of elevated CO2 on a lake microbial community. The incubation of soils under elevated CO2 resulted in an increase in the volume of leachates and in both chromophoric dissolved organic matter (CDOM) absorption and fluorescence in leachate. When this leachate was added to lake water during a 3-day aquatic incubation, we observed negative direct effects of elevated CO2 on photosynthetic microorganism abundance and a positive, indirect effect on heterotrophic microbial community cell abundances. We also observed a strong, indirect impact on the functional structure of the community with higher metabolic capacities under elevated CO2 along with a significant direct effect on CDOM absorption. All of these changes point to a shift towards heterotrophic processes in the aquatic compartment under higher atmospheric CO2 concentrations.
This is a preview of subscription content, log in via an institution to check access.
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
Change history
30 April 2018
Under higher atmospheric CO2 concentrations.
References
Adair EC, Reich PB, Trost JJ, Hobbie SE (2011) Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture. Glob Chan Biol 17:3546–3563 https://doi.org/10.1111/j.1365-2486.2011.02484.x
Blough NV, Del Vecchio R (2002) Chromophoric dissolved organic matter in the coastal environment. In: Hansell D, Carlson C (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, New York, pp 509–546
Butcher JB, Johnson TE, Nover D, Sarkar S (2014) Incorporating the effects of increased atmospheric CO2 in watershed model projections of climate change impacts. J Hydrol 513:322–334 https://doi.org/10.1016/j.jhydrol.2014.03.073
Causse J et al (2015) Field and modelling studies of Escherichia coli loads in tropical streams of montane agro-ecosystems. J Hydro-Environ Res 9:496–507. https://doi.org/10.1016/j.jher.2015.03.003
Caverly E, Kaste JM, Hancock GS, Chambers RM (2013) Dissolved and particulate organic carbon fluxes from an agricultural watershed during consecutive tropical storms. Geophys Res Lett 40:5147–5152. https://doi.org/10.1002/grl.50982
Cole JJ, Caraco NF (2001) Carbon in catchments: connecting terrestrial carbon losses with aquatic metabolism. Mar Freshwa Res 52:101–110
Cole JJ, Carpenter SR, Pace ML, Van de Bogert MC, Kitchell JL, Hodgson JR (2006) Differential support of lake food webs by three types of terrestrial organic carbon. Ecol Lett 9:558–568
Danger M, Leflaive J, Oumarou C, Ten-Hage L, Lacroix G (2007a) Control of phytoplankton–bacteria interactions by stoichiometric constraints. Oikos 116:1079–1086. https://doi.org/10.1111/j.0030-1299.2007.15424.x
Danger M, Oumarou C, Benest D, Lacroix G (2007b) Bacteria can control stoichiometry and nutrient limitation of phytoplankton. Func Ecol 21:202–210. https://doi.org/10.1111/j.1365-2435.2006.01222.x
Del Vecchio R, Blough NV (2004) Spatial and seasonal distribution of chromophoric dissolved organic matter and dissolved organic carbon in the Middle Atlantic Bight. Mar Chem 89:169–187
Dhillon GS, Inamdar S (2013) Extreme storms and changes in particulate and dissolved organic carbon in runoff: Entering uncharted waters? Geophys Res Lett 40:1322–1327. https://doi.org/10.1002/grl.50306
Dimitriou E (2011) Overland flow. In: Gliński J, Horabik J, Lipiec J (eds) Encyclopedia of agrophysics. Springer Netherlands, Dordrecht, pp 536–536. https://doi.org/10.1007/978-90-481-3585-1_104
Drigo B et al. (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci 107:10938–10942. https://doi.org/10.1073/pnas.0912421107
Endres S, Galgani L, Riebesell U, Schulz K-G, Engel A (2014) Stimulated bacterial growth under elevated pCO2: results from an off-shore mesocosm study. PLoS One 9:e99228. https://doi.org/10.1371/journal.pone.0099228
Faithfull CL, Mathisen P, Wenzel A, Bergstrom AK, Vrede T (2015) Food web efficiency differs between humic and clear water lake communities in response to nutrients. and light. Oecologia 177:823–835. https://doi.org/10.1007/s00442-014-3132-2
Fasching C, Ulseth AJ, Schelker J, Steniczka G, Battin TJ (2016) Hydrology controls dissolved organic matter export and composition in an Alpine stream and its hyporheic. zone. Limnol Oceanogr 61:558–571
