Chapter 5 : General Characteristics of Cold-Adapted Microorganisms

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

General Characteristics of Cold-Adapted Microorganisms, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817183/9781555816049_Chap05-1.gif /docserver/preview/fulltext/10.1128/9781555817183/9781555816049_Chap05-2.gif


Although interest in microbes inhabiting low-temperature environments has increased in recent years, significant gaps remain in understanding what makes certain microorganisms cold adapted. Interest in the structural, biochemical, and physiological properties of psychrophilic microorganisms has motivated investigations to characterize the adaptations that maintain enzymatic reaction rates, macromolecular stability, and homeostasis at cold temperature. This chapter provides an overview on the state of knowledge about adaptations that allow certain bacteria and archaea to persist in the coldest regions of the biosphere. In general, the proteins of psychrophilic microorganisms must maintain flexibility to perform catalysis at low temperatures, whereas thermophilic proteins are rigid to protect them from thermal denaturation. Importantly, adaptations that enhance protein flexibility reduce the activation energy needed for the formation of the enzyme-substrate complex, resulting in enhanced catalytic activity at low temperature. The chapter discusses many of the most common and generally understood biochemical and physiological adaptations that appear unique to the psychrophilic lifestyle. Psychrophilic microorganisms use a range of strategies to persist at low temperatures, including possessing catalytically efficient enzymes, synthesizing specialized lipids that increase membrane flexibility, and producing proteins that affect freezing and ice structure. Coupled with technological advances in high-throughput DNA sequencing and proteomics, one can expect that information on cold-adapted bacteria and archaea will increase in the future.

Citation: Doyle S, Dieser M, Broemsen E, Christner B. 2012. General Characteristics of Cold-Adapted Microorganisms, p 103-125. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch5

Key Concept Ranking

Bacteria and Archaea
Bacterial Proteins
Acidic Amino Acids
Elongation Factor 2
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

The effect of temperature on the growth rate of K5 in liquid culture. values for bacterial growth increase with decreasing temperature ( ). A of 2.3, similar to published values for complex communities ( ), is obtained when using the high- and low-temperature data points. (Generation times are based on unpublished data [P. Amato] and the data for growth at −10°C are from .)

Citation: Doyle S, Dieser M, Broemsen E, Christner B. 2012. General Characteristics of Cold-Adapted Microorganisms, p 103-125. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Thermodependence of enzyme activity. α-Amylase activity for (•) and (°), illustrating the greater of the psychrophilic organism's enzyme at low temperature. (Adapted from )

Citation: Doyle S, Dieser M, Broemsen E, Christner B. 2012. General Characteristics of Cold-Adapted Microorganisms, p 103-125. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Bright field image of polycrystalline ice. The image shows narrow, intergranular veins and triple junctions formed between ice crystals. cells that were frozen in LB broth at −20°C on a cryostage were excluded into the vein network during ice formation. The width of the image is 230 µm.

Citation: Doyle S, Dieser M, Broemsen E, Christner B. 2012. General Characteristics of Cold-Adapted Microorganisms, p 103-125. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

(A) Bulk percentage estimates of unfrozen water in various icy substrates. The inclusion of 1 M NaCl is for comparison. (B) Predicted ionic strength and a of the unfrozen water. (Water chemistry data: Seawater, ; Antarctic Permafrost, ; Antarctic Glacial Ice, S. Montross [unpublished data]. Calculations were performed on dissolved major ions using FREZCHEM [v. 11.2; ].)

