Sea ice microorganisms: Environmental constraints and extracellular responses

Biology

Volumn 2, Issue 2, 2013, Pages 603-628

  Ewert, Marcela ^a   Deming, Jody W ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Bacteria; Extracellular polymeric substances; Halophiles; Sea ice

Indexed keywords

EID: 84896853008     PISSN: None     EISSN: 20797737     Source Type: Journal    
DOI: 10.3390/biology2020603     Document Type: Article

References (128)

1. Junge, K.; Eicken, H.; Deming, J.W. Bacterial activity at-2 to-20 °C in Arctic wintertime sea ice. Appl. Environ. Microbiol. 2004, 70, 550-557.
2. Søgaard, D.H.; Kristensen, M.; Rysgaard, S.; Glud, R.N.; Hansen, P.J.; Hilligsøe, K.M. Autotrophic and heterotrophic activity in Arctic first-year sea ice: Seasonal study from Malene Bight, SW Greenland. Mar. Ecol. Prog. Ser. 2010, 419, 31-45.
3. Brown, M.V.; Bowman, J.P. A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol. Ecol. 2001, 35, 267-275.
4. Brinkmeyer, R.; Knittel, K.; Jürgens, J.; Weyland, H.; Amann, R.; Helmke, E. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl. Environ. Microbiol. 2003, 69, 6610-6619.
5. Bowman, J.S.; Rasmussen, S.; Blom, N.; Deming, J.W.; Rysgaard, S.; Sicheritz-Ponten, T. Microbial community structure of Arctic multiyear sea ice and surface seawater by 454 sequencing of the 16S RNA gene. ISME J. 2012, 6, 11-20.
6. Maas, E.W.; Simpson, A.M.; Martin, A.; Thompson, S.; Koh, E.Y.; Davy, S.K.; Ryan, K.G.; O'Toole, R.F. Phylogenetic analyses of bacteria in sea ice at Cape Hallett, Antarctica. N. Z. J. Mar. Freshw. Res. 2012, 46, 3-12.
7. Horner, R.; Ackley, S.F.; Dieckmann, G.S.; Gulliksen, B.; Hoshiai, T.; Legendre, L.; Melnikov, I.A.; Reeburgh, W.S.; Spindler, M.; Sullivan, C.W. Ecology of sea ice biota. Polar Biol. 1992, 12, 417-427.
8. Gradinger, R.; Ikävalko, J. Organism incorporation into newly forming Arctic sea ice in the Greenland Sea. J. Plankton Res. 1998, 20, 871-886.
9. Krembs, C.; Gradinger, R.; Spindler, M. Implications of brine channel geometry and surface area for the interaction of sympagic organisms in Arctic sea ice. J. Exp. Mar. Biol. Ecol. 2000, 243, 55-80.
10. Lizotte, M.P. The microbiology of sea ice. In Sea Ice: An Introduction to Its Physics, Chemistry, Biology and Geology; Thomas, D.N., Dieckmann, G.S., Eds.; Wiley-Blackwell: Oxford, UK, 2003; pp. 184-210.
11. Collins, R.E.; Rocap, G.; Deming, J.W. Persistence of bacterial and archaeal communities in sea ice through an Arctic winter. Environ. Microbiol. 2010, 12, 1828-1841.
12. Miller, L.A.; Papakyriakou, T.N.; Collins, R.E.; Deming, J.W.; Ehn, J.K.; Macdonald, R.W.; Mucci, A.; Owens, O.; Raudsepp, M.; Sutherland, N. Carbon dynamics in sea ice: A winter flux time series. J. Geophys. Res. 2011, 116, C02028.
13. Lee, S.H.; Stockwell, D.A.; Joo, H.M.; Son, Y.B.; Kang, C.K.; Whitledge, T.E. Phytoplankton production from melting ponds on Arctic sea ice. J. Geophys. Res. 2012, 117, C04030.
14. Kaartokallio, H. Evidence for active microbial nitrogen transformations in sea ice (Gulf of Bothnia, Baltic Sea) in midwinter. Polar Biol. 2001, 24, 21-28.
15. 2 production in Arctic sea ice. Limnol. Oceanogr. 2004, 49, 86-94.
16. Delille, D.; Basseres, A.; Dessommes, A. Seasonal variation of bacteria in sea ice contaminated by diesel fuel and dispersed crude oil. Microb. Ecol. 1997, 33, 97-105.