Fey SB, Mertens AN, Beversdorf LJ, McMahon KD, Cottingham KL (2015) Recognizing cross-ecosystem responses to changing temperatures: soil warming impacts pelagic food webs. Oikos 124:1473–1481. https://doi.org/10.1111/oik.01939
Field CB, Jackson RB, Mooney HA (1995) Stomatal responses to increased CO2: implications from the plant to the global scale. Plant, Cell Environ 18:1214–1225 https://doi.org/10.1111/j.1365-3040.1995.tb00630.x
Gómez-Consarnau L, Lindh MV, Gasol JM, Pinhassi J (2012) Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ Microbiol 14:2361–2378. https://doi.org/10.1111/j.1462-2920.2012.02804.x
Gravel D, Guichard F, Loreau M, Mouquet N (2010) Source and sink dynamics in meta-ecosystems. Ecology 91:2172–2184
Green SA, Blough NV (1994) Optical absorption and fluorescence properties of chromophoric dissolved organic matter in natural waters. Limnol Oceanogr 39:1903–1916
Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH, Scanlan DJ, Zubkov MV (2012) Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc Natl Acad Sci USA 109:5756–5760. https://doi.org/10.1073/pnas.1118179109
Harvey E, Gounand I, Ganesanandamoorthy P, Altermatt F (2016) Spatially cascading effect of perturbations in experimental meta-ecosystems. Proc R Soc B: Biol Sci. https://doi.org/10.1098/rspb.2016.1496
Harvey E, Gounand I, Ward CL, Altermatt F (2017) Bridging ecology and conservation: from ecological networks to ecosystem function. J Appl Ecol 54:371–379. https://doi.org/10.1111/1365-2664.12769
Hedges JI (1992) Global biogeochemical cycles: progress and problems. Mar Chem 39:67–93
Helms JR, Stubbins A, Ritchie RD, Minor EC, Kieber DJ, Mopper K (2008) Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter. Limnol Oceanogr 53:955–969
Hill PW, Garnett MH, Farrar J, Iqbal Z, Khalid M, Soleman N, Jones DL (2015) Living roots magnify the response of soil organic carbon decomposition to temperature in temperate grassland. Glob Chan Biol 21:1368–1375. https://doi.org/10.1111/gcb.12784
Hillel D (2003) 14—Water entry into soil. In: Introduction to environmental soil physics (first). Academic Press, Burlington, pp 259–282. https://doi.org/10.1016/B978-012348655-4/50015-0
Hoekman D (2010) Turning up the heat: Temperature influences the relative importance of top-down and bottom-up effects. Ecology 91:2819–2825. https://doi.org/10.1890/10-0260.1
Hoge FE, Vodacek A, Blough NV (1993) Inherent optical properties of the ocean—retrieval of the absorption coefficient of chromophoric dissolved organic matter from fluorescence measurements. Limnol Oceanogr 38:1394–1402
Hungate BA (1999) Ecosystems responses to rising atmospheric CO2: feedbacks through the Nitrogen cycle. In: Luo Y, Mooney HA (eds) Carbon dioxide and environmental stress. Academic Press, San Diego, pp 265–285
IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to Fifth Assesment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9781107415324
Ishii SKL, Boyer TH (2012) Behavior of reoccurring PARAFAC components in fluorescent dissolved organic matter in natural and engineered systems: a critical review. Environ Sci Tech 46:2006–2017. https://doi.org/10.1021/es2043504
Jacinthe PA, Lal R, Owens LB, Hothem DL (2004) Transport of labile carbon in runoff as affected by land use and rainfall characteristics. Soil Tillage Res 77:111–123. https://doi.org/10.1016/j.still.2003.11.004
Janeau JL et al (2014) Soil erosion, dissolved organic carbon and nutrient losses under different land use systems in a small catchment in northern Vietnam. Ag Wat Man 146:314–323. https://doi.org/10.1016/j.agwat.2014.09.006
Jansson M, Karlsson J, Jonsson A (2012) Carbon dioxide supersaturation promotes primary production in lakes. Ecol Lett 15:527–532. https://doi.org/10.1111/j.1461-0248.2012.01762.x
Jones RI (2000) Mixotrophy in planktonic protists: an overview FreshwBiol 45:219–226 https://doi.org/10.1046/j.1365-2427.2000.00672.x
Karlsson J, Bystrom P, Ask J, Ask P, Persson L, Jansson M (2009) Light limitation of nutrient-poor lake ecosystems. Nature 460:506–509
