Bacterial community composition responds to changes in copepod abundance and alters ecosystem function in an Arctic mesocosm study
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29991763
PubMed Central
PMC6194086
DOI
10.1038/s41396-018-0217-7
PII: 10.1038/s41396-018-0217-7
Knihovny.cz E-zdroje
- MeSH
- autotrofní procesy MeSH
- Bacteria růst a vývoj izolace a purifikace metabolismus MeSH
- Ciliophora fyziologie MeSH
- Copepoda fyziologie MeSH
- fyziologie bakterií * MeSH
- glukosa metabolismus MeSH
- heterotrofní procesy MeSH
- mikrobiota MeSH
- potravní řetězec * MeSH
- uhlík metabolismus MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Arktida MeSH
- Názvy látek
- glukosa MeSH
- uhlík MeSH
Combining a minimum food web model with Arctic microbial community dynamics, we have suggested that top-down control by copepods can affect the food web down to bacterial consumption of organic carbon. Pursuing this hypothesis further, we used the minimum model to design and analyse a mesocosm experiment, studying the effect of high (+Z) and low (-Z) copepod density on resource allocation, along an organic-C addition gradient. In the Arctic, both effects are plausible due to changes in advection patterns (affecting copepods) and meltwater inputs (affecting carbon). The model predicts a trophic cascade from copepods via ciliates to flagellates, which was confirmed experimentally. Auto- and heterotrophic flagellates affect bacterial growth rate and abundance via competition for mineral nutrients and predation, respectively. In +Z, the model predicts low bacterial abundance and activity, and little response to glucose; as opposed to clear glucose consumption effects in -Z. We observed a more resilient bacterial response to high copepods and demonstrate this was due to changes in bacterial community equitability. Species able to use glucose to improve their competitive and/or defensive properties, became predominant. The observed shift from a SAR11-to a Psychromonodaceae - dominated community suggests the latter was pivotal in this modification of ecosystem function. We argue that this group used glucose to improve its defensive or its competitive abilities (or both). Adding such flexibility in bacterial traits to the model, we show how it creates the observed resilience to top-down manipulations observed in our experiment.
Department of Biological Sciences University of Bergen Bergen Norway
Department of Biology NTNU Norwegian University of Science and Technology Trondheim Norway
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Arrigo KR. Marine microorganisms and global nutrient cycles. Nature. 2005;437:349–55. doi: 10.1038/nature04159. PubMed DOI
Jiao N, Robinson C, Azam F, Thomas H, Baltar F, Dang H, et al. Mechanisms of microbial carbon sequestration in the ocean - future research directions. Biogeosciences. 2014;11:5285–306. doi: 10.5194/bg-11-5285-2014. DOI
Riebesell U, Gattuso JP, Thingstad TF, Middelburg JJ. Preface “Arctic ocean acidification: pelagic ecosystem and biogeochemical responses during a mesocosm study”. Biogeosciences. 2013;10:5619–26. doi: 10.5194/bg-10-5619-2013. DOI
Engel A, Borchard C, Piontek J, Schulz KG, Riebesell U, Bellerby R. CO2 increases 14C primary production in an Arctic plankton community. Biogeosciences. 2013;10:1291–308. doi: 10.5194/bg-10-1291-2013. DOI
AMAP. AMAP Assessment 2013: Arctic Ocean Acidification. Oslo, Norway: Arctic Monitoring and Assessment Programme (AMAP); 2013. p. viii+99.
Anisimov OA, Vaughan DG, Callaghan TV, Furgal C, Marchant H, Prowse TD et al. Polar regions (Arctic and Antarctic). Climate change 2007: impacts, adaptation and vulnerab ility. contribution of working group II to the fourth. In: Change ML, Parry OF, Canziani JP, Palutikof PJ, van der Linden, Hanson CE, (eds.) Assessment Report of the Intergovernmental Panel on Climate. Cambridge: Cambridge University Press; 2007. p. 653–85.