17. Brakstad, O.G.; Nonstad, I.; Faksness, L.G.; Brandvik, P.J. Responses of microbial communities in Arctic sea ice after contamination by crude petroleum oil. Microb. Ecol. 2008, 55, 540-552.
18. Barkay, T.; Poulain, A.J. Mercury (micro) biogeochemistry in polar environments. FEMS Microbiol. Ecol. 2006, 59, 232-241.
19. Møller, A.K.; Barkay, T.; Abu Al-Soud, W.; Sørensen, S.J.; Skov, H.; Kroer, N. Diversity and characterization of mercury-resistant bacteria in snow, freshwater and sea-ice brine from the High Arctic. FEMS Microbiol. Ecol. 2011, 75, 390-401.
20. Assur, A. Composition of Sea Ice and Its Tensile Strength; University of California Libraries: San Diego, CA, USA, 1960; pp. 106-138.
21. Cox, G.F.N.; Weeks, W.F. Equations for determining the gas and brine volumes in sea-ice samples. J. Glaciol. 1983, 29, 306-316.
22. Leppäranta, M.; Manninen, T. The brine and gas content of sea ice with attention to low salinities and high temperatures. Finn. Inst. Mar. Res. Int. Rep. 1988, 2, 1-14.
23. Thomas, D.N.; Papadimitriou, S.; Michel, C. Biogeochemistry of Sea Ice. In Sea Ice, 2nd ed.; Thomas, D.N., Dieckmann, G.S., Eds.; Wiley-Blackwell: Oxford, UK, 2010; pp. 425-467.
24. Petri, R.; Imhoff, J.F. Genetic analysis of sea-ice bacterial communities of the Western Baltic Sea using an improved double gradient method. Polar Biol. 2001, 24, 252-257.
25. Meiners, K.; Krembs, C.; Gradinger, R. Exopolymer particles: Microbial hotspots of enhanced bacterial activity in Arctic fast ice (Chuckchi Sea). Aquat. Microb. Ecol. 2008, 52, 195-207.
26. Brinkmeyer, R.; Glockner, F.O.; Helmke, E.; Amann, R. Predominance of proteobacteria in summer melt pools on Arctic pack ice. Limnol. Oceanogr. 2004, 49, 1013-1021.
27. Gradinger, R.; Meiners, K.; Plumley, G.; Zhang, Q.; Bluhm, B.A. Abundance and composition of the sea-ice meiofauna in off-shore pack ice of the Beaufort Gyre in summer 2002 and 2003. Polar Biol. 2005, 28, 171-181.
28. Mundy, C.J.; Gosselin, M.; Ehn, J.K.; Belzile, C.; Poulin, M.; Alou, E.; Roy, S.; Hop, H.; Lessard, S.; Papakyriakou, T.N.; et al. Characteristics of two distinct high-light acclimated algal communities during advanced stages of sea ice melt. Polar Biol. 2011, 34, 1869-1886.
29. McLean, A.L. Bacteria of ice and snow in Antarctica. Nature 1918, 102, 35-39.
30. Legendre, L.; Ackley, S.F.; Dieckmann, G.S.; Gulliksen, B.; Horner, R.; Hoshiai, T.; Melnikov, I.A.; Reeburgh, W.S.; Spindler, M.; Sullivan, C.W. Ecology of sea ice biota. Polar Biol. 1992, 12, 429-444.
31. Ackley, S.F.; Sullivan, C.W. Physical controls on the development and characteristics of Antarctic sea ice biological communities-A review and synthesis. Deep Sea Res. Part I 1994, 41, 1583-1604.
32. Staley, J.T.; Gosink, J.J. Poles apart: Biodiversity and biogeography of sea ice bacteria. Annu. Rev. Microbiol. 1999, 53, 189-215.
33. Thomas, D.N.; Dieckmann, G.S. Antarctic sea ice-A habitat for extremophiles. Science 2002, 295, 641-644.
34. Mock, T.; Thomas, D.N. Recent advances in sea-ice microbiology. Environ. Microbiol. 2005, 7, 605-619.
35. Deming, J.W. Extremophiles: Cold Environments. In Encyclopedia of Microbiology; Shaechter, M., Ed.; Elsevier: Oxford, UK, 2009; pp. 147-158.