Citation: Doyle S, Dieser M, Broemsen E, Christner B. 2012. General Characteristics of Cold-Adapted Microorganisms, p 103-125. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abyzov, S. S.,, I. N. Mitskevich,, and M. N. Poglazova. 1998. Microflora of the deep glacier horizons of central Antarctica. Microbiology 67:6673.
2. Aghajari, N.,, G. Feller,, C. Gerday,, and R. Haser. 1998. Structures of the psychrophilic Alteromonas haloplanctis α-amylase give insights into cold adaptation at a molecular level. Structure 6:15031516.
3. Amato, P.,, and B. C. Christner. 2009. Energy metabolism response to low-temperature and frozen conditions in Psychrobacter cryohalolentis. Appl. Environ. Microbiol. 75:711718.
4. Amato, P.,, S. M. Doyle,, J. R. Battista,, and B. C. Christner. 2010. Implications of subzero metabolic activity on long-term microbial survival in terrestrial and extraterrestrial permafrost. Astrobiology 10:789798.
5. Amato, P.,, S. M. Doyle,, and B. C. Christner. 2009. Macromolecular synthesis by yeasts under frozen conditions. Environ. Microbiol. 11:589596.
6. Amato, P.,, M. Parazols,, M. Sancelme,, P. Laj,, G. Mailhot,, and A. Delort. 2007. Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dôme: major groups and growth abilities at low temperatures. FEMS Microbiol. Ecol. 59:242254.
7. Appelo, C. A. J.,, and D. Postma. 2005. Geochemistry, Groundwater and Pollution, 2nd ed. A. A. Balkerma Publishers, Leiden, The Netherlands.
8. Arpigny, J. L.,, J. Lamotte,, and C. Gerday. 1997. Molecular adaptation to cold of an Antarctic bacterial lipase. J. Mol. Catal. B Enzym. 3:2935.
9. Ayala-del-Río, H. L.,, P. S. Chain,, J. J. Grzymski,, M. A. Ponder,, N. Ivanova,, P. W. Bergholz,, G. Di Bartolo,, L. Hauser,, M. Land,, C. Bakermans,, D. Rodrigues,, J. Klappenbach,, D. Zarka,, F. Larimer,, P. Richardson,, A. Murray,, M. Thomashow,, and J. M. Tiedje. 2010. The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Appl. Environ. Microbiol. 76:23042312.
10. Bakermans, C.,, S. L. Tollaksen,, C. S. Giometti,, C. Wilkerson,, J. M. Tiedje,, and M. F. Thomashow. 2007. Proteomic analysis of Psychrobacter cryohalolentis K5 during growth at subzero temperatures. Extremophiles 11:343354.
11. Bakermans, C.,, A. I. Tsapin,, V. Souza-Egipsy,, D. A. Gilichinsky,, and K. H. Nealson. 2003. Reproduction and metabolism at -10°C of bacteria isolated from Siberian permafrost. Environ. Microbiol. 5:321326.
12. Bentahir, M.,, G. Feller,, M. Aittaleb,, J. Lamotte-Brasseur,, T. Himri,, J.-P. Chessa,, and C. Gerday. 2000. Structural, kinetic, and calorimetric characterization of the cold-active phosphoglycerate kinase from the Antarctic Pseudomonas sp. TACII18. J. Biol. Chem. 275:1114711153.
13. Bidle, K. D.,, S. Lee,, D. R. Marchant,, and P. G. Falkowski. 2007. Fossil genes and microbes in the oldest ice on Earth. Proc. Natl. Acad. Sci. USA 104:1345513460.
14. Breezee, J.,, N. Cady,, and J. T. Staley. 2004. Subfreezing growth of the sea ice bacterium “Psychromonas ingrahamii.” Microb. Ecol. 47:300304.
15. Brinton, K. L. F.,, A. I. Tsapin,, D. A. Gilichinsky,, and G. D. McDonald. 2002. Aspartic acid racemization and age-depth relationships for organic carbon in Siberian permafrost. Astrobiology 2:7782.
16. Britton, G. 1995. Structure and properties of carotenoids in relation to function. FASEB J. 9:15511558.
17. Brooks, P. D.,, S. K. Schmidt,, and M. W. Williams. 1997. Winter production of CO2 and N2O from alpine tundra: environmental controls and relationship to inter-system C and N fluxes. Oecologia 110:403413.
18. Campen, R. K.,, T. Sowers,, and R. B. Alley. 2003. Evidence of microbial consortia metabolizing within a low-latitude mountain glacier. Geology 31:231234.
19. Carpenter, E. J.,, S. Lin,, and D. G. Capone. 2000. Bacterial activity in South Pole snow. Appl. Environ. Microbiol. 66:45144517.
20. Chaikam, V.,, and D. T. Karlson. 2010. Comparison of structure, function and regulation of plant cold shock domain proteins to bacterial and animal cold shock domain proteins. BMB Rep. 43:18.
21. Chattopadhyay, M. K.,, M. V. Jagannadham,, M. Vairamani,, and S. Shivaji. 1997. Carotenoid pigments of an Antarctic psychrotrophic bacterium Micrococcus roseus: temperature dependent biosynthesis, structure, and interaction with synthetic membranes. Biochem. Biophys. Res. Commun. 239:8590.
22. Christner, B. C. 2002. Incorporation of DNA and protein precursors into macromolecules by bacteria at -15°C. Appl. Environ. Microbiol. 68:64356438.
23. Christner, B. C. 2010. Bioprospecting for microbial products that affect ice crystal formation and growth. Appl. Microbiol. Biotechnol. 85:481489.