Holmes RM, McClelland JW, Peterson BJ, Tank SE, Bulygina E, Eglinton TI, et al. Seasonal and annual fluxes of nutrients and organic matter from large rivers to the Arctic Ocean and surrounding seas. Estuaries Coasts. 2012;35:369–82. doi: 10.1007/s12237-011-9386-6. DOI
Fellman JB, Spencer RGM, Hernes PJ, Edwards RT, D’Amore DV, Hood E. The impact of glacier runoff on the biodegradability and biochemical composition of terrigenous dissolved organic matter in near-shore marine ecosystems. Mar Chem. 2010;121:112–22. doi: 10.1016/j.marchem.2010.03.009. DOI
Hood E, Fellman J, Spencer RGM, Hernes PJ, Edwards R, D’Amore D, et al. Glaciers as a source of ancient and labile organic matter to the marine environment. Nature. 2009;462:1044–7. doi: 10.1038/nature08580. PubMed DOI
Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR. Lipids and life strategy of Arctic Calanus. Mar Biol Res. 2009;5:18–39. doi: 10.1080/17451000802512267. DOI
Rhein M, Rintoul SR, Aoki S, Campos E, Chambers D, Freely RA et al. Observations: ocean. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, (eds.) Climate Change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press; 2013.
Ducklow HW, Steinberg DK, Buesseler KO. Upper ocean carbon export and the biological pump. Oceanography. 2001;14:50–8. doi: 10.5670/oceanog.2001.06. DOI
Eppley RW, Peterson BJ. Particulate organic matter flux and planktonic new production in the deep ocean. Nature. 1979;282:677–80. doi: 10.1038/282677a0. DOI
Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol. 2010;8:593–9. doi: 10.1038/nrmicro2386. PubMed DOI
Legendre L, Rivkin RB, Weinbauer MG, Guidi L, Uitz J. The microbial carbon pump concept: Potential biogeochemical significance in the globally changing ocean. Prog Oceanogr. 2015;134:432–50. doi: 10.1016/j.pocean.2015.01.008. DOI
Polimene L, Sailley S, Clark D, Mitra A, Allen JI. Biological or microbial carbon pump? The role of phytoplankton stoichiometry in ocean carbon sequestration. J Plankton Res. 2017;39:180–6.
Brussaard CPD, Bidle KD, Pedrós-Alió C, Legrand C. The interactive microbial ocean. Nat Microbiol. 2016;2:16255. doi: 10.1038/nmicrobiol.2016.255. PubMed DOI
Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT, et al. Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J. 2016;10:2557–68. doi: 10.1038/ismej.2016.45. PubMed DOI PMC
Landa M, Blain S, Christaki U, Monchy S, Obernosterer I. Shifts in bacterial community composition associated with increased carbon cycling in a mosaic of phytoplankton blooms. ISME J. 2016;10:39–50. doi: 10.1038/ismej.2015.105. PubMed DOI PMC
Jónasdóttir SH, Visser AW, Richardson K, Heath MR. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. Proc Natl Acad Sci USA. 2015;112:12122–6. doi: 10.1073/pnas.1512110112. PubMed DOI PMC
Schulz KG, Bellerby RGJ, Brussaard CPD, Budenbender J, Czerny J, Engel A, et al. Temporal biomass dynamics of an Arctic plankton bloom in response to increasing levels of atmospheric carbon dioxide. Biogeosciences. 2013;10:161–80. doi: 10.5194/bg-10-161-2013. DOI
Legendre L, Rassoulzadegan F. Food-web mediated export of biogenic carbon in oceans: hydrodynamic control. Mar Ecol Prog Ser. 1996;145:179–93. doi: 10.3354/meps145179. DOI
Hessen DO, Ågren GI, Anderson TR, Elser JJ, de Ruiter PC. Carbon sequestration in ecosystems: The role of stoichiometry. Ecology. 2004;85:1179–92. doi: 10.1890/02-0251. DOI
Thingstad TF, Havskum H, Zweifel UL, Berdalet E, Sala MM, Peters F, et al. Ability of a “minimum” microbial food web model to reproduce response patterns observed in mesocosms manipulated with N and P, glucose, and Si. J Mar Syst. 2007;64:15–34. doi: 10.1016/j.jmarsys.2006.02.009. DOI
Larsen A, Egge JK, Nejstgaard JC, Di Capua I, Thyrhaug R, Bratbak G, et al. Contrasting response to nutrient manipulation in Arctic mesocosms are reproduced by a minimum microbial food web model. Limnol Oceanogr. 2015;60:360–74. doi: 10.1002/lno.10025. PubMed DOI PMC
Sandaa RA, Pree B, Larsen A, Våge S, Töpper B, Töpper J, et al. The response of heterotrophic prokaryote and viral communities to labile organic carbon inputs is controlled by the predator food chain structure. Viruses. 2017;9:238. doi: 10.3390/v9090238. PubMed DOI PMC
Koroleff F. Determination of nutrients. In: Grasshoff K, Ehrhardt M, Kremling K, editors. Methods in seawater analyses. Weinheim/Deerfield Beach, Florida: Verlag Chemie; 1983. pp. 125–31.