36. Petrich, C.; Eicken, H. Growth, Structure and Properties of Sea Ice. In Sea Ice, 2nd ed.; Thomas, D.N., Dieckmann, G.S., Eds.; Wiley-Blackwell: Oxford, UK, 2010; pp. 247-282.
37. Junge, K.; Krembs, C.; Deming, J.W.; Stierle, A.; Eicken, H. A microscopic approach to investigate bacteria under in-situ conditions in sea-ice samples. Ann. Glaciol. 2001, 33, 304-310.
38. Weissenberger, J.; Grossmann, S. Experimental formation of sea ice: Importance of water circulation and wave action for incorporation of phytoplankton and bacteria. Polar Biol. 1998, 20, 178-188.
39. Garrison, D.L.; Ackley, S.F.; Buck, K.R. A physical mechanism for establishing algal populations in frazil ice. Nature 1983, 306, 363-365.
40. Garrison, D.L.; Close, A.R.; Reimnitz, E. Algae concentrated by frazil ice: Evidence from laboratory experiments and field measurements. Antarct. Sci. 1989, 1, 313-316.
41. Knopf, D.A.; Alpert, P.A.;Wang, B.; Aller, J.Y. Stimulation of ice nucleation by marine diatoms. Nature Geosci. 2011, 4, 88-90.
42. Grossmann, S.; Dieckmann, G.S. Bacterial standing stock, activity, and carbon production during formation and growth of sea ice in the Weddell Sea, Antarctica. Appl. Environ. Microbiol. 1994, 60, 2746-2753.
43. Riedel, A.; Michel, C.; Gosselin, M.; LeBlanc, B. Enrichment of nutrients, exopolymeric substances and microorganisms in newly formed sea ice on the Mackenzie shelf. Mar. Ecol. Prog. Ser. 2007, 342, 55-67.
44. Meiners, K.; Gradinger, R.; Fehling, J.; Civitarese, G.; Spindler, M. Vertical distribution of exopolymer particles in sea ice of the Fram Strait (Arctic) during autumn. Mar. Ecol. Prog. Ser. 2003, 248, 1-13.
45. Deming, J.W. Sea Ice Bacteria and Viruses. In Sea Ice, 2nd ed.; Thomas, D.N., Dieckmann, G.S., Eds.; Wiley-Blackwell: Oxford, UK, 2010; pp. 247-282.
46. Ewert, M.; Deming, J.W. Selective retention in saline ice of extracellular polysaccharides produced by the cold-adapted marine bacterium Colwellia psychrerythraea strain 34H. Ann. Glaciol. 2011, 52, 111-117.
47. Bowman, J.S.; Deming, J.W. Elevated bacterial abundance and exopolymers in saline frost flowers and implications for atmospheric chemistry and microbial dispersal. Geophys. Res. Lett. 2010, 37, L13501, doi:10.1029/2010GL043020.
48. Ewert, M.; Carpenter, S.D.; Colangelo-Lillis, J.; Deming, J.W. Bacterial and extracellular polysaccharide content of brine-wetted snow over Arctic winter first-year sea ice. J. Geophys. Res. 2013, doi:10.1002/jgrc.20055.
49. Collins, R.E.; Carpenter, S.D.; Deming, J.W. Spatial heterogeneity and temporal dynamics of particles, bacteria, and pEPS in Arctic winter sea ice. J. Mar. Syst. 2008, 74, 902-917.
50. Druckenmiller, M.L.; Eicken, H.; Johnson, M.; Pringle, D.; Williams, C. Towards an integrated coastal sea-ice observatory: System components and a case study at Barrow, Alaska. Cold Reg. Sci. Technol. 2009, 56, 61-72.
51. Georlette, D.; Blaise, V.; Collins, T.; D'Amico, S.; Gratia, E.; Hoyoux, A.; Marx, J.C.; Sonan, G.; Feller, G.; Gerday, C. Some like it cold: Biocatalysis at low temperatures. FEMS Microbiol. Rev. 2004, 28, 25-42.
52. Bakermans, C.; Tollaksen, S.L.; Giometti, C.S.; Wilkerson, C.; Tiedje, J.M.; Thomashow, M.F. Proteomic analysis of Psychrobacter cryohalolentis K5 during growth at subzero temperatures. Extremophiles 2007, 11, 343-354.
53. Shivaji, S.; Prakash, J.S.S. How do bacteria sense and respond to low temperature? Arch. Microbiol. 2010, 192, 85-95.
