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Respiration and bacterial carbon dynamics in Arctic sea ice

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Abstract

Bacterial carbon demand, an important component of ecosystem dynamics in polar waters and sea ice, is a function of both bacterial production (BP) and respiration (BR). BP has been found to be generally higher in sea ice than underlying waters, but rates of BR and bacterial growth efficiency (BGE) are poorly characterized in sea ice. Using melted ice core incubations, community respiration (CR), BP, and bacterial abundance (BA) were studied in sea ice and at the ice–water interface (IWI) in the Western Canadian Arctic during the spring and summer 2008. CR was converted to BR empirically. BP increased over the season and was on average 22 times higher in sea ice as compared with the IWI. Rates in ice samples were highly variable ranging from 0.2 to 18.3 μg C l−1 d−1. BR was also higher in ice and on average ~10 times higher than BP but was less variable ranging from 2.39 to 22.5 μg C l−1 d−1. Given the high variability in BP and the relatively more stable rates of BR, BP was the main driver of estimated BGE (r 2 = 0.97, P < 0.0001). We conclude that microbial respiration can consume a significant proportion of primary production in sea ice and may play an important role in biogenic CO2 fluxes between the sea ice and atmosphere.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42

    Google Scholar 

  • Apple JK, del Giorgio PA, Kemp WM (2006) Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquat Microb Ecol 43:243–254

    Article  Google Scholar 

  • Arrigo KR, van Dijken G, Pabi S (2008) Impact of a shrinking Arctic ice cover on marine primary production. Geophys Res Lett 35:6. doi:L19603101029/2008gl035028

    Google Scholar 

  • Arrigo KR, Mock T, Lizotte MP (2010) Primary producers and sea ice. In: Thomas DN, Dieckman GS (eds) Sea ice, 2nd edn. Wiley-Blackwell, Oxford, pp 283–325

    Google Scholar 

  • Barber DG, Asplin MG, Gratton Y, Lukovich J, Galley R, Raddatz R, Leitch D (2010) The International Polar Year (IPY) Circumpolar Flaw Lead (CFL) system study: introduction and physical system. Atmos Ocean 48:225–243

    Google Scholar 

  • Becquevort S, Dumont I, Tison JL, Lannuzel D, Sauvee ML, Chou L, Schoemann V (2009) Biogeochemistry and microbial community composition in sea ice and underlying seawater off East Antarctica during early spring. Polar Biol 32:879–895. doi:10.1007/s00300-009-0589-2

    Article  Google Scholar 

  • Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 63:3068–3078

    PubMed  CAS  Google Scholar 

  • Bunch JN, Harland RC (1990) Bacterial production in the bottom surface of sea ice in the Canadian Sub-Arctic. Can J Fish Aquat Sci 47:1986–1995

    Article  Google Scholar 

  • Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems—A cross-system overview. Mar Ecol Prog Ser 43:1–10

    Article  Google Scholar 

  • Cottrell MT, Malmstrom RR, Hill V, Parker AE, Kirchman DL (2006) The metabolic balance between autotrophy and heterotrophy in the western Arctic Ocean. Deep Sea Res Pt I 53:1831–1844. doi:10.1016/j.dsr.2006.08.010

    Article  Google Scholar 

  • del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541

    Article  Google Scholar 

  • del Giorgio PA, Cole JJ, Cimbleris A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385:148–151

    Article  CAS  Google Scholar 

  • Delille D (1992) Marine bacterioplankton at the Weddell Sea ice edge, distribution of psychrophilic and psychrotrophic populations. Polar Biol 12:205–210

    Article  Google Scholar 

  • Delille B, Rosiers C (1996) Seasonal changes of Antarctic marine bacterioplankton and sea ice bacterial assemblages. Polar Biol 16:27–34

    Google Scholar 

  • Delille D, Jourdain B, Borges AV, Tison JL, Delille B (2007) Biogas (CO2, O2, dimethylsulfide) dynamics in spring Antarctic fast ice. Limnol Oceanogr 52:1367–1379