Valderrama JC. Methods of nutrient analysis. In: Hallograeff GM, Anderson DM, Cembella AD, editors. Manual of harmful marine microalgae. IOC manuals and guides. Paris: UNESCO; 1995. pp. 262–5.
Holmes RM, Aminot A, Keroul R, Hooker AH, Peterson BJ. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci. 1999;56:1801–8. doi: 10.1139/f99-128. DOI
Cauwet G. Determination of dissolved organic carbon and nitrogen by high temperature combution. In: Grasshoff K, Kremling K, Ehrhardt M, editors. Methods of Seawater Analysis. 3rd edn. Weinheim, Germany: Wiley-VCH Verlag GmbH; 1999.
Pella E, Colombo B. Study of carbon, hydrogen and nitrogen determination by combustion-gas chromatography. Microchim Acta. 1973;61:697–719. doi: 10.1007/BF01218130. DOI
Kwasniewski S, Hop H, Falk-Petersen S, Pedersen G. Distribution of Calanus species in Kongsfjorden, a glacial fjord in Svalbard. J Plankton Res. 2003;25:1–20. doi: 10.1093/plankt/25.1.1. DOI
Hay SJ, Kiørboe T, Matthews A. Zooplankton biomass and production in the North Sea during the Autumn Circulation experiment, October 1987–March 1988. Cont Shelf Res. 1991;11:1453–76. doi: 10.1016/0278-4343(91)90021-W. DOI
Hay SJ, Evans GT, Gamble JC. Birth, growth and death rates for enclosed populations of calanoid copepods. J Plankton Res. 1988;10:431–54. doi: 10.1093/plankt/10.3.431. DOI
Båmstedt U. Chemical composition and energy content. In: Corner EDS, O’Hara SCM, editors. The Biological Chemistry of Marine Copepods. Oxford: Clarendon Press; 1986. pp. 1–58.