24. Christner, B. C.,, E. Mosley-Thompson,, L. G. Thompson,, and J. N. Reeve. 2001. Isolation of bacteria and 16S rDNAs from Lake Vostok accretion ice. Environ. Microbiol. 3:570577.
25. Christner, B. C.,, E. Mosley-Thompson,, L. G. Thompson,, V. Zagorodnov,, K. Sandman,, and J. N. Reeve. 2000. Recovery and identification of viable bacteria immured in glacial ice. Icarus 144:479485.
26. Christner, B. C.,, E. Mosley-Thompson,, L. G. Thompson,, and J. N. Reeve. 2003. Bacterial recovery from ancient ice. Environ. Microbiol. 5:433436.
27. Christner, B. C.,, G. Royston-Bishop,, C. F. Foreman,, B. R. Arnold,, M. Tranter,, K. A. Welch,, W. B. Lyons,, A. I. Tsapin,, M. Studinger,, and J. C. Priscu. 2006. Limnological conditions in Subglacial Lake Vostok, Antarctica. Limnol. Oceanogr. 51:24852501.
28. Collins, T.,, C. Gerday,, and G. Feller. 2005. Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol. Rev. 29:323.
29. Cybulski, L. E.,, G. Solar,, P. O. Craig,, M. Espinosa,, and D. Mendoza. 2004. Bacillus subtilis DesR functions as a phosphorylation-activated switch to control membrane lipid fluidity. J. Biol. Chem. 279:3934039347.
30. Dalluge, J. J.,, T. Hamamoto,, K. Horikoshi,, R. Y. Morita,, K. O. Stetter,, and J. A. McCloskey. 1997. Posttranscriptional modification of tRNA in psychrophilic bacteria. J. Bacteriol. 179:19181923.
31. Dalluge, J. J.,, T. Hashizume,, A. E. Sopchik,, J. A. McCloskey,, and D. R. Davis. 1996. Conformational flexibility in RNA: the role of dihydrouridine. Nucl. Acids Res. 24:10731079.
32. D'Amico, S.,, T. Collins,, J.-C. Marx,, G. Feller,, and C. Gerday. 2006. Psychrophilic microorganisms: challenges for life. EMBO Rep. 7:385389.
33. D'Amico, S.,, C. Gerday,, and G. Feller. 2001. Structural determinants of cold adaptation and stability in a large protein. J. Biol. Chem. 276:2579125796.
34. DeVries, A. L.,, and D. E. Wohlschlag. 1969. Freezing resistance in some Antarctic fishes. Science 163:10731075.
35. Dieser, M.,, M. Greenwood,, and C. M. Foreman. 2010. Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arct. Antarct. Alp. Res. 42:396405.
36. Dumon, C.,, A. Varvak,, M. A. Wall,, J. E. Flint,, R. J. Lewis,, J. H. Lakey,, C. Morland,, P. Luginbühl,, S. Healey,, T. Todaro,, G. DeSantis,, M. Sun,, L. Parra-Gessert,, X. Tan,, D. P. Weiner,, and H. J. Gilbert. 2008. Engineering hyperthermostability into a GH11 xylanase is mediated by subtle changes to protein structure. J. Biol. Chem. 283:2255722564.
37. Duplantis, B.,, M. Osusky,, C. L. Schmerk,, D. R. Ross,, C. M. Bosio,, and F. E. Nano. 2010. Essential genes from Arctic bacteria used to construct stable, temperature-sensitive bacterial vaccines. Proc. Natl. Acad. Sci. USA 107:1345613460.
38. Edmonds, C. G.,, P. F. Crain,, R. Gupta,, T. Hashizume,, C. H. Hocart,, J. A. Kowalak,, S. C. Pomerantz,, K. O. Stetter,, and J. A. McCloskey. 1991. Posttranscriptional modification of tRNA in thermophilic archaea (archaebacteria). J. Bacteriol. 173:31383148.
39. Empadinhas, N.,, and M. S. da Costa. 2009. Diversity, distribution and biosynthesis of compatible solutes in prokaryotes. Contrib. Sci. 5:95109.
40. Fedøy, A.,, N. Yang,, A. Martinez,, H. S. Leiros,, and I. H. Steen. 2007. Structural and functional properties of isocitrate dehydrogenase from the psychrophilic bacterium Desulfotalea psychrophila reveal a cold-active enzyme with an unusual high thermal stability. J. Mol. Biol. 372:130149.
41. Feller, G.,, and C. Gerday. 2003. Psychrophilic enzymes: hot topics in cold adaptation. Nat. Rev. Microbiol. 1:200208.
42. Feller, G.,, T. Lonhienne,, C. Deroanne,, C. Libioulle,, J. Van Beeumen,, and C. Gerday. 1992. Purification, characterization, and nucleotide sequence of the thermolabile α-amylase from the Antarctic psychrotroph Alteromonas haloplanctis A23. J. Biol. Chem. 267:52175221.
43. Feller, G.,, P. Sonnet,, and C. Gerday. 1995. The β-lactamase secreted by the Antarctic psychrophile Psychrobacter immobilis A8. Appl. Environ. Microbiol. 61:44744476.
44. Fong, N. J. C.,, M. L. Burgess,, K. D. Barrow,, and D. R. Glenn. 2001. Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress. Appl. Microbiol. Biotechnol. 56:750756.
45. Gabriel, J. L.,, and P. K. L. Chong. 2000. Molecular modeling of archaebacterial bipolar tetraether lipid membranes. Chem. Phys. Lipids 105:193200.
46. Garnham, C. P.,, J. A. Gilbert,, C. P. Hartman,, R. L. Campbell,, J. Laybourn-Parry,, and P. L. Davies. 2008. A Ca2+ dependent bacterial antifreeze protein domain has a novel β-helical ice-binding fold. Biochem. J. 411:171180.
47. Georlette, D.,, V. Blaise,, T. Collins,, S. D'Amico,, E. Gratia,, A. Hoyoux,, J. C. Marx,, G. Sonan,, G. Feller,, and C. Gerday. 2004. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol. Rev. 28:2542.