    Article  CAS  Google Scholar 

  • Ducklow H (2000) Bacterial production and biomass in the oceans. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 85–120

    Google Scholar 

  • Fransson A, Chierici M, Nojiri Y (2009) New insights into the spatial variability of the surface water carbon dioxide in varying sea ice conditions in the Arctic Ocean. Cont Shelf Res 29:1317–1328. doi:10.1016/j.csr.2009.03.008

    Article  Google Scholar 

  • Garneau ME, Roy S, Lovejoy C, Gratton Y, Vincent WF (2008) Seasonal dynamics of bacterial biomass and production in a coastal arctic ecosystem: Franklin Bay, western Canadian Arctic. J Geophys Res Oc 113 (C7). doi:10.1029/2007jc004281

  • Garneau ME, Vincent WF, Terrado R, Lovejoy C (2009) Importance of particle-associated bacterial heterotrophy in a coastal Arctic ecosystem. J Marine Syst 75:185–197. doi:10.1016/j.jmarsys.2008.09.002

    Article  Google Scholar 

  • Garrison DL, Buck KR (1986) Organism losses during ice melting—A serious bias in sea ice community studies. Polar Biol 6:237–239

    Article  Google Scholar 

  • Gasol JM, del Giorgio PA, Massana R, Duarte CM (1995) Active versus inactive bacteria: size-dependence in a coastal marine plankton community. Mar Ecol Prog Ser 128:91–97

    Article  Google Scholar 

  • Gosselin M, Legendre L, Therriault JC, Demers S, Rochet M (1986) Physical control of the horizontal patchiness of sea-ice microalgea. Mar Ecol Prog Ser 29:289–298

    Article  Google Scholar 

  • Grossmann S, Dieckmann GS (1994) Bacterial standing stock, activity, and carbon production during formation and growth of sea-ice in the Weddell sea, Antarctica. Appl Environ Microbiol 60:2746–2753

    PubMed  CAS  Google Scholar 

  • Helmke E, Weyland H (1995) Bacteria in sea-ice and underlying water of the Eastern Weddell sea in midwinter. Mar Ecol Prog Ser 117:269–287

    Article  Google Scholar 

  • Hoppe HG, Breithaupt P, Walther K, Koppe R, Bleck S, Sommer U, Jurgens K (2008) Climate warming in winter affects the coupling between phytoplankton and bacteria during the spring bloom: a mesocosm study. Aquat Microb Ecol 51:105–115. doi:10.3354/ame01198

    Article  Google Scholar 

  • Ikeya T, Kashino Y, Kudohl S, Imural S, Watanabe K, Fukuchil M (2000) Acclimation of photosynthetic properties in psychrophilic diatom isolates under different light intensities. Polar Biosci 13:43–54

    Google Scholar 

  • Jahnke RA, Craven DB (1995) Quantifying the role of heterotrophic bacteria in the carbon cycle—A need for respiration rate measurements. Limnol Oceanogr 40:436–441

    Article  CAS  Google Scholar 

  • Jorgensen NOG, Kroer N, Coffin RB, Hoch MP (1999) Relations between bacterial nitrogen metabolism and growth efficiency in an estuarine and an open-water ecosystem. Aquat Microb Ecol 18:247–261

    Article  Google Scholar 

  • Junge K, Eicken H, Deming JW (2004) Bacterial activity at −2 to −20°C in Arctic wintertime sea ice. Appl Environ Microbiol 70:550–557

    Article  PubMed  CAS  Google Scholar 

  • Kaartokallio H, Kuosa H, Thomas DN, Granskog MA, Kivi K (2007) Biomass, composition and activity of organism assemblages along a salinity gradient in sea ice subjected to river discharge in the Baltic Sea. Polar Biol 30:183–197. doi:10.1007/s00300-006-0172-z

    Article  Google Scholar 

  • Kirchman DL, Malmstrom RR, Cottrell MT (2005) Control of bacterial growth by temperature and organic matter in the Western Arctic. Deep-Sea Res Pt II 52:3386–3395