Marie D, Partensky F, Vaulot D, Brussaard CP. Enumeration of phytoplankton, bacteria and viruses in marine samples. In: Robinson JP, editor. Current Protocols in cytometry. New York, NY: John Wiley & Sons; 1999. PubMed
Zubkov M, Burkill PH, Topping JN. Flow cytometric enumeration of DNA-stained oceanic planktonic protists. J Plankton Res. 2007;29:79–86. doi: 10.1093/plankt/fbl059. DOI
Gasol JM, Zweifel UL, Peters F, Fuhrman JA, Hagstrom A. Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl Environ Microb. 1999;65:4475–83. PubMed PMC
Li WKW, Jellett JF, Dickie PM. DNA distributions in planktonic bacteria stained with TOTO or TO-PRO. Limnol Oceanogr. 1995;40:1485–95. doi: 10.4319/lo.1995.40.8.1485. DOI
Longnecker K, Sherr BF, Sherr EB. Variation in cell-specific rates of leucine and thymidine incorporation by marine bacteria with high and with low nucleic acid content off the Oregon coast. Aquat Microb Ecol. 2006;43:113–25. doi: 10.3354/ame043113. DOI
Morán XAG, Calvo-Díaz A, Ducklow HW. Total and phytoplankton mediated bottom-up control of bacterioplankton change with temperature in NE Atlantic shelf waters. Aquat Microb Ecol. 2010;58:229–39. doi: 10.3354/ame01374. DOI
Proctor CR, Besmer MD, Langenegger T, Beck K, Walser JC, Ackermann M, Bürgmann H, Hammes F. Phylogenetic clustering of small low nucleic acid-content bacteria across diverse freshwater ecosystems. ISME J. 2018;12:1344–59. doi: 10.1038/s41396-018-0070-8. PubMed DOI PMC
Scharek R, Latasa M. Growth, grazing and carbon flux of high and low nucleic acid bacteria differ in surface and deep chlorophyll maximum layers in the NW Mediterranean Sea. Aquat Microb Ecol. 2007;46:153–61. doi: 10.3354/ame046153. DOI
Van Wambeke F, Catala P, Pujo-Pay M, Lebaron P. Vertical and longitudinal gradients in HNA-LNA cell abundances and cytometric characteristics in the Mediterranean Sea. Biogeosciences. 2011;8:1853–63. doi: 10.5194/bg-8-1853-2011. DOI
Zhixin N, Huang X, Zhang X. Picoplankton and virioplankton abundance and community structure in Pearl River Estuary and Daya Bay, South China. J Environ Sci. 2015;32:146–54. doi: 10.1016/j.jes.2014.12.019. PubMed DOI
Holm-Hansen O, Riemann B. Chlorophyll a determination: improvements in methodology. Oikos. 1978;30:438–47. doi: 10.2307/3543338. DOI
Simon M, Azam F. Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser. 1989;51:201–13. doi: 10.3354/meps051201. DOI
Kirchman D. Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ, editors. Current methods in aquatic microbial ecology. London: Lewis Publisher; 1993. pp. 509–12.
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41. doi: 10.1128/AEM.01541-09. PubMed DOI PMC
Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ. Removing noise from pyrosequenced amplicons. BMC Bioinform. 2011;12:38. doi: 10.1186/1471-2105-12-38. PubMed DOI PMC
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200. doi: 10.1093/bioinformatics/btr381. PubMed DOI PMC
Needleman SB, Wunsch CD. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970;48:443–53. doi: 10.1016/0022-2836(70)90057-4. PubMed DOI
Gihring TM, Green SJ, Schadt CW. Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environ Microbiol. 2012;14:285–90. doi: 10.1111/j.1462-2920.2011.02550.x. PubMed DOI
Polis GA, Sears ALW, Huxel GR, Strong DR, Maron J. When is a trophic cascade a trophic cascade? Trends Ecol Evol. 2000;15:473–5. doi: 10.1016/S0169-5347(00)01971-6. PubMed DOI
Carpenter SR, Kitchell JF, Hodgson JR. Cascading trophic interactions and lake productivity. Bioscience. 1985;35:634–9. doi: 10.2307/1309989. DOI
Sommer U. Trophic cascades in marine and freshwater plankton. Int Rev Hydrobiol. 2008;93:506–16. doi: 10.1002/iroh.200711039. DOI
Alonso C, Pernthaler J. Roseobacter and SAR11 dominate microbial glucose uptake in coastal North Sea waters. Environ Microbiol. 2006;8:2022–30. doi: 10.1111/j.1462-2920.2006.01082.x. PubMed DOI
Satomi M, Fujii T. The family Oceanospirillaceae. In: Rosenberg E, editor. The Prokaryotes: Gammaproteobacteria. Berlin, Heidelberg: Springer-Verlag; 2013. pp. 491–529.
