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Dissolved extracellular polymeric substances (dEPS) dynamics and bacterial growth during sea ice formation in an ice tank study

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Abstract

Extracellular polymeric substances (EPS) are known to help microorganisms to survive under extreme conditions in sea ice. High concentrations of EPS are reported in sea ice from both poles; however, production and dynamics of EPS during sea ice formation have been little studied to date. This investigation followed the production and partitioning of existing and newly formed dissolved organic matter (DOM) including dissolved carbohydrates (dCHO), dissolved uronic acids (dUA) and dissolved EPS (dEPS), along with bacterial abundances during early stages of ice formation. Sea ice was formed from North Sea water with (A) ambient DOM (NSW) and (B) with additional algal-derived DOM (ADOM) in a 6d experiment in replicated mesocosms. In ADOM seawater, total bacterial numbers (TBN) increased throughout the experiment, whereas bacterial growth occurred for 5d only in the NSW seawater. TBN progressively decreased within developing sea ice but with a 2-fold greater decline in NSW compared to ADOM ice. There were significant increases in the concentrations of dCHO in ice. Percentage contribution of dEPS was highest (63%) in the colder, uppermost parts in ADOM ice suggesting the development of a cold-adapted community, producing dEPS possibly for cryo-protection and/or protection from high salinity brines. We conclude that in the early stages of ice formation, allochthonous organic matter was incorporated from parent seawater into sea ice and that once ice formation had established, there were significant changes in the concentrations and composition of dissolved organic carbon pool, resulting mainly from the production of autochthonous DOM by the bacteria.

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References

  • Arrigo KR, Dieckmann G, Gosselin M, Robinson DH, Fritsen CH, Sullivan CW (1995) High resolution study of the platelet ice ecosystem in McMurdo Sound, Antarctica: biomass, nutrient, and production profiles within a dense microalgal bloom. Mar Ecol Prog Ser 127:255–268. doi:10.3354/meps127255

    Article  Google Scholar 

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

    Google Scholar 

  • Aspinall GO (1982) The polysaccharides, vol 1. Academic Press, New York

    Google Scholar 

  • Bellinger BJ, Abdullahi AS, Gretz MR, Underwood GJC (2005) Biofilm polymers: relationship between carbohydrate biopolymers from estuarine mudflats and unialgal cultures of benthic diatoms. Aquat Microb Ecol 38:169–180

    Article  Google Scholar 

  • Bitter T, Muir HM (1962) A modified uronic acid carbazole reaction. Anal Biochem 4:330–334. doi:10.1016/0003-2697(62)90095-7

    Article  PubMed  CAS  Google Scholar 

  • Bowman JS, Deming JW (2010) Elevated bacterial abundance and exopolymers in saline frost flowers and implications for atmospheric chemistry and microbial dispersal. Geophys Res Lett 37:L13501. doi:10.1029/2010GL043020

    Article  Google Scholar 

  • Brierley AS, Thomas DN (2002) Ecology of Southern Ocean pack ice. Adv Mar Biol 43:171–276. doi:10.1016/S0065-2881(02)43005-2

    Article  PubMed  Google Scholar 

  • Brinkmeyer R, Knittel K, Jürgens J, Weyland H, Amann R, Helmke E (2003) Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl Environ Microbiol 69:6610–6619. doi:10.1128/AEM.69.11.6610-6619.2003

    Article  PubMed  CAS  Google Scholar 

  • Caron DA, Gast RJ (2010) Heterotrophic protists associated with sea ice. In: Thomas DN, Dieckmann GS (eds) Sea ice, 2nd edn. Blackwell, Oxford, pp 327–356

    Google Scholar 

  • Clarke DB, Ackley SF (1984) Sea ice structure and biological activity in the Antarctic marginal ice zone. J Geophys Res 89:2087–2095

    Article  Google Scholar 

  • Collins RE, Rocap G, Deming JW (2010) Persistence of bacterial and archaeal communities in sea ice through an Arctic winter. Environ Microbiol 12:1828–1841

    Article  PubMed  CAS  Google Scholar 

  • Cota GF, Prinsenberg SJ, Bennett EB, Loder JW, Lewis MR, Anning JL, Watson NHF, Harris LR (1987) Nutrient fluxes during extended blooms of arctic ice algae. J Geophys Res 92:1951–1962. doi:10.1029/JC092iC02p01951

    Article  CAS  Google Scholar 

  • Deming JW (2010) Sea ice bacteria and viruses. In: Thomas DN, Dieckmann GS (eds) Sea ice, 2nd edn. Blackwell, Oxford, pp 247–282

    Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Dumont I, Schoemann V, Lannuzel D, Chou L, Tison JL, Becquevort S (2009) Distribution and characterization of dissolved and particulate organic matter in Antarctic pack ice. Polar Biol 32:733–750

    Article  Google Scholar 

  • Engel N, Jenny TA, Mooser V, Gossauer A (1991) Chlorophyll catabolism in Chlorella protothecoides—isolation and structure elucidation of a red bilin derivative. FEBS Lett 293:131–133

    Article  PubMed  CAS  Google Scholar 

  • Ewert MEM, Deming JW (2011) Selective retention in saline ice of extracellular polysaccharides produced by the cold-adapted marine bacterium Colwellia psychrerythraea strain 34H. Ann Glaciol 52:111–117

    Article  CAS  Google Scholar 

  • Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64:3352–3358

    PubMed  CAS  Google Scholar 

  • Garrison DL, Close AR, Gordon LI (1990) Nutrient concentrations in Antarctic pack ice during the austral winter. In: Ackley SF, Weeks WF (eds) Sea ice properties and processes. Proceedings of W. F. weeks sea ice symposium, CRREL, Monograph 90–91, pp 35–40

  • Gasol JM, Zweifel UL, Peters F, Fuhrman JA, Hagstrom A (1999) Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl Environ Microbiol 65:4475–4483

    PubMed  CAS  Google Scholar 

  • Giannelli V, Thomas DN, Haas C, Kattner G, Kennedy H, Dieckmann GS (2001) Behaviour of dissolved organic matter and inorganic nutrients during experimental sea ice formation. Ann Glaciol 33:317–321. doi:10.3189/172756401781818572

    Article  CAS  Google Scholar 

  • Gleitz M, von der loeff MR, Thomas DN, Dieckmann GS, Millero FJ (1995) Comparison of summer and winter inorganic carbon, oxygen and nutrient concentrations in antarctic sea-ice brine. Mar Chem 51:81–91

    Article  CAS  Google Scholar 

  • Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie, Weinheim

    Google Scholar 

  • Hales B, van Geen A, Takahashi T (2004) High-frequency measurement of seawater chemistry: flow-injection analysis of macronutrients. Limnol Oceanogr Meth 2:91–101

    Article  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 

  • Herborg LM, Thomas DN, Kennedy H, Haas C, Dieckmann GS (2001) Dissolved carbohydrates in Antarctic sea ice. Antarct Sci 13:119–125

    Article  Google Scholar 

  • Hoagland KD, Rosowski JR, Gretz MR, Roemer SC (1993) Diatom extracellular polymeric substances—function, fine-structure, chemistry, and physiology. J Phycol 29:537–566

    Article  CAS  Google Scholar 

  • Hofmann T, Hanlon ARM, Taylor JD, Ball AS, Osborn AM, Underwood GJC (2009) Dynamics and compositional changes in extracellular carbohydrates in estuarine sediments during degradation. Mar Ecol Prog Ser 379:45–58

    Article  CAS  Google Scholar 

  • Holmes RM, Aminot A, Kerouel R, Hooker BA, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808. doi:10.1139/cjfas-56-10-1801

    CAS  Google Scholar 

  • Horner R, Ackley SF, Dieckmann GS, Gulliksen B, Hoshiai T, Legendre L, Melnikov IA, Reeburgh WS, Spindler M, Sullivan CW (1992) Ecology of sea ice biota. Polar Biol 12:417–427

    Article  Google Scholar 

  • Hortensteiner S, Chinner J, Matile P, Thomas H, Donnison IS (2000) Chlorophyll breakdown in Chlorella protothecoides: characterization of degreening and cloning of degreening-related genes. Plant Mol Biol 42:439–450

    Article  PubMed  CAS  Google Scholar 

  • Juhl AR, Krembs C, Meiners KM (2011) Seasonal development and differential retention of ice algae and other organic fractions in first-year Arctic sea ice. Mar Ecol Prog Ser 436:1–16. doi:10.3354/meps09277

    Article  CAS  Google Scholar 

  • Junge K, Krembs C, Deming J, Stierle A, Eicken H (2001) A microscopic approach to investigate bacteria under in situ conditions in sea-ice samples. Ann Glaciol 33:304–310. doi:10.3189/172756401781818275

    Article  CAS  Google Scholar 

  • Junge K, Imhoff F, Staley T, Deming JW (2002) Phylogenetic diversity of numerically important arctic sea-ice bacteria cultured at subzero temperature. Microb Ecol 43:315–328