    Article  Google Scholar 

  • Kirchman DL, Hill V, Cottrell MT, Gradinger R, Malmstrom RR, Parker A (2009a) Standing stocks, production, and respiration of phytoplankton and heterotrophic bacteria in the western Arctic Ocean. Deep-Sea Res Pt II 56:1237–1248. doi:10.1016/j.dsr2.2008.10.018

    Article  CAS  Google Scholar 

  • Kirchman DL, Moran XAG, Ducklow H (2009b) Microbial growth in the polar oceans—role of temperature and potential impact of climate change. Nat Rev Microbiol 7:451–459. doi:10.1038/nrmicro2115

    PubMed  CAS  Google Scholar 

  • Kottmeier ST, Sullivan CW (1987) Late winter primary production and bacterial production in sea ice aand seawater west of the Antarctic peninsula. Mar Ecol Prog Ser 36:287–298

    Article  Google Scholar 

  • Kottmeier ST, Sullivan CW (1988) Sea ice microbial communities (Simco) 9. Effects of temperature and salinity on rates of metabolism and growth of autotrophs and heterotrophs. Polar Biol 8:293–304

    Article  Google Scholar 

  • Kottmeier ST, Grossi SM, Sullivan CW (1987) Sea ice microbial communities. 8. Bacterial production in annual sea ice of mcmurdo sound, Antarctica. Mar Ecol Prog Ser 35:175–186

    Article  Google Scholar 

  • Kragh T, Sondergaard M, Tranvik L (2008) Effect of exposure to sunlight and phosphorus-limitation on bacterial degradation of coloured dissolved organic matter (CDOM) in freshwater. FEMS Microb Ecol 64:230–239. doi:10.1111/j.1574-6941.2008.00449.x

    Article  CAS  Google Scholar 

  • Kritzberg ES, Cole JJ, Pace MM, Graneli W (2005) Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquat Microb Ecol 38:103–111

    Article  Google Scholar 

  • Kritzberg ES, Duarte CM, Wassmann P (2010) Changes in Arctic marine bacterial carbon metabolism in response to increasing temperature. Polar Biol. doi:10.1007/s00300-010-0799-7

  • Kuparinen J, Kuosa H, Andersson A, Autio R, Granskog MA, Ikavalko J, Kaartokallio H, Karell K, Leskinen E, Piiparinen J, Rintala JM, Tuomainen J (2007) Role of sea-ice biota in nutrient and organic material cycles in the northern Baltic Sea. Ambio 36:149–154

    Article  PubMed  CAS  Google Scholar 

  • Legendre L, Ackley SF, Dieckmann GS, Gulliksen B, Horner R, Hoshiai T, Melnikov IA, Reeburgh WS, Spindler M, Sullivan CW (1992) Ecology of sea ice biota.2. Global significance. Polar Biol 12:429–444

    Google Scholar 

  • Lizotte MP (2001) The contributions of sea ice algae to Antarctic marine primary production. Am Zool 41:57–73

    Article  Google Scholar 

  • Maranger R, Bird DF, Juniper SK (1994) Viral and bacterial dynamics in arctic sea-ice during the spring algal bloom near resolute, Nwt, Canada. Mar Ecol Prog Ser 111:121–127

    Article  Google Scholar 

  • Marchand D, Prairie YT, del Giorgio PA (2009) Linking forest fires to lake metabolism and carbon dioxide emissions in the boreal region of Northern Quebec. Glob Change Biol 15:2861–2873. doi:10.1111/j.1365-2486.2009.01979.x

    Article  Google Scholar 

  • Michel C, Legendre L, Ingram RG, Gosselin M, Levasseur M (1996) Carbon budget of sea-ice algae in spring: evidence of a significant transfer to zooplankton grazers. J Geophys Res-Oceans 101:18345–18360

    Article  CAS  Google Scholar 

  • Middelboe M, Jorgensen NOG, Kroers N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62:1991–1997

    PubMed  CAS  Google Scholar 

  • Miller LA, Papakyriakou TN, Collins RE, Deming JW, Ehn JK, Macdonald RW, Mucci A, Owens O, Raudsepp M, Sutherland N (2011) Carbon dynamics in sea ice: a winter flux time series. J Geophys Res 116 (C2):C02028. doi:10.1029/2009jc006058