48. Georlette, D.,, B. Damien,, V. Blaise,, E. Depiereux,, V. N. Uversky,, C. Gerday,, and G. Feller. 2003. Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic, and thermophilic DNA ligases. J. Biol. Chem. 278:3701537023.
49. Georlette, D.,, Z. O. Jónsson,, F. Van Petegem,, J. Chessa,, J. Van Beeumen,, U. Hübscher,, and C. Gerday. 2000. A DNA ligase from the psychrophile Pseudoalteromonas haloplanktis gives insights into the adaptation of proteins to low temperatures. Eur. J. Biochem. 267:35023512.
50. Giaquinto, L.,, P. M. G. Curmi,, K. S. Siddiqui,, A. Poljak,, E. DeLong,, S. DasSarma,, and R. Cavicchioli. 2007. Structure and function of cold shock proteins in archaea. J. Bacteriol. 189:57385748.
51. Gibson, J. A. E.,, M. R. Miller,, N. W. Davies,, G. P. Neill,, D. S. Nichols,, and J. K. Volkman. 2005. Unsaturated diether lipids in the psychrotrophic archaeon Halorubrum lacusprofundi. Syst. Appl. Microbiol. 28:1926.
52. Gilbert, J. A.,, P. L. Davies,, and J. Laybourn-Parry. 2005. A hyperactive, Ca2+-dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol. Lett. 245:6772.
53. Gilbert, J. A.,, P. J. Hill,, C. E. R. Dodd,, and J. Laybourn-Parry. 2004. Demonstration of antifreeze protein activity in Antarctic lake bacteria. Microbiology 150:171180.
54. Gilichinsky, D.,, E. Rivkina,, V. Shcherbakova,, K. Laurinavichuis,, and J. Tiedje. 2003. Supercooled water brines within permafrost—an unknown ecological niche for microorganisms: a model for astrobiology. Astrobiology 3:331341.
55. Giuliodori, A. M.,, F. Di Pietro,, S. Marzi,, B. Masquida,, R. Wagner,, P. Romby,, C. O. Gualerzi,, and C. L. Pon. 2010. The cspA mRNA is a thermosensor that modulates translation of the cold-shock protein CspA. Mol. Cell 37:2133.
56. Goldstein, J.,, N. S. Pollitt,, and M. Inouye. 1990. Major cold shock protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 87:283287.
57. Goodchild, A.,, M. Raftery,, N. F. W. Saunders,, M. Guilhaus,, and R. Cavicchioli. 2005. Cold adaptation of the Antarctic archaeon, Methanococcoides burtonii assessed by proteomics using ICAT. J. Proteome Res. 4:473480.
58. Graumann, P. L.,, and M. A. Marahiel. 1998. A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23:286290.
59. Grossmann, S. 1994. Bacterial activity in sea ice and open water of the Weddell Sea, Antarctica: a microautoradiographic study. Microb. Ecol. 28:118.
60. Gualerzi, C. O.,, A. M. Giuliodori,, and C. L. Pon. 2003. Transcriptional and post-transcriptional control of cold-shock genes. J. Mol. Biol. 331:527539.
61. Hansen, A. J.,, D. L. Mitchell,, C. Wiuf,, L. Paniker,, T. B. Brand,, J. Binladen,, D. A. Gilichinsky,, R. Rønn,, and E. Willerslev. 2006. Crosslinks rather than strand breaks determine access to ancient DNA sequences from frozen sediments. Genetics 173:11751179.
62. Hébraud, M.,, and P. Potier. 1999. Cold shock response and low temperature adaptation in psychrotrophic bacteria. J. Mol. Microbiol. Biotechnol. 1:211219.
63. Hirano, S. S.,, and C. D. Upper,. 1995. Ecology of ice nucleation-active bacteria, p. 4161. In R. E. Lee Jr.,, G. J. Warren,, and L. V. Gusta (ed.), Biological Ice Nucleation and Its Applications. APS Press, St. Paul, MN.
64. Hochachka, P.W.,, and G. N. Somero. 2002. Temperature, p. 290449. In Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, New York, NY.
65. Hoshino, T.,, M. Kiriaki,, S. Ohgiya,, M. Fujiwara,, H. Kondo,, Y. Nishimiya,, I. Yumoto,, and S. Tsuda. 2003. Antifreeze proteins from snow mold fungi. C. J. Bot. 81:11751181.
66. Hoyoux, A.,, I. Jennes,, P. Dubois,, S. Genicot,, F. Dubail,, J. M. François,, E. Baise,, G. Feller,, and C. Gerday. 2001. Cold-Adapted β-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis. Appl. Environ. Microbiol. 67:15291535.
67. Huston, A. L.,, B. Methe,, and J. W. Deming. 2004. Purification, characterization, and sequencing of an extracellular cold-active aminopeptidase produced by marine psychrophile Colwellia psychrerythraea strain 34H. Appl. Environ. Microbiol. 70:33213328.
68. Jagannadham, M. V.,, M. K. Chattopadhyay,, C. Subbalakshmi,, M. Vairamani,, K. Narayanan,, C. M. Rao,, and S. Shivaji. 2000. Carotenoids of an Antarctic psychrotolerant bacterium, Sphingobacterium antarcticus, and a mesophilic bacterium, Sphingobacterium multivorum. Arch. Microbiol. 173:418424.
69. Jakosky, B. M.,, K. H. Nealson,, C. Bakermans,, R. E. Ley,, and M. T. Mellon. 2003. Subfreezing activity of microorganisms and the potential habitability of Mars’ polar region. Astrobiology 3:343350.
70. Janech, M. G.,, A. Krell,, T. Mock,, J. S. Kang,, and J. A. Raymond. 2006. Ice-binding proteins from sea ice diatoms (Bacillariophyceae). J. Phycol. 42:410416.