    Article  PubMed  CAS  Google Scholar 

  • Kaartokallio H (2004) Food web components, and physical and chemical properties of Baltic Sea ice. Mar Ecol Prog Ser 273:49–63

    Article  CAS  Google Scholar 

  • Kaartokallio H, Laamanen M, Sivonen K (2005) Responses of Baltic Sea ice and open-water natural bacterial communities to salinity change. Appl Environ Microbiol 71:4364–4371

    Article  PubMed  CAS  Google Scholar 

  • Kaartokallio H, Tuomainen J, Kuosa H, Kuparinen J, Martikainen PJ, Servomaa K (2008) Succession of sea-ice bacterial communities in the Baltic Sea fast ice. Polar Biol 31:783–793

    Article  Google Scholar 

  • Kaleschke L, Richter A, Burrows J, Afe O, Heygster G, Notholt J, Rankin AM, Roscoe HK, Hollwedel J, Wagner T, Jacobi HW (2004) Frost flowers on sea ice as a source of sea salt and their influence on tropospheric halogen chemistry. Geophys Res Lett 31:L16114. doi:10.1029/2004GL020655

    Article  Google Scholar 

  • Kattner G, Thomas DN, Haas C, Kennedy H, Dieckmann GS (2004) Surface ice and gap layers in Antarctic sea ice: highly productive habitats. Mar Ecol Prog Ser 277:1–12

    Article  Google Scholar 

  • Krembs C, Deming JW (2008) The role of exopolymers in microbial adaptation to sea-ice. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 247–264

    Chapter  Google Scholar 

  • Krembs C, Eicken H, Junge K, Deming JW (2002) High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep Sea Res I 49:2163–2181

    Article  CAS  Google Scholar 

  • Krembs C, Eicken H, Deming JW (2011) Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc Natl Acad Sci USA 108:3653–3658

    Article  PubMed  CAS  Google Scholar 

  • Kroon H (1993) Determination of nitrogen in water—comparison of a continuous-flow method with online UV digestion with the original kjeldahl method. Anal Chim Acta 276:287–293

    Article  CAS  Google Scholar 

  • Kuosa H, Kaartokallio H (2006) Experimental evidence on nutrient and substrate limitation of Baltic Sea sea-ice algae and bacteria. Hydrobiologia 554:1–10

    Article  CAS  Google Scholar 

  • Mancuso Nichols C, Bowman JP, Guezennec J (2005) Effects of incubation temperature on growth and production of exopolysaccharides by an Antarctic sea ice bacterium grown in batch culture. Appl Environ Microbiol 71:3519–3523

    Article  Google Scholar 

  • McConville MJ, Wetherbee R, Bacic A (1999) Subcellular location and composition of the wall and secreted extracellular sulphated polysaccharides/proteoglycans of the diatom Stauroneis amphioxys Gregory. Protoplasma 206:188–200

    Article  CAS  Google Scholar 

  • Meiners K, Gradinger R, Fehling J, Civitarese G, Spindler M (2003) Vertical distribution of exopolymer particles in sea ice of the Fram Strait (Arctic) during autumn. Mar Ecol Prog Ser 248:1–13

    Article  CAS  Google Scholar 

  • Meiners K, Krembs C, Gradinger R (2008) Exopolymer particles: microbial hotspots of enhanced bacterial activity in Arctic fast ice (Chukchi Sea). Aquat Microb Ecol 52:195–207

    Article  Google Scholar 

  • Mock T, Thomas DN (2005) Recent advances in sea-ice microbiology. Environ Microbiol 7:605–619

    Article  PubMed  CAS  Google Scholar 

  • Norman L, Thomas DN, Stedmon CA, Granskog MA, Papadimitriou S, Krapp RH, Meiners KM, Lannuzel D, van der Merwe P, Dieckmann GS (2011) The characteristics of dissolved organic matter (DOM) and chromophoric dissolved organic matter (CDOM) in Antarctic sea ice. Deep Sea Res II 58:1075–1091

    Article  CAS  Google Scholar 

  • Papadimitriou S, Thomas DN, Kennedy H, Haas C, Kuosa H, Krell A, Dieckmann GS (2007) Biogeochemical composition of natural sea ice brines from the Weddell Sea during early austral summer. Limnol Oceanogr 52:1809–1823

    Article  CAS  Google Scholar 

  • Petrich C, Eicken H (2010) Growth, structure and properties of sea ice. In: Thomas DN, Dieckmann GS (eds) Sea ice, 2nd edn. Blackwell, Oxford, pp 23–77

