Diatoms and other algae not only survive, but thrive in sea ice. Among sea ice diatoms, all species examined so far produce ice-binding proteins (IBPs), whereas no such proteins are found in non-ice-associated diatoms, which strongly suggests that IBPs are essential for survival in ice. The restricted occurrence also raises the question of how the IBP genes were acquired. Proteins with similar sequences and ice-binding activities are produced by ice-associated bacteria, and so it has previously been speculated that the genes were acquired by horizontal transfer (HGT) from bacteria. Here we report several new IBP sequences from three types of ice algae, which together with previously determined sequences reveal a phylogeny that is completely incongruent with algal phylogeny, and that can be most easily explained by HGT. HGT is also supported by the finding that the closest matches to the algal IBP genes are all bacterial genes and that the algal IBP genes lack introns. We also describe a highly freeze-tolerant bacterium from the bottom layer of Antarctic sea ice that produces an IBP with 47% amino acid identity to a diatom IBP from the same layer, demonstrating at least an opportunity for gene transfer. Together, these results suggest that the success of diatoms and other algae in sea ice can be at least partly attributed to their acquisition of prokaryotic IBP genes.
References
[1]
Thomas DN, Dieckmann GS (2002) Ocean science - Antarctic Sea ice - a habitat for extremophiles. Science 295: 641–644.
[2]
Horner RA (1985) Taxonomy of sea ice microbiota. In: Horner RA, editor. Sea Ice Biota. Boca Raton, FL: CRC Press. pp. pp. 147–158.
[3]
Kropuenske LR, Mills MM, van Dijken GL, Alderkamp A-C, Berg GM, et al. (2010) Strategies and rates of photoacclimation in two major southern ocean phytoplankton taxa: Phaeocystis antarctica (Haptophyta) and Fragilariopsis cylindrus (Bacillariophyceae). J Phycol 46: 1138–1151.
[4]
Mock T, Valentin K (2004) Photosynthesis and cold acclimation: Molecular evidence from a polar diatom. J Phycol 40: 732–741.
[5]
Krell A, Funck D, Plettner I, John U, Dieckmann G (2007) Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). J Phycol 43: 753–762.
[6]
Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NPA (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70: 222–252.
[7]
Park S, Jung G, Hwang YS, Jin E (2010) Dynamic response of the transcriptome of a psychrophilic diatom, Chaetoceros neogracile, to high irradiance. Planta 231: 349–360.
[8]
Hwang YS, Jung G, Jin E (2008) Transcriptome analysis of acclimatory responses to thermal stress in Antarctic algae. Biochem Biophys Res Commun 367: 635–641.
[9]
Griffith M, Yaish MWF (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9: 399–405.
[10]
Raymond JA, Janech MG (2003) Cryoprotective property of diatom ice-active substance. Cryobiology 46: 203–204.
[11]
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 U S A 108: 3653–3658.
[12]
Price PB (2000) A habitat for psychrophiles in deep Antarctic ice. Proc Natl Acad Sci U S A 97: 1247–1251.
[13]
Raymond JA, Janech MG, Fritsen CH (2009) Novel ice-binding proteins from a psychrophilic Antarctic alga (Chlamydomonadaceae, Chlorophyceae). J Phycol 45: 130–136.
[14]
Raymond JA, Sullivan CW, Devries AL (1994) Release of an ice-active substance by Antarctic sea-ice diatoms. Polar Biol 14: 71–75.
[15]
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, et al. (2004) The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306: 79–86.
[16]
Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, et al. (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239–244.
[17]
Bayer-Giraldi M, Weikusat I, Besir H, Dieckmann G (2011) Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice. Cryobiology 63: 210–219.
[18]
Raymond JA, Christner BC, Schuster SC (2008) A bacterial ice-binding protein from the Vostok ice core. Extremophiles 12: 713–717.
[19]
Raymond JA, Fritsen C, Shen K (2007) An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol Ecol 61: 214–221.
[20]
Hoshino T, Kiriaki M, Ohgiya S, Fujiwara M, Kondo H, et al. (2003) Antifreeze proteins from snow mold fungi. Can J Bot 81: 1175–1181.
[21]
Lee JK, Park KS, Park S, Park H, Song YH, et al. (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60: 222–228.
[22]
Raymond JA, Janech MG (2009) Ice-binding proteins from enoki and shiitake mushrooms. Cryobiology 58: 151–156.
[23]
Janech MG, Krell A, Mock T, Kang JS, Raymond JA (2006) Ice-binding proteins from sea ice diatoms (Bacillariophyceae). J Phycol 42: 410–416.
[24]
Bayer-Giraldi M, Uhlig C, John U, Mock T, Valentin K (2010) Antifreeze proteins in polar sea ice diatoms: diversity and gene expression in the genus Fragilariopsis. Environ Microbiol 12: 1041–1052.