54. Bowman, J.P.; McCammon, S.A.; Brown, M.V.; Nichols, D.S.; McMeekin, T.A. Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl. Environ. Microbiol. 1997, 63, 3068-3078.
55. Huston, A.L.; Krieger-Brockett, B.B.; Deming, J.W. Remarkably low temperature optima for extracellular enzyme activity from Arctic bacteria and sea ice. Environ. Microbiol. 2001, 2, 383-388.
56. Deming, J.W. Life in Ice Formations at Very Cold Temperatures. In Physiology and Biochemistry of Extremophiles; ASM Press: Washington, DC, USA, 2007; pp. 133-144.
57. Weissenberger, J.; Dieckmann, G.; Gradinger, R.; Spindler, M. Sea ice: A cast technique to examine and analyze brine pockets and channel structure. Limnol. Oceanogr. 1992, 37, 179-183.
58. Golden, K.M.; Eicken, H.; Heaton, A.L.; Miner, J.; Pringle, D.J.; Zhu, J. Thermal evolution of permeability and microstructure in sea ice. Geophys. Res. Lett. 2007, 34, L16501.
59. Golden, K.M.; Ackley, S.F.; Lytle, V.I. The percolation phase transition in sea ice. Science 1998, 282, 2238-2241.
60. 2 exchange in the Arctic and Southern Oceans. Tellus B 2011, 63, 823-830.
61. Collins, R.E.; Deming, J.W. Abundant dissolved genetic material in Arctic sea ice Part II: Viral dynamics during autumn freeze-up. Polar Biol. 2011, 34, 1831-1841.
62. Collins, R.E.; Deming, J.W. Abundant dissolved genetic material in Arctic sea ice Part I: Extracellular DNA. Polar Biol. 2011, 34, 1819-1830.
63. Wells, L.E.; Deming, J.W. Modelled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ. Microbiol. 2006, 8, 1115-1121.
64. Collins, R.E. Microbial evolution in sea ice: Communities to genes. PhD thesis, University of Washington, Seattle, WA, USA, 2009.
65. Gradinger, R.; Friedrich, C.; Spindler, M. Abundance, biomass and composition of the sea ice biota of the Greenland Sea pack ice. Deep Sea Res. Part II 1999, 46, 1457-1472.
66. Krembs, C.; Eicken, H.; Deming, J.W. Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc. Natl. Acad. Sci. USA 2011, 108, 3653-3658.
67. Janech, M.G.; Krell, A.; Mock, T.; Kang, J.; Raymond, J.A. Ice-binding proteins from sea ice diatoms (Bacillarophyceae). J. Phycol. 2006, 42, 410-416.
68. Raymond, J.A.; Fritsen, C.; Shen, K. An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol. Ecol. 2007, 61, 214-221.
69. Raymond, J.A. Algal ice-binding proteins change the structure of sea ice. Proc. Natl. Acad. Sci. USA 2011, 108, E198.
70. Bayer-Giraldi, M.; Weikusat, I.; Besir, H.; Dieckmann, G. Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice. Cryobiology 2011, 63, 210-219.
71. Dinnbier, U.; Limpinsel, E.; Schmid, R.; Bakker, E.P. Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations. Arch. Microbiol. 1988, 150, 348-357.
72. Wood, J.M. Osmosensing by bacteria: Signals and membrane-based sensors. Microbiol. Mol. Biol. Rev. 1999, 63, 230-262.
73. Roberts, M. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst. 2005, 1, doi:10.1186/1746-1448-1-5.
74. Mao, X.; Olman, V.; Stuart, R.; Paulsen, I.T.; Palenik, B.; Xu, Y. Computational prediction of the osmoregulation network in Synechococcus sp. WH8102. BMC Genomics 2010, 11, 291.
75. Kennedy, S.P.; Ng, W.V.; Salzberg, S.L.; Hood, L.; DasSarma, S. Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res. 2001, 11, 1641-1650.
76. Saum, S.H.; Pfeiffer, F.; Palm, P.; Rampp, M.; Schuster, S.C.; Müller, V.; Oesterhelt, D. Chloride and organic osmolytes: A hybrid strategy to cope with elevated salinities by the moderately halophilic, chloride-dependent bacterium Halobacillus halophilus. Environ. Microbiol. 2012, doi:10.1111/j.1462-2920.2012.02770.x.