  • Mock T, Meiners KM, Giesenhagen HC (1997) Bacteria in sea ice and underlying brackish water at 54 degrees 26′50″N (Baltic Sea, Kiel Bight). Mar Ecol Prog Ser 158:23–40

    Article  Google Scholar 

  • Mundy CJ, Barber DG, Michel C (2005) Variability of snow and ice thermal, physical and optical properties pertinent to sea ice algae biomass during spring. J Mar Syst 58:107–120

    Article  Google Scholar 

  • Pabi S, van Dijken GL, Arrigo KR (2008) Primary production in the Arctic Ocean, 1998–2006. J Geophys Res-Oceans 113:C8

    Article  Google Scholar 

  • Papakyriakou T, Miller S (2011) Springtime CO2 exchange over seasonal ice in the Canadian Arctic Archipelago. Ann Glaciol 52:215–224

    Article  CAS  Google Scholar 

  • Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23(2):187–204

    Article  Google Scholar 

  • Porter KG, Feig YS (1980) The use of dapi for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  • Pusceddu A, Dell’Anno A, Vezzulli L, Fabiano M, Saggiomo V, Cozzi S, Catalano G, Guglielmo L (2009) Microbial loop malfunctioning in the annual sea ice at Terra Nova Bay (Antarctica). Polar Biol 32:337–346. doi:10.1007/s00300-008-0539-4

    Article  Google Scholar 

  • Riedel A, Michel C, Gosselin M (2006) Seasonal study of sea-ice exopolymeric substances on the Mackenzie shelf: implications for transport of sea-ice bacteria and algae. Aquat Microb Ecol 45:195–206

    Article  Google Scholar 

  • Riedel A, Michel C, Gosselin M, LeBlanc B (2008) Winter-spring dynamics in sea-ice carbon cycling in the coastal Arctic Ocean. J Marine Syst 74:918–932

    Article  Google Scholar 

  • Rivkin RB, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400

    Article  PubMed  CAS  Google Scholar 

  • Robinson C (2008) Heterotrophic bacterial respiration. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Blackwell, New Jersey, pp 299–334

    Chapter  Google Scholar 

  • Robinson C, Williams PJB (2005) Respiration and its measurement in surface marine waters. In: del Giorgio PA, Williams PJB (eds) Respiration in aquatic ecosystems. Oxford University Press, New York, pp 147–180

    Chapter  Google Scholar 

  • Robinson C, Archer SD, Williams PJL (1999) Microbial dynamics in coastal waters of East Antarctica: plankton production and respiration. Mar Ecol Prog Ser 180:23–36

    Article  Google Scholar 

  • Roland F, Cole JJ (1999) Regulation of bacterial growth efficiency in a large turbid estuary. Aquat Microb Ecol 20:31–38

    Article  Google Scholar 

  • Rysgaard S, Glud RN, Sejr MK, Blicher ME, Stahl HJ (2008) Denitrification activity and oxygen dynamics in Arctic sea ice. Polar Biol 31:527–537. doi:10.1007/s00300-007-0384-x

    Article  Google Scholar 

  • Semiletov IP, Pipko II, Repina I, Shakhova NE (2007) Carbonate chemistry dynamics and carbon dioxide fluxes across the atmosphere-ice-water interfaces in the Arctic Ocean: Pacific sector of the Arctic. J Marine Syst 66:204–226. doi:10.1016/j.jmarsys.2006.05.012

    Article  Google Scholar 

  • Sherr EB, Sherr BF (1996) Temporal offset in oceanic production and respiration processes implied by seasonal changes in atmospheric oxygen: the role of heterotrophic microbes. Aquat Microb Ecol 11:91–100

    Article  Google Scholar 

  • Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rate using 3H-leucine. Marine Microb Food Webs:107–114

  • Smith EM, Prairie YT (2004) Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol Oceanogr 49:137–147

    Article  CAS  Google Scholar 

  • Smith REH, Clement P, Cota GF (1989) Population dynamics of bacteria in Arctic sea ice. Microb Ecol 17(1):63–76