[25]
Goldenfeld N, Woese C (2007) Biology's next revolution. Nature 445: 369–369.
[26]
Parker MS, Mock T, Armbrust EV (2008) Genomic Insights into Marine Microalgae. Annu Rev Genet 42: 619–645.
[27]
Bowler C, Vardi A, Allen AE (2010) Oceanographic and Biogeochemical Insights from Diatom Genomes. Ann Rev Mar Sci 2: 333–365.
[28]
Andersson JO (2009) Gene Transfer and Diversification of Microbial Eukaryotes. Ann Rev Microbiol 63: 177–193.
[29]
Wenzl P, Wong L, Kwang-Won K, Jefferson RA (2005) A functional screen identifies lateral transfer of beta-glucuronidase (gus) from bacteria to fungi. Mol Biol Evol 22: 308–316.
[30]
Belbahri L, Calmin G, Mauch F, Andersson JO (2008) Evolution of the cutinase gene family: Evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 408: 1–8.
Gwak IG, Jung WS, Kim HJ, Kang SH, Jin E (2010) Antifreeze Protein in Antarctic Marine Diatom, Chaetoceros neogracile. Mar Biotechnol 12: 630–639.
[33]
Arrigo KR, Robinson DH, Dunbar RB, Leventer AR, Lizotte MP (2003) Physical control of chlorophyll a, POC, and TPN distributions in the pack ice of the Ross Sea, Antarctica. J Geophys Res 108: 3316–3323.
[34]
McFadden GI, Moestrup O, Wetherbee R (1982) Pyramimonas gelidicola sp. nov. (Prasinophyceae), a new species isolated from Antarctic sea ice. Phycologia 21: 103–111.
[35]
Raymond JA, Fritsen CH (2001) Semipurification and ice recrystallization inhibition activity of ice-active substances associated with Antarctic photosynthetic organisms. Cryobiology 43: 63–70.
[36]
Johnson DB, Rolfe S, Hallberg KB, Iversen E (2001) Isolation and phylogenetic characterization of acidophilic microorganisms indigenous to acidic drainage waters at an abandoned Norwegian copper mine. Environ Microbiol 3: 630–637.
[37]
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.
[38]
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 10: 2731–2739.
[39]
Rampen SW, Schouten S, Panoto FE, Brink M, Andersen RA, et al. (2009) Phylogenetic position of Attheya longicornis and Attheya septentrionalis (Bacillariophyta). J Phycol 45: 444–453.
[40]
Derelle E, Ferraz C, Escande ML, Eychenie S, Cooke R, et al. (2008) Life-Cycle and Genome of OtV5, a Large DNA Virus of the Pelagic Marine Unicellular Green Alga Ostreococcus tauri. Plos One 3: 13.
[41]
Monier A, Pagarete A, de Vargas C, Allen MJ, Read B, et al. (2009) Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus. Genome Res 19: 1441–1449.
[42]
Collins RE, Deming JW (2011) Abundant dissolved genetic material in Arctic sea ice Part I: Extracellular DNA. Polar Biol 34: 1819–1830.
[43]
Collins RE, Deming JW (2011) Abundant dissolved genetic material in Arctic sea ice Part II: Viral dynamics during autumn freeze-up. Polar Biol 34: 1831–1841.
[44]
Andersson JO (2011) Evolution of patchily distributed proteins shared between eukaryotes and prokaryotes: Dictyostelium as a case study. J Mol Microbiol Biotechnol 20: 83–95.
[45]
Kiko R (2010) Acquisition of freeze protection in a sea-ice crustacean through horizontal gene transfer? Polar Biol 33: 543–556.
[46]
Sullivan CW, Palmisano AC (1984) Sea ice microbial communities - Distribution, abundance, and diversity of ice bacteria in McMurdo Sound, Antarctica, in 1980. Appl Environ Microbiol 47: 788–795.
Gosink JJ, Woese CR, Staley JT (1998) Polaribacter gen. nov., with three new species, P-irgensii sp. nov., P-franzmannii sp. nov., and P-filamentus sp. nov., gas vacuolate polar marine bacteria of the Cytophaga-Flavobacterium-Bacteroides group and reclassification of 'Flectobacillus glomeratus' as Polaribacter glomeratus comb. nov. Int J Syst Bacteriol 48: 223–235.
[49]
Yu Y, Li H, Zeng Y, Chen B (2009) Extracellular enzymes of cold-adapted bacteria from Arctic sea ice, Canada Basin. Polar Biol 32: 1539–1547.
[50]
Finneran KT, Johnsen CV, Lovley DR (2003) Rhodoferax ferrireducens sp. nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III). Int J Syst Evol Microbiol 53: 669–673.