71. Johnson, S. S.,, M. B. Hebsgaard,, T. R. Christensen,, M. Mastepanov,, R. Nielsen,, K. Munch,, T. Brand,, M. T. P. Gilbert,, M. T. Zuber,, M. Bunce,, R. Rønn,, D. Gilichinsky,, D. Froese,, and E. Willerslev. 2007. Ancient bacteria show evidence of DNA repair. Proc. Natl. Acad. Sci. USA 104:1440114405.
72. Junge, K.,, B. C. Christner,, and J. T. Staley,. 2011. Diversity of psychrophilic bacteria from sea ice—and glacial ice communities, p. 794815. In K. Horikoshi,, G. Antranikian,, A. T. Bull,, F. T. Robb,, and K. O. Stetter (ed.), Extremophiles Handbook. Springer, Berlin, Germany.
73. Junge, K.,, H. Eicken,, and J. W. Deming. 2003. Motility of Colwellia psychrerythraea strain 34H at subzero temperatures. Appl. Environ. Microbiol. 69:42824284.
74. Junge, K.,, H. Eicken,, and J. W. Deming. 2004. Bacterial activity at -2 to -20°C in Arctic wintertime sea ice. Appl. Environ. Microbiol. 70:550557.
75. Junge, K.,, H. Eicken,, B. D. Swanson,, and J. W. Deming. 2006. Bacterial incorporation of leucine into protein down to -20°C with evidence for potential activity in sub-eutectic saline ice formations. Cryobiology 52:417429.
76. Kawahara, H.,, Y. Iwanaka,, S. Higa,, N. Muryoi,, M. Sato,, M. Honda,, H. Omura,, and H. Obata. 2007. A novel, intracellular antifreeze protein in an Antarctic bacterium, Flavobacterium xanthum. Cryo Lett. 28:3949.
77. Kawamoto, J.,, T. Kurihara,, M. Kitagawa,, I. Kato,, and N. Esaki. 2007. Proteomic studies of an Antarctic cold-adapted bacterium, Shewanella livingstonensis Ac10, for global identification of cold-inducible proteins. Extremophiles 11:819826.
78. Kempf, B.,, and E. Bremer. 1998. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolarity environments. Arch. Microbiol. 170:319330.
79. Kim, S. Y.,, K. Y. Hwang,, S. H. Kim,, H. C. Sung,, Y. S. Han,, and Y. Cho. 1999. Structural basis for cold adaptation. Sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium arcticum. J. Biol. Chem. 274:1176111767.
80. Knoblauch, C.,, B. B. Jørgensen,, and J. Harder. 1999. Community size and metabolic rates of psychrophilic sulfate-reducing bacteria in Arctic marine sediments. Appl. Environ. Microbiol. 65:42304233.
81. Ko, R.,, L. T. Smith,, and G. M. Smith. 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J. Bacteriol. 176:426431.
82. Koshland, D. E., Jr. 2002. The application and usefulness of the ratio kcat/KM. Bioorg. Chem. 30:211213.
83. Krembs, C.,, H. Eicken,, K. Junge,, and J. W. Deming. 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. Part 1 Oceanogr. Res. Pap. 49:21632181.
84. Lettinga, G.,, S. Rebac,, and G. Zeeman. 2001. Challenge of psychrophilic anaerobic wastewater treatment. Trends Biotechnol. 19:363370.
85. Li, Y.,, F. Li,, X. Zhang,, S. Qin,, Z. Zeng,, H. Dang,, and Y. Qin. 2008. Vertical distribution of bacterial and archaeal communities along discrete layers of a deep-sea cold sediment sample at the East Pacific Rise (~13°N). Extremophiles 12:573585.
86. Liebner, S.,, K. Rublack,, T. Stuehrmann,, and D. Wagner. 2009. Diversity of aerobic methanotrophic bacteria in a permafrost active layer soil of the Lena Delta, Siberia. Microb. Ecol. 57:2535.
87. Lim, J.,, T. Thomas,, and R. Cavicchioli. 2000. Low temperature regulated DEAD-box RNA helicase from the Antarctic archaeon, Methanococcoides burtonii. J. Mol. Biol. 297:553567.
88. Lipson, D. A.,, C. W. Schadt,, and S. K. Schmidt. 2002. Changes in microbial community structure and function in an alpine dry meadow following spring snow melt. Microb. Ecol. 43:307314.
89. Los, D. A.,, and N. Murata. 2004. Membrane fluidity and its role in the perceptions of environmental signals. Biochim. Biophys. Acta 1666:142147.
90. Lundheim, R. 2002. Physiological and ecological significance of biological ice nucleators. Philos. Trans. R. Soc. Lond. B 357:937943.
91. Mader, H. M.,, M. E. Pettitt,, J. L. Wadham,, E. W. Wolff,, and R. J. Parkes. 2006. Subsurface ice as a microbial habitat. Geology 34:169172.
92. Mancuso Nichols, C. A.,, J. Guezenec,, and J. P. Bowman. 2005. Bacterial exopolysaccharides from extreme marine environments with special consideration of the Southern Ocean, sea ice, and deep-sea hydrothermal vents: a review. Mar. Biotechnol. 7:253271.
93. Mandelman, D.,, M. Bentahir,, G. Feller,, C. Gerday,, and R. Haser. 2001. Crystallization and preliminary X-ray analysis of a bacterial psychrophilic enzyme, phosphoglycerate kinase. Acta Crystallogr. D Biol. Crystallogr. 57:16661668.
94. McLeod, M.,, J. G. Bockheim,, and M. R. Balks. 2008. Glacial geomorphology, soil development and permafrost features in central-upper Wright Valley, Antarctica. Geoderma 144:93103.