    Google Scholar 

  • Piot M, von Glasow R (2007) The potential importance of frost flowers, recycling on snow, and open leads for ozone depletion events. Atmos Chem Phys Discuss 7:4521–4595. doi:10.5194/acpd-7-4521-2007

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Qian JG, Mopper K (1996) Automated high performance, high-temperature combustion total organic carbon analyzer. Anal Chem 68:3090–3097

    Article  CAS  Google Scholar 

  • Rankin AM, Wolff EW, Martin S (2002) Frost flowers: implications for tropospheric chemistry and ice core interpretation. J Geophys Res 107:4683. doi:10.1029/20021JD002492

    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 (2007) Enrichment of nutrients, exopolymeric substances and microorganisms in newly formed sea ice on the Mackenzie shelf. Mar Ecol Prog Ser 342:55–67

    Article  CAS  Google Scholar 

  • Shaw PM, Russell LM, Jefferson A, Quinn PK (2010) Arctic organic aerosol measurements show particles from mixed combustion in spring haze and from frost flowers in winter. Geophys Res Lett 37:L10803. doi:10.1029/2010GL042831

    Article  Google Scholar 

  • Stedmon CA, Thomas DN, Granskog M, Kaartokallio H, Papadimitriou S, Kuosa H (2007) Characteristics of dissolved organic matter in Baltic coastal sea ice: Allochthonous or autochthonous origins? Environ Sci Technol 41:7273–7279

    Article  PubMed  CAS  Google Scholar 

  • Stewart FJ, Fritsen CH (2004) Bacteria–algae relationships in Antarctic sea ice. Antarct Sci 16:143–156

    Article  Google Scholar 

  • Style RW, Worster MG (2009) Frost flower formation on sea ice and lake ice. Geophys Res Lett 36:L11501. doi:10.1029/2009GL037304

    Article  Google Scholar 

  • Sutherland IW (1990) Biotechnology of microbial exopolysaccharides. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Thomas DN, Kattner G, Engbrodt R, Giannelli V, Kennedy H, Haas C, Dieckmann GS (2001) Dissolved organic matter in Antarctic sea ice. Ann Glaciol 33:297–303. doi:10.3189/172756401781818338

    Article  CAS  Google Scholar 

  • Tranvik LJ (1990) Bacterioplankton growth on fractions of dissolved organic-carbon of different molecular-weights from humic and clear waters. Appl Environ Microbiol 56:1672–1677

    PubMed  CAS  Google Scholar 

  • Underwood GJC, Boulcott M, Raines CA, Waldron K (2004) Environmental effects on exopolymer production by marine benthic diatoms: dynamics, changes in composition, and pathways of production. J Phycol 40:293–304

    Article  CAS  Google Scholar 

  • Underwood GJC, Fietz S, Papadimitriou S, Thomas DN, Dieckmann GS (2010) Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice. Mar Ecol Prog Ser 404:1–19

    Article  CAS  Google Scholar 

  • van der Merwe P, Lannuzel D, Nichols CAM, Meiners K, Heil P, Norman L, Thomas DN, Bowie AR (2009) Biogeochemical observations during the winter-spring transition in East Antarctic sea ice: evidence of iron and exopolysaccharide controls. Mar Chem 115:163–175

    Article  Google Scholar 

  • Volkman JK, Tanoue E (2002) Chemical and biological studies of particulate organic matter in the ocean. J Oceanogr 58:265–279. doi:10.1023/A:1015809708632

    Article  CAS  Google Scholar 

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Acknowledgments

The work described in this report was supported by the European Community’s Sixth Framework Programme through the grant to the budget of the Integrated Infrastructure Initiative HYDRALAB III, Contract no. 022441(RII3) and U.K. Natural Environment Research Council (NE/E016251/1). The authors would like to thank the Hamburg Ship Model Basin (HSVA), especially Kalle Evers and the ice tank crew, for the hospitality, technical and scientific support and the professional execution of the test programme in the Research Infrastructure ARCTECLAB. We are indebted to Naomi Thomas for the unenviable task of producing the ADOM additive and her support in nutrient and DOM analyses. Erika Allhusen provided essential support for the setting up and successful execution of the experiment. We thank Dr Ben Green for PRIMER analysis. We are very grateful to 3 anonymous reviewers for their detailed and highly constructive suggestions on an earlier draft of the manuscript.

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Correspondence to Shazia N. Aslam.

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Aslam, S.N., Underwood, G.J.C., Kaartokallio, H. et al. Dissolved extracellular polymeric substances (dEPS) dynamics and bacterial growth during sea ice formation in an ice tank study. Polar Biol 35, 661–676 (2012). https://doi.org/10.1007/s00300-011-1112-0

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