77. Aslam, S.; Cresswell-Maynard, T.; Thomas, D.N.; Underwood, G.J.C. Production and characterization of the intra-and extracellular carbohydrates and polymeric substances (EPS) of three sea-ice diatom species, and evidence for a cryoprotective role for EPS. J. Phycol. 2012, 48, 1494-1509.
78. Liu, S.B.; Chen, X.L.; He, H.L.; Zhang, X.Y.; Xie, B.B.; Yu, Y.; Chen, B.; Zhou, B.C.; Zhang, Y.Z. Structure and ecological roles of a novel exopolysaccharide from the Arctic sea ice bacterium Pseudoalteromonas sp. Strain SM20310. Appl. Environ. Microbiol. 2013, 79, 224-230.
79. Ghosh, D.; Roy, K.; Williamson, K.E.; Srinivasiah, S.; Wommack, K.E.; Radosevich, M. Acyl-homoserine lactones can induce virus production in lysogenic bacteria: An alternative paradigm for prophage induction. Appl. Environ. Microbiol. 2009, 75, 7142-7152.
80. Shkilnyj, P.; Koudelka, G.B. Effect of salt shock on stability of imm433 lysogens. J. Bacteriol. 2007, 189, 3115-3123.
81. ExPASy. SIB Bioinformatics Resource Portal, Compute pI/Mw. Available online: http://web.expasy.org/compute pi/(accessed on 1 November 2012).
82. Universal Protein Resource (UniProt). Available online: http://www.uniprot.org/uniprot/ (accessed on 1 November 2012).
83. Thomas, V.K.; Kuehn, K.A.; Francoeur, S.N. Effects of UV radiation on wetland periphyton: Algae, bacteria, and extracellular polysaccharides. J. Freshw. Ecol. 2009, 24, 315-326.
84. Underwood, G.J.C.; Nilsson, C.; Sundbäck, K.; Wulff, A. Short-term effects of UVB radiation on chlorophyll fluorescence, biomass, pigments, and carbohydrate fractions in a benthic diatom mat. J. Phycol. 1999, 35, 656-666.
85. Jeffrey, S.W.; MacTavish, H.S.; Dunlap, W.C.; Vesk, M.; Groenewoud, K. Occurrence of UVA-and UVB-absorbing compounds in 152 species (206 strains) of marine microalgae. Mar. Ecol. Prog. Ser. 1999, 189, 35-51.
86. Uusikivi, J.; Vähätalo, A.V.; Granskog, M.A.; Sommaruga, R. Contribution of mycosporine-like amino acids and colored dissolved and particulate matter to sea ice optical properties and ultraviolet attenuation. Limnol. Oceanogr. 2010, 55, 703-713.
87. Horner, R.; Schrader, G.C. Relative contributions of ice algae, phytoplankton, and benthic microalgae to primary production in nearshore regions of the Beaufort Sea. Arctic 1982, 4, 485-503.
88. Norman, L.; Thomas, D.N.; Stedmon, C.A.; Granskog, M.A.; Papadimitriou, S.; Krapp, R.H.; Meiners, K.M.; Lannuzel, D.; van der Merwe, P.; Dieckmann, G.S. The characteristics of dissolved organic matter (DOM) and chromophoric dissolved organic matter (CDOM) in Antarctic sea ice. Deep Sea Res. Part II 2011, 58, 1075-1091.
89. Ortega-Retuerta, E.; Passow, U.; Duarte, C.M.; Reche, I. Effects of ultraviolet B radiation on (not so) transparent exopolymer particles. Biogeosci. Discuss. 2009, 6, 7599-7625.
90. Cockell, C.; Rettberg, P.; Horneck, G.; Scherer, K.; Stokes, D.M. Measurements of microbial protection from ultraviolet radiation in polar terrestrial microhabitats. Polar Biol. 2003, 26, 62-69.
91. Sturm, M.; Massom, R.A. Snow and Sea Ice. In Sea Ice, 2nd ed.; Thomas, D.N., Dieckmann, G.S., Eds.; Wiley-Blackwell: Oxford, UK, 2010; pp. 153-204.
92. Ruas-Madiedo, P.; de los Reyes-Gavilán, C.G. Methods for the screening, isolation and characterization of exopolysaccharides produced by lactic acid bacteria. J. Dairy Sci. 2005, 88, 843-856.
93. Mancuso Nichols, C.; Garon Lardière, S.; Bowman, J.P.; Nichols, P.D.; Gibson, J.A.E.; Guézennec, J. Chemical characterization of exopolysaccharides from Antarctic marine bacteria. Microb. Ecol. 2005, 49, 578-589.