95. Metpally, R. P. R.,, and B. V. B. Reddy. 2009. Comparative proteome analysis of psychrophilic versus mesophilic bacterial species: insights into the molecular basis of cold adaptation of proteins. BMC Genomics 10:11.
96. Mikan, C. J.,, J. P. Schimel,, and A. P. Doyle. 2002. Temperature controls of microbial respiration in Arctic tundra soils above and below freezing. Soil Biol. Biochem. 34:17851795.
97. Mironenko, M. V.,, S. A. Grant,, G. M. Marion,, and R. E. Farren. 1997. FREZCHEM2: a chemical thermodynamic model for electrolyte solutions at subzero temperatures. CRREL Spec. Rept. 97-5. USACRREL, Hanover, NH.
98. Miteva, V.,, T. Sowers,, and J. Brenchley. 2007. Production of N2O by ammonia oxidizing bacteria at subfreezing temperatures as a model for assessing the N2O anomalies in the Vostok ice core. Geomicrobiol. J. 24:451459.
99. Moissl, C.,, C. Rudolph,, R. Rachel,, M. Koch,, and R. Huber. 2003. In situ growth of the novel SM1 euryarchaeon from a string-of pearls-like microbial community in its cold biotope, its physical separation and insights into its structure and physiology. Arch. Microbiol. 180:211217.
100. Morita, R. Y. 1988. Bioavailability of energy and its relationship to growth and starvation survival in nature. Can. J. Microbiol. 34:436441.
101. Muryoi, N.,, M. Sato,, S. Kaneko,, H. Kawahara,, H. Obata,, M. W. Yaish,, M. Griffith,, and B. R. Glick. 2004. Cloning and expression of afpA, a gene encoding an antifreeze protein from the Arctic plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. J. Bacteriol. 186:56615671.
102. Nahvi, A.,, N. Sudarsan,, M. S. Ebert,, X. Zou,, K. L. Brown,, and R. R. Breaker. 2002. Genetic control by a metabolite binding mRNA. Chem. Biol. 9:10431049.
103. Napolitano, M. J.,, and D. H. Shain. 2005. Distinctions in adenylate metabolism among organisms inhabiting temperature extremes. Extremophiles 9:9398.
104. Narberhaus, F.,, T. Waldminghaus,, and S. Chowdhury. 2006. RNA thermometers. FEMS Microbiol. Rev. 30:316.
105. Narinx, E.,, E. Baise,, and C. Gerday. 1997. Subtilisin from psychrophilic Antarctic bacteria: characterization and site-directed mutagenesis of residues possibly involved in the adaptation to cold. Protein Eng. 10:12711279.
106. Nichols, D. S.,, M. R. Miller,, N. W. Davies,, A. Goodchild,, M. Raftery,, and R. Cavicchioli. 2004. Cold adaptation in the Antarctic archaeon Methanococcoides burtonii involves membrane lipid unsaturation. J. Bacteriol. 186:85088515.
107. Noon, K. R.,, R. Guymon,, P. F. Crain,, J. A. McCloskey,, M. Thomm,, J. Lim,, and R. Cavicchioli. 2003. Influence of temperature on tRNA modification in archaea: Methanococcoides burtonii (optimum growth temperature [Topt], 23°C) and Stetteria hydrogenophila (Topt, 95°C). J. Bacteriol. 185:54835490.
108. Panikov, N. S., 2009. Microbial activity in frozen soils. p. 119147. In R. Margesin (ed.), Permafrost Soils. Springer, Berlin, Germany.
109. Panikov, N. S.,, P. W. Flanagan,, W. C. Oechel,, M. A. Mastepanov,, and T. R. Christensen. 2006. Microbial activity in soils frozen to below -39°C. Soil Biol. Biochem. 38:785794.
110. Panikov, N. S.,, and M. V. Sizova. 2007. Growth kinetics of microorganisms isolated from Alaskan soil and permafrost in solid media frozen down to 35°C. FEMS Microbiol. Ecol. 59:500512.
111. Panoff, J. M.,, D. Corroler,, B. Thammavongs,, and P. Boutibonnes. 1997. Differentiation between cold shock proteins and cold acclimation proteins in a mesophilic gram-positive bacterium, Enterococcus faecalis JH2-2. J. Bacteriol. 179:44514454.
112. Paul, S.,, S. K. Bag,, S. Das,, E. T. Harvill,, and C. Dutta. 2008. Molecular signature of hypersaline adaptation: insights from genome and proteome composition of halophilic prokaryotes. Genome Biol. 9:R70.
113. Pearson, R. T.,, and W. Derbyshire. 1974. NMR studies of water adsorbed on a number of silica surfaces. J. Colloid Interface Sci. 46:232248.
114. Phadtare, S.,, and M. Inouye,. 2008. Cold-shock proteins, p. 191209. In R. Margesin,, F. Schinner,, J.-C. Marx,, and C. Gerday (ed.), Psychrophiles: from Biodiversity to Biotechnology. Springer, Berlin, Germany.
115. Piette, F.,, S. D'Amico,, C. Struvay,, G. Mazzucchelli,, J. Renaut,, M. L. Tutino,, A. Danchin,, P. Leprince,, and G. Feller. 2010. Proteomics of life at low temperatures: trigger factor is the primary chaperone in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Mol. Microbiol. 76:120132.
116. Poolman, B.,, and E. Glaasker. 1998. Regulation of compatible solute accumulation in bacteria. Mol. Microbiol. 29:397407.
117. Price, P. B. 2000. A habitat for psychrophiles in deep Antarctic ice. Proc. Natl. Acad. Sci. USA 97:12471251.