    Article  Google Scholar 

  • Smith REH, Gosselin M, Kudoh S, Robineau B, Taguchi S (1997) DOC and its relationship to algae in bottom ice communities. J Marine Syst 11(1–2):71–80

    Article  Google Scholar 

  • Straza TRA, Cottrell MT, Ducklow HW, Kirchman DL (2009) Geographic and phylogenetic variation in bacterial biovolume as revealed by protein and nucleic acid staining. Appl Environ Microbiol 75(12):4028–4034. doi:10.1128/aem.00183-09

    Article  PubMed  CAS  Google Scholar 

  • Thomas DN, Dieckmann GS (2010) Sea ice, 2nd edn. Wiley-Blackwell, Oxford

    Google Scholar 

  • Vaquer-Sunyer R, Duarte CM, Wassmann P, Santiago R, Reigstad M (2010) Experimental evaluation of planktonic respiration response to warming in the European Arctic sector. Polar Biol. doi:10.1007/s00300-010-0788-x

  • Wassmann P, Carroll J, Bellerby RGJ (2008) Carbon flux and ecosystem feedback in the northern Barents Sea in an era of climate change: an introduction. Deep-Sea Res Part Ii-Top Stud Oceanogr 55:2143–2153. doi:10.1016/j.dsr2.2008.05.025

    Article  Google Scholar 

  • Williams PJB, del Giorgio PA (2005) Respiration in aquatic ecosystems: history and background. In: del Giorgio PA, Williams PJB (eds) Respiration in aquatic ecosystems. Oxford biology, New York, pp 267–303

    Google Scholar 

  • Yager PL, Deming JW (1999) Pelagic microbial activity in an arctic polynya: testing for temperature and substrate interactions using a kinetic approach. Limnol Oceanogr 44:1882–1893

    Article  CAS  Google Scholar 

  • Yager PL, Connelly TL, Mortazavi B, Wommack KE, Bano N, Bauer JE, Opsahl S, Hollibaugh JT (2001) Dynamic bacterial and viral response to an algal bloom at subzero temperatures. Limnol Oceanogr 46:790–801

    Article  CAS  Google Scholar 

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Acknowledgments

We sincerely thank the Capts and crew of the CCGS Amundsen, the CFL-IPY logistical personnel and numerous collaborators and colleagues for their devotion to the CFL project. We also thank M. Gosselin for Chl a data, J.E. Tremblay for nutrient data, G. Carnat, and A. Rossnagel for additional data. C. Robinson was very helpful with CR to BR conversions. L. Delaney, G. Maltais-Landry, C. Pedros-Alìo and participating members from ICM and the «ice team» provided critical logistic and technical support. Helpful comments that improved the manuscript were kindly provided by E. Collins, J. Deming, C.J. Mundy, D. Piepenburg and 2 anonymous reviewers. Research was supported by a CFL-IPY-Team grant (R.M, Team 7, theme lead JE Tremblay; Overall project lead D. Barber, co PIs J. Deming and G. Stern) and by an NSERC discovery grant (R.M.). D.N. is supported by a FQRNT and NSERC Ph.D. student scholarships. This is a contribution from the Groupe de Recherche Interuniversitaire en Limnologie (GRIL) and Québec-Océan.

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  1. Département des sciences biologiques, Groupe de Recherche Interuniversitaire en Limnologie (GRIL-UdeM), Université de Montréal, CP 6128, Succ. Centre-ville, Montréal, QC, H3C 3J7, Canada

    Dan Nguyen & Roxane Maranger

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  1. Dan Nguyen
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  2. Roxane Maranger
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Correspondence to Roxane Maranger.

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This article belongs to the special issue “Circumpolar Flaw Lead Study (CFL)”, coordinated by J. Deming and L. Fortier.

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Nguyen, D., Maranger, R. Respiration and bacterial carbon dynamics in Arctic sea ice. Polar Biol 34, 1843–1855 (2011). https://doi.org/10.1007/s00300-011-1040-z

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