Kritzberg ES, Cole JJ, Pace ML, Granéli W, Bade DL (2004) Autochthonous versus allochthonous carbon sources of bacteria: results from whole-lake 13C addition experiments. Limnol Oceanogr 49:588–596 https://doi.org/10.4319/lo.2004.49.2.0588
Le TH et al (2016) Responses of aquatic bacteria to terrestrial runoff: effects on community structure and key taxonomic groups. Front Microbiol: Aquatic Microbiol. https://doi.org/10.3389/fmicb.2016.00889
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876 https://doi.org/10.1093/jxb/erp096
Loreau M, Mouquet N, Holt RD (2003) Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecol Lett 6:673–679. https://doi.org/10.1046/j.1461-0248.2003.00483.x
Low-Décarie E, Fussmann GF, Bell G (2014) Aquatic primary production in a high-CO2 world. Trends Ecol Evolut 29:223–232 https://doi.org/10.1016/j.tree.2014.02.006
Maberly SC (1996) Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. FreshwBiol 35:579–598
Maberly SC, Barker PA, Stott AW, De Ville MM (2013) Catchment productivity controls CO2 emissions from lakes. Nat Clim Change 3
Mailapalli D, Horwath W, Wallender W, Burger M (2012) Infiltration, runoff, and export of dissolved organic carbon from furrow-irrigated forage fields under cover crop and no-till management in the arid climate of California. J Irrig Drain Eng 138:35–42 doi. https://doi.org/10.1061/(ASCE)IR.1943-4774.0000385
Malcolm RL (1990) The uniqueness of humic substances in each of soil, stream and marine environments. Anal Chim Acta 232:19–30
Marie D, Partensky F, Jacquet S, Vaulot D (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol 63:186–193
Nakagawa S, Schielzeth H, O’Hara RB (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142
Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci 98:166–170. https://doi.org/10.1073/pnas.98.1.166
Nelson NB, Siegel DA, Michaels AF (1998) Seasonal dynamics of colored dissolved material in the sargasso sea deep-sea research part. I-Oceanogr Res Papers 45:931–957
Nelson NB, Carlson CA, Steinberg DK (2004) Production of chromophoric dissolved organic matter by Sargasso Sea microbes. Mar Chem 89:273–287
Niboyet A et al. (2011) Testing interactive effects of global environmental changes on soil nitrogen cycling. Ecosphere. https://doi.org/10.1890/es10-00148.1
Niboyet A, Bardoux G, Barot S, Bloor JMG (2017) Elevated CO2 mediates the short-term drought recovery of ecosystem function in low-diversity grassland systems. Plant Soil. https://doi.org/10.1007/s11104-017-3377-8
O’Connor NE, Emmerson MC, Crowe TP, Donohue I (2013) Distinguishing between direct and indirect effects of predators in complex ecosystems. J Anim Ecol 82:438–448. https://doi.org/10.1111/1365-2656.12001
Orchard CM, Lorentz SA, Jewitt GPW, Chaplot VAM (2013) Spatial and temporal variations of overland flow during rainfall events and in relation to catchment conditions. Hydrol Proc 27:2325–2338. https://doi.org/10.1002/hyp.9217
Pommier T et al (2014) Off-site impacts of agricultural composting: role of terrestrially derived organic matter in structuring aquatic microbial communities and their metabolic potential FEMS. Microbiol Ecol 90:622–632. https://doi.org/10.1111/1574-6941.12421
Rochelle-Newall EJ, Fisher TR (2002a) Chromophoric dissolved organic matter and dissolved organic carbon in Chesapeake. Bay Mar Chem 77:23–41
Rochelle-Newall EJ, Fisher TR (2002b) Production of chromophoric dissolved organic matter fluorescence in marine and estuarine environments: an investigation into the role of phytoplankton. Mar Chem 77:7–21
Rochelle-Newall EJ et al. (2004) Chromophoric dissolved organic matter in experimental mesocosms maintained under different pCO2 levels. Mar Ecol Prog Ser 272:25–31
Rochelle-Newall E, Hulot FD, Janeau JL, Merroune A (2014) CDOM fluorescence as a proxy of DOC concentration in natural waters: a comparison of four contrasting tropical systems. Environ Monit Assess 186:589–596. https://doi.org/10.1007/s10661-013-3401-2
Romera-Castillo C, Sarmento H, Alvarez-Salgado XA, Gasol JM, Marrase C (2011) Net production and consumption of fluorescent colored dissolved organic matter by natural bacterial assemblages growing on marine phytoplankton exudates. Appl Environ Microbiol 77:7490–7498. https://doi.org/10.1128/aem.00200-11