94. Lemoine, J.; Chirat, F.; Wieruszeski, J.M.; Strecker, G.; Favre, N.; Neeser, J.R. Structural characterization of the exocellular polysaccharides produced by Streptococcus thermophilus SFi39 and SFi12. Appl. Environ. Microbiol. 1997, 63, 3512-3518.
95. Schiano Moriello, V.; Lama, L.; Poli, A.; Gugliandolo, C.; Maugeri, T.L.; Gambacorta, A.; Nicolaus, B. Production of exopolysaccharides from a thermophilic microorganism isolated from a marine hot spring in flegrean areas. J. Ind. Microbiol. Biotechnol. 2003, 30, 95-101.
96. Vyrides, I.; Stuckey, D. Adaptation of anaerobic biomass to saline conditions: Role of compatible solutes and extracellular polysaccharides. Enzyme Microb. Technol. 2009, 44, 46-51.
97. Mancuso Nichols, C.; Bowman, J.P.; Guezennec, J. Effects of incubation temperature on growth and production of exopolysaccharides by an Antarctic sea ice bacterium grown in batch culture. Appl. Environ. Microbiol. 2005, 71, 3519-3523.
98. Guibaud, G.; Comte, S.; Bordas, F.; Dupuy, S.; Baudu, M. Comparison of the complexation potential of extracellular polymeric substances (EPS), extracted from activated sludge and produced by pure bacterial strains, for cadmium, lead and nickel. Chemosphere 2005, 59, 629-638.
99. Decho, A.W. Microbial Exopolymer Secretions in Ocean Environments: Their Role(s) in Food Webs and Marine Processes. In Oceanography and Marine Biology, an Annual Review; Barnes, H., Barnes, M., Eds.; Aberdeen University Press: Aberdeen, UK, 1990; Volume 28, pp. 73-153.
100. Ding, Y.X.; Chin, W.C.; Rodriguez, A.; Hung, C.C.; Santschi, P.H.; Verdugo, P. Amphiphilic exopolymers from Sagittula stellata induce DOM self-assembly and formation of marine microgels. Mar. Chem. 2008, 112, 11-19.
101. Krembs, C.; Eicken, H.; Junge, K.; Deming, J.W. High concentrations of exopolymeric substances in Arctic winter sea ice: Implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep Sea Res. Part I 2002, 49, 2163-2181.
102. Aslam, S.; Underwood, G.J.C.; Kaartokallio, H.; Norman, L.; Autio, R.; Fischer, M.; Kuosa, H.; Dieckmann, G.S.; Thomas, D.N. Dissolved extracellular polymeric substances (dEPS) dynamics and bacterial growth during sea ice formation in an ice tank study. Polar Biol. 2012, 35, 661-676.
103. Underwood, G.J.C.; Fietz, S.; Papadimitriou, S.; Thomas, D.N.; Dieckmann, G. Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice. Mar. Ecol. Prog. Ser. 2010, 404, 1-19.
104. Wolfaardt, G.M.; Lawrence, J.R.; Korber, D.R. Function of EPS. In Microbial Extracellular Polymeric Substances;Wingender, J., Neu, T.R., Flemming, H.-C., Eds.; Springer Verlag: Berlin, Germany, 1999; pp. 171-200.
105. Mora, P.; Rosconi, F.; Franco Fraguas, L.; Castro-Sowinski, S. Azospirillum brasilense Sp7 produces an outer-membrane lectin that specifically binds to surface-exposed extracellular polysaccharide produced by the bacterium. Arch. Microbiol. 2008, 189, 519-524.
106. Lind, J.L.; Heimann, K.; Miller, E.A.; van Vliet, C.; Hoogenraad, N.J.;Wetherbee, R. Substratum adhesion and gliding in a diatom are mediated by extracellular proteoglycans. Planta 1997, 203, 213-221.
107. Baker, M.G.; Lalonde, S.V.; Konhauser, K.O.; Foght, J.M. Role of extracellular polymeric substances in the surface chemical reactivity of Hymenobacter aerophilus, a psychrotolerant bacterium. Appl. Environ. Microbiol. 2010, 76, 102-109.
108. Bitton, G.; Freihofer, V. Influence of extracellular polysaccharides on the toxicity of copper and cadmium toward Klebsiella aerogenes. Microb. Ecol. 1977, 4, 119-125.