Gomez-Consarnau L, Lindh MV, Gasol JM, Pinhassi J. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ Microbiol. 2012;14:2361–78. doi: 10.1111/j.1462-2920.2012.02804.x. PubMed DOI
Gómez-Pereira PR, Schüler M, Fuchs BM, Bennke C, Teeling H, Waldmann J, et al. Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean. Environ Microbiol. 2012;14:52–66. doi: 10.1111/j.1462-2920.2011.02555.x. PubMed DOI
Kirchman DL. The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol. 2002;39:91–100. PubMed
Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science. 2012;336:608–11. doi: 10.1126/science.1218344. PubMed DOI
Wilson B, Müller O, Nordmann E-L, Seuthe L, Bratbak G, Øvreås L. Changes in marine prokaryote composition with season and depth over an arctic polar year. Front Mar Sci. 2017; 4.
Lebaron P, Servais P, Agogué H, Courties C, Joux F. Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl Environ Microbiol. 2001;67:1775–82. doi: 10.1128/AEM.67.4.1775-1782.2001. PubMed DOI PMC
Jürgens K, Matz C. Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek. 2002;81:413–34. doi: 10.1023/A:1020505204959. PubMed DOI
Mathisen P, Thelaus J, Sjöstedt de Luna S, Andersson A. Rapid adaptation of predation resistance in bacteria isolated from a seawater microcosm. Aquat Microb Ecol. 2016;78:81–92. doi: 10.3354/ame01802. DOI
Baumgartner M, Roffler S, Wicker T, Pernthaler J. Letting go: bacterial genome reduction solves the dilemma of adapting to predation mortality in a substrate-restricted environment. ISME J. 2017;11:2258–66. doi: 10.1038/ismej.2017.87. PubMed DOI PMC
Matz C, Jürgens K. Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb Ecol. 2003;45:384–98. doi: 10.1007/s00248-003-2000-0. PubMed DOI
Thingstad TF, Øvreas L, Egge JK, Løvdal T, Heldal M. Use of non-limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecol Lett. 2005;8:675–82. doi: 10.1111/j.1461-0248.2005.00768.x. DOI
Longhurst AR. Ecological geography of the sea. Academic Press; Burlington 2010.
Le Moigne FAC, Henson SA, Sanders RJ, Madsen E. Global database of surface ocean particulate organic carbon export fluxes diagnosed from the 234Th technique. Earth Syst Sci Data. 2013;5:295–304. doi: 10.5194/essd-5-295-2013. DOI
Le Moigne FAC, Poulton AJ, Henson SA, Daniels CJ, Fragoso GM, Mitchell E, et al. Carbon export efficiency and phytoplankton community composition in the Atlantic sector of the Arctic Ocean. J Geophys Res Oceans. 2015;120:3896–912. doi: 10.1002/2015JC010700. DOI
Kosobokova KN. The reproductive cycle and life history of the Arctic copepod Calanus glacialis in the White Sea. Polar Biol. 1999;22:254–63. doi: 10.1007/s003000050418. DOI
Lechtenfeld OJ, Hertkorn N, Shen Y, Witt M, Benner R. Marine sequestration of carbon in bacterial metabolites. Nat Commun. 2015;6:6711. doi: 10.1038/ncomms7711. PubMed DOI
Thingstad TF, Bellerby RGJ, Bratbak G, Borsheim KY, Egge JK, Heldal M, et al. Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature. 2008;455:387–37. doi: 10.1038/nature07235. PubMed DOI
Edwards M, Richardson AJ. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature. 2004;430:881–4. doi: 10.1038/nature02808. PubMed DOI
Kraft A, Nothig EM, Bauerfeind E, Wildish DJ, Pohle GW, Bathmann UV, et al. First evidence of reproductive success in a southern invader indicates possible community shifts among Arctic zooplankton. Mar Ecol Prog Ser. 2013;493:291–6. doi: 10.3354/meps10507. DOI
Weydmann A, Carstensen J, Goszczko I, Dmoch K, Olszewska A, Kwasniewski S. Shift towards the dominance of boreal species in the Arctic: inter-annual and spatial zooplankton variability in the West Spitsbergen Current. Mar Ecol Prog Ser. 2014;501:41–52. doi: 10.3354/meps10694. DOI