Salles JF, Poly F, Schmid B, Le Roux X (2009) Community niche predicts the functioning of denitrifying bacterial assemblages. Ecology 90:3324–3332
Steinberg DK, Nelson NB, Carlson CA, Prusak AC (2004) Production of chromophoric dissolved organic matter (CDOM) in the open ocean by zooplankton and the colonial cyanobacterium Trichodesmium spp. Mar. Ecol Prog Ser 267:45–56
Team RDC (2013) A language and environment for statistical computing. Vienna
Torbert HA, Prior SA, Rogers HH, Wood CW (2000) Review of elevated atmospheric CO2 effects on agro-ecosystems: residue decomposition processes and soil C storage. Plant Soil 224:59–73 https://doi.org/10.1023/a:1004797123881
Trinh DA et al (2016) Impact of terrestrial runoff on organic matter, trophic state, and phytoplankton in a tropical upland reservoir. Aquat Sci 78:367–379. https://doi.org/10.1007/s00027-015-0439-y
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x
Unrein F, Massana R, Alonso-Saez L, Gasol JM (2007) Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Oceanogr 52:456–469
Verdier B et al (2014) Climate and atmosphere simulator for experiments on ecological systems in changing environments. Environ Sci Tech 48:8744–8753. https://doi.org/10.1021/es405467s
Vodacek A, Blough NV, DeGrandpre MD, Peltzer ET, Nelson RK (1997) Seasonal variation of CDOM and DOC in the Middle Atlantic Bight: terrestrial inputs and photooxidation. Limnol Oceanogr 42:674–686
Worrall F, Burt T (2005) Predicting the future DOC flux from upland peat catchments. J Hydrol 300:126–139. https://doi.org/10.1016/j.jhydrol.2004.06.007
Yamashita Y, Kloeppel BD, Knoepp J, Zausen GL, Jaffe R (2011) Effects of watershed history on dissolved organic matter characteristics in headwater streams. Ecosystems 14:1110–1122. https://doi.org/10.1007/s10021-011-9469-z
Zou K, Thébault E, Lacroix G, Barot S (2016) Interactions between the green and brown food web determine ecosystem functioning. Func Ecol 30:1454–1465. https://doi.org/10.1111/1365-2435.12626
Zubkov MV, Burkill PH (2006) Syringe pumped high speed flow cytometry of oceanic phytoplankton. Cytometry A 69:1010–1019
Acknowledgements
This work was supported by the “Agence Nationale de la Recherche” (ANR CEP&S program - PULSE project, ANR-10-CEPL-010). The CEREEP-Ecotron Ile De France benefited from the support by CNRS and ENS, by the “Conseil régional d’Ile-de-France” (DIM R2DS Program “I-05-098/R”, “2011-11017735” & “2015-1657”), and by European Union (FEDER 2007–2013). The Ecolabs also benefited from the support received by the infrastructure PLANAQUA under the program “Investissements d’Avenir” launched by the French government and implemented by ANR with the references ANR-10-EQPX-13-01 Planaqua and ANR-11-INBS-0001 AnaEE France. This research was also supported by the Institut de Recherche pour le Développement (IRD), the UMR laboratories iEES-Paris and ESE. The authors also thank the members of the UMS 3194 CEREEP-Ecotron iDF and the group “Pochetron” for their invaluable help and encouragement during this work. We warmly thank Ross Holland from Aqua Cytometry (UK) for his precious contribution in the microbial counts by flow cytometry. Stuart Findlay is thanked for his helpful comments on an initial version of the manuscript.
Author information
Authors and Affiliations
Contributions
GL, AN, ERN, LJ designed the experiments; GL, AN, LJ, ERN, SF, SC, ML, EDS, SB carried out the work; ERN, LJ, GL, SB, SF, AN interpreted the results and ERN, LJ, GL prepared the figures and wrote the manuscript that was revised and improved by all the coauthors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial interests.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rochelle-Newall, E., Niboyet, A., Jardiller, L. et al. Impacts of elevated atmospheric CO2 concentration on terrestrial-aquatic carbon transfer and a downstream aquatic microbial community. Aquat Sci 80, 27 (2018). https://doi.org/10.1007/s00027-018-0577-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00027-018-0577-0