118. Price, P. B.,, and T. Sowers. 2004. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Natl. Acad. Sci. USA 101:46314636.
119. Priscu, J. C.,, C. H. Fritsen,, E. E. Adams,, S. J. Giovannoni,, H. W. Paerl,, C. P. McKay,, P. T. Doran,, D. A. Gordon,, B. D. Lanoil,, and J. L. Pinckney. 1998. Perennial Antarctic lake ice: an oasis for life in a polar desert. Science 280:20952098.
120. Qin, G.,, L. Zhu,, X. Chen,, P. G. Wang,, and Y. Zhang. 2007. Structural characterization and ecological roles of a novel exopolysaccharide from the deep-sea psychrotolerant bacterium Pseudoalteromonas sp. SM9913. Microbiology 153:15661572.
121. Ræder, I. L. U.,, I. Leiros,, N. P. Willassen,, A. O. Smalas,, and E. Moe. 2008. Uracil-DNA N-glycosylase (UNG) from the marine pyschrophilic bacterium Vibrio salmonicida shows cold adapted features: a comparative analysis to Vibrio cholerae uracil-DNA N-glycosylase. Enzyme Microb. Technol. 42:594600.
122. Raymond, J. A.,, B. C. Christner,, and S. C. Schuster. 2008. A bacterial ice-binding protein from the Vostok ice core. Extremophiles 12:713717.
123. Raymond, J. A.,, and C. H. Fritsen. 2001. Semipurification and ice recrystallization inhibition activity of ice-active substances associated with Antarctic photosynthetic organisms. Cryobiology 43:6370.
124. Raymond, J. A.,, C. Fritsen,, and K. Shen. 2007. An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol. Ecol. 61:214221.
125. Reid, I. N.,, W. B. Sparks,, S. Lubow,, M. McGrath,, M. Livio,, J. Valenti,, K. R. Sowers,, H. D. Shukla,, S. MacAuley,, T. Miller,, R. Suvanasuthi,, R. Belas,, A. Colman,, F. T. Robb,, P. DasSarma,, J. A. Müller,, J. A. Coker,, R. Cavicchioli,, F. Chen,, and S. DasSarma. 2006. Terrestrial models for extraterrestrial life: methanogens and halophiles at Martian temperatures. Int. J. Astrobiol. 5:8997.
126. Ritzrau, W. 1997. Pelagic microbial activity in the Northeast Water Polynya, summer 1992. Polar Biol. 17:259267.
127. Rivkina, E. M.,, E. I. Friedmann,, C. P. McKay,, and D. A. Gilichinsky. 2000. Metabolic activity of permafrost bacteria below the freezing point. Appl. Environ. Microbiol. 66:32303233.
128. Rivkina, E.,, K. Laurinavichius,, J. McGrath,, J. Tiedje,, V. Shcherbakova,, and D. Gilichinsky. 2004. Microbial life in permafrost. Adv. Space Res. 33:12151221.
129. Roberts, M. F. 2005. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Systems 1:5.
130. Rodionov, D. A.,, A. G. Vitreschak,, A. A. Mironov,, and M. S. Gelfand. 2003. Regulation of lysine biosynthesis and transport genes in bacteria: yet another RNA riboswitch? Nucl. Acids Res. 31:316.
131. Russell, N. J., 2008. Membrane components and cold sensing, p. 177190. In R. Margesin,, F. Schinner,, J.-C. Marx,, and C. Gerday (ed.), Psychrophiles: from Biodiversity to Biotechnology. Springer, Berlin, Germany.
132. Russell, R. J. M.,, U. Gerike,, M. J. Danson,, D. W. Hough,, and G. L. Taylor. 1998. Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6:351361.
133. Sand-Jensen, K.,, N. L. Pedersen,, and M. Søndergaard. 2007. Bacterial metabolism in small temperate streams under contemporary and future climates. Freshw. Biol. 52:23402353.
134. Saunders, N. F. W.,, T. Thomas,, P. M. G. Curmi,, J. S. Mattick,, E. Kuczek,, R. Slade,, J. Davis,, P. D. Franzmann,, D. Boone,, K. Rusterholtz,, R. Feldman,, C. Gates,, S. Bench,, K. Sowers,, K. Kadner,, A. Aerts,, P. Dehal,, C. Detter,, T. Glavina,, S. Lucas,, P. Richardson,, F. Larimer,, L. Hauser,, M. Land,, and R. Cavicchioli. 2003. Mechanisms of thermal adaptation revealed from the genomes of the Antarctic archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res. 13:15801588.
135. Schimel, J. P.,, C. Bilbrough,, and J. M. Welker. 2004. Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol. Biochem. 36:217227.
136. Schleper, C.,, R. V. Swanson,, E. J. Mathur,, and E. F. DeLong. 1997. Characterization of a DNA polymerase from the uncultivated psychrophilic archaeon Cenarchaeum symbiosum. J. Bacteriol. 179:78037811.
137. Schouten, S.,, E. C. Hopmans,, E. Schefuss,, and J. S. Sinninghe Damsté. 2002. Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Earth Planet. Sci. Lett. 204:265274.
138. Shivaji, S.,, and J. S. S. Prakash. 2010. How do bacteria sense and respond to low temperature? Arch. Microbiol. 192:8595.
139. Siddiqui, K. S.,, R. Cavicchioli,, and T. Thomas. 2002. Thermodynamic activation properties of elongation factor 2 (EF-2) proteins from psychrotolerant and thermophilic Archaea. Extremophiles 6:143150.
140. Sinensky, M. 1974. Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. USA 71:522525.
141. Sinninghe Damsté, J. S.,, S. Schouten,, E. C. Hopmans,, A. C. T. van Duin,, and J. A. J. Geenevasen. 2002. Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J. Lipid Res. 43:16411651.