109. Knowes, E.J.; Castenholz, R.W. Effect of exogenous extracellular polysaccharides on the dessication and freezing tolerance of rock-inhabiting phototrophic microorganisms. FEMS Microbiol. Ecol. 2008, 66, 261-270.
110. Ozturk, S.; Aslim, B. Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ. Sci. Pollut. R. 2010, 17, 595-602.
111. Marx, J.G.; Carpenter, S.D.; Deming, J.W. Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditions. Can. J. Microbiol. 2009, 55, 63-72.
112. Krembs, C.; Deming, J.W. The role of exopolymers in microbial adaptation to sea ice. In Psychrophiles: From Biodiversity to Biotechnology; Margesin, R., Schinner, F., Marx, J.C., Gerda, C., Eds.; Springer-Verlag: Berlin, Germany, 2008; pp. 247-264.
113. Mancuso Nichols, C.; Guezennec, J.; Bowman, J.P. Bacterial exopolysaccharides from extreme marine environments with special consideration of the southern ocean, sea ice, and deep-sea hydrothermal vents: A review. Mar. Biotechnol. 2005, 7, 253-271.
114. Verdugo, P. Marine microgels. Annu. Rev. Mar. Sci. 2012, 4, 375-400.
115. 2 system dynamics. Cryosphere 2013, in press.
116. Fischer, M.; Thomas, D.N.; Krell, A.; Nehrke, G.; Göttlicher, J.; Norma, L.; Riaux-Gobin, C.; Dieckmann, G. Quantification of ikaite in Antarctic sea ice. Cryosphere Discuss. 2012, 6, 505-530.
117. Chave, K.E.; Suess, E. Calcium carbonate saturation in seawater: Effects of dissolved organic matter. Limnol. Oceanogr. 1970, 15, 633-637.
118. Braissant, O.; Cailleau, G.; Dupraz, C.; Verrecchia, E.P. Bacterially induced mineralization of calcium carbonate in terrestrial environments: The role of exopolysaccharides and amino acids. J. Sediment. Res. 2003, 73, 485-490.
119. Bergmann, D.; Furth, G.; Mayer, C. Binding of bivalent cations by xanthan in aqueous solution. Int. J. Biol. Macromol. 2008, 43, 245-251.
120. Farris, S.; Mora, L.; Capretti, G.; Piergiovanni, L. Charge density quantification of polyelectrolyte polysaccharides by conductometric titration: An analytical chemistry experiment. J. Chem. Educ. 2011, 89, 121-124.
121. Hardikar, V.V.; Matijević, E. Influence of ionic and nonionic dextrans on the formation of calcium hydroxide and calcium carbonate particles. Colloid. Surf. A 2001, 186, 23-31.
122. Comte, S.; Guibaud, G.; Baudu, M. Biosorption properties of extracellular polymeric substances (EPS) towards Cd, Cu and Pb for different pH values. J. Hazard Mater. 2008, 151, 185-193.
123. Zhang, D.; Lee, D.J.; Pan, X. Desorption of Hg (II) and Sb (V) on extracellular polymeric substances: Effects of pH, EDTA, Ca (II) and temperature shocks. Bioresour. Technol. 2013, 128, 711-715.
124. Bhaskar, P.V.; Bhosle, N.B. Bacterial extracellular polymeric substance (EPS): A carrier of heavy metals in the marine food-chain. Environ. Int. 2006, 32, 191-198.
125. Schlekat, C.E.; Decho, A.W.; Chandler, G.T. Bioavailability of particle-associated silver, cadmium, and zinc to the estuarine amphipod Leptocheirus plumulosus through dietary ingestion. Limnol. Oceanogr. 2000, 45, 11-21.
126. Campbell, L.M.; Norstrom, R.J.; Hobson, K.A.; Muir, D.C.G.; Backus, S.; Fisk, A.T. Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci. Total Environ. 2005, 351, 247-263.
127. Turgeon, S.L.; Schmitt, C.; Sanchez, C. Protein-polysaccharide complexes and coacervates. Curr. Opin. Colloid Interface Sci. 2007, 12, 166-178.
128. Huston, A.L.; Methe, B.; Deming, J.W. Purification, characterization, and sequencing of an extracellular cold-active aminopeptidase produced by marine psychrophile Colwellia psychrerythraea strain 34H. Appl. Environ. Microbiol. 2004, 70, 3321-3328.