142. Smith, J. J.,, L. A. Tow,, W. Stafford,, C. Cary,, and D. Cowan. 2006. Bacterial diversity in three different Antarctic cold desert mineral soils. Microb. Ecol. 51:413421.
143. Smith, R. E. H.,, and P. Clement. 1990. Heterotrophic activity and bacterial productivity in assemblages of microbes from sea ice in the high Arctic. Polar Biol. 10:351357.
144. Sowers, T. 2001. The N2O record spanning the penultimate deglaciation from the Vostok ice core. J. Geophys. Res. 106:903931.
145. Steven, B.,, R. Leveille,, W. H. Pollard,, and L. G. Whyte. 2006. Microbial ecology and biodiversity in permafrost. Extremophiles 10:259267.
146. Steven, B.,, W. H. Pollard,, C. W. Greer,, and L. G. Whyte. 2007. Microbial diversity and activity through a permafrost/ground ice core profile from the Canadian high Arctic. Environ. Microbiol. 10:33883403.
147. Strand, A.,, S. Shivaji,, and S. Liaaen-Jensen. 1997. Bacterial carotenoids 55. C50-carotenoids 25. Revised structures of carotenoids associated with membranes in psychrotrophic Micrococcus roseus. Biochem. Syst. Ecol. 25:547552.
148. Takacs, C. T.,, and J. C. Priscu. 1998. Bacterioplankton dynamics in the McMurdo Dry Valley lakes: production and biomass loss over four seasons. Microb. Ecol. 36:239250.
149. Thomas, T.,, and R. Cavicchioli. 1998. Archaeal cold-adapted proteins: structural and evolutionary analysis of the elongation factor 2 proteins from psychrophilic, mesophilic and thermophilic methanogens. FEBS Lett. 439:281286.
150. Thomas, T.,, and R. Cavicchioli. 2000. Effect of temperature on stability and activity of elongation factor 2 proteins from Antarctic and thermophilic methanogens. J. Bacteriol. 182:13281332.
151. Thomas, T.,, and R. Cavicchioli. 2002. Cold adaptation of archaeal elongation factor 2 (EF-2) proteins. Curr. Prot. Pept. Sci. 3:223230.
152. Thomas, T.,, N. Kumar,, and R. Cavicchioli. 2001. Effects of ribosomes and intracellular solutes on activities and stabilities of elongation factor 2 proteins from psychrotolerant and thermophilic methanogens. J. Bacteriol. 183:19741982.
153. Tung, H. C.,, P. B. Price,, N. E. Bramall,, and G. Vrdoljak. 2006. Microorganisms metabolizing on clay grains in 3-km-deep Greenland basal ice. Astrobiology 6:6986.
154. Vitreschak, A. G.,, D. A. Rodionov,, A. A. Mironov,, and M. S. Gelfand. 2004. Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet. 20:4450.
155. Walker, V. K.,, G. R. Palmer,, and G. Voordouw. 2006. Freeze-thaw tolerance and clues to winter survival of a soil community. Appl. Environ. Microbiol. 72:17841792.
156. Wallon, G.,, S. T. Lovett,, C. Magyar,, A. Svingor,, A. Szilagyi,, P. Zàvodszky,, D. Ringe,, and G. A. Petsko. 1997. Sequence and homology model of 3-isopropylmalate dehydrogenase from the psychrotrophic bacterium Vibrio sp. I5 suggest reasons for thermal instability. Protein Eng. 10:665672.
157. Watanabe, S.,, Y. Yasutake,, I. Tanaka,, and Y. Takada. 2005. Elucidation of stability determinants of cold-adapted monomeric isocitrate dehydrogenase from a psychrophilic bacterium, Colwellia maris, by construction of chimeric enzymes. Microbiology 151:10831094.
158. Williams, T. J.,, D. W. Burg,, M. J. Raftery,, A. Poljak,, M. Guilhaus,, O. Pilak,, and R. Cavicchioli. 2010. Global proteomic analysis of the insoluble, soluble, and supernatant fractions of the psychrophilic archaeon Methanococcoides burtonii. Part I: The effect of growth temperature. J. Proteome Res. 9:640652.
159. Wood, J. M.,, E. Bremer,, L. N. Csonka,, R. Kraemer,, B. Poolman,, T. van der Heide,, and L. T. Smith. 2001. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130:437460.
160. Yamashita, Y. N. Nakamura,, K. Omiya,, J. Nishikawa,, H. Kawahara,, H. Obata. 2002. Identification of an antifreeze lipoprotein from Moraxella sp. of Antarctic origin. Biosci. Biotechnol. Biochem 66:239247.


Generic image for table

Examples of molecular adaptations in genes, proteins, and enzymes documented in psychrophilic prokaryotes

Citation: Doyle S, Dieser M, Broemsen E, Christner B. 2012. General Characteristics of Cold-Adapted Microorganisms, p 103-125. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch5
Generic image for table

Reports documenting evidence for subzero metabolic activity

CF-IRMS, continuous flow isotope ratio monitoring mass spectrometry; CTC, 5-cyano-2,3-ditolyl tetrazolium chloride.

Citation: Doyle S, Dieser M, Broemsen E, Christner B. 2012. General Characteristics of Cold-Adapted Microorganisms, p 103-125. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch5

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error