Skip to main content
SpringerLink
Log in

Genomic Insights into Cold Adaptation of Permafrost Bacteria

  • Chapter
Permafrost Soils

Part of the book series: Soil Biology ((SOILBIOL,volume 16))

Genomic analysis of the permafrost isolate Psychrobacter arcticus 273-4 has revealed that a variety of adaptations are employed to enable active growth at subzero temperatures. Many of these low-temperature adaptations are largely similar to adaptations found in other psychrophilic microorganisms isolated from other low-temperature environments and include: changes in amino acid abundance that favor protein mobility; RNA and protein chaperones; and desaturation of membrane lipids. Unlike other psychrophiles, P. arcticus 273-4 constitutively expressed the major cold shock protein (cspA, an RNA chaperone); employed several pairs of isozymes (homologous enzymes with different temperature optima); regulated cell wall elasticity as temperatures decreased; and utilized resources efficiently. These unique low-temperature adaptations may be advantageous in permafrost, where subzero temperatures reign.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Auman AJ, Breezee JL, Gosink JJ, Kampfer P, Staley JT (2006) Psychromonas ingrahamii sp. nov., a novel gas vacuolate, psychrophilic bacterium isolated from Arctic polar sea ice. Int J Syst Evol Microbiol 56:1001–1007

    Article  PubMed  CAS  Google Scholar 

  • Bakermans C, Nealson KH (2004) Relationship of critical temperature to macromolecular synthesis and growth yield in “Psychrobacter cryopegella.” J Bacteriol 186:2340–2345

    Article  PubMed  CAS  Google Scholar 

  • Bakermans C, Tsapin AI, Souza-Egipsy V, Gilichinsky DA, Nealson KH (2003) Reproduction and metabolism at −10°C of bacteria isolated from Siberian permafrost. Environ Microbiol 5:321–326

    Article  PubMed  Google Scholar 

  • Bakermans C, Ayala-del-Río HL, Ponder MA, Vishnivetskaya T, Gilichinsky D, Thomashow MF, Tiedje JM (2006) Psychrobacter cryohalolentis sp. nov. and Psychrobacter arcticus sp. nov. isolated from Siberian permafrost. Int J Syst Evol Microbiol 56:1285–1291

    Article  PubMed  CAS  Google Scholar 

  • Bakermans C, Tollaksen SL, Giometti CS, Wilkerson C, Tiedje JM, Thomashow MF (2007) Proteomic analysis of Psychrobacter cryohalolentis K5 during growth at subzero temperatures. Extremophiles 11: 345–354

    Article  CAS  Google Scholar 

  • Bayles D, Tunick M, Foglia T, Miller A (2000) Cold shock and its effect on ribosomes and thermal tolerance in Listeria monocytogenes. Appl Environ Microbiol 66:4351–4355

    Article  PubMed  CAS  Google Scholar 

  • Beckering CL, Steil L, Weber MHW, Volker U, Marahiel MA (2002) Genomewide transcriptional analysis of the cold-shock response in Bacillus subtilis. J Bacteriol 184:6395–6402

    Article  PubMed  CAS  Google Scholar 

  • Bock C, Eicken H (2005) A magnetic resonance study of temperature-dependent microstructural evolution and self-diffusion of water in Arctic first-year sea ice. Ann Glaciol 40:179–184

    Article  Google Scholar 

  • Bowman J, Nichols D, McMeekin T (1997) Psychrobacter glacincola sp. nov, a halotolerant, psychrophilic bacterium isolated from Antarctic sea ice. Syst Appl Microbiol 20:209–215

    CAS  Google Scholar 

  • Budde I, Steil L, Scharf C, Volker U, Bremer E (2006) Adaptation of Bacillus subtilis to growth at low temperature: a combined transcriptomic and proteomic appraisal. Microbiology-SGM 152:831–853

    Article  CAS  Google Scholar 

  • Chamot D, Owttrim GW (2000) Regulation of cold-shock-induced RNA helicase gene expression in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 182:1251–1256

    Article  PubMed  CAS  Google Scholar 

  • Feller G (2007) Life at low temperatures: is disorder the driving force? Extremophiles 6:211–216

    Article  CAS  Google Scholar 

  • Feller G, Narinx E, Arpigny JL, Aittaleb M, Baise E, Genicot S, Gerday C. (1996) Enzymes from psychrophilic organisms. FEMS Microbiol Rev 18:189–202

    Article  CAS  Google Scholar 

  • Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM et al (1995) The minimal gene complement of Mycoplasma genitalium. Science 270:397–403

    Article  PubMed  CAS  Google Scholar 

  • Gao HC, Yang ZMK, Wu LY, Thompson DK, Zhou JZ (2006) Global transcriptome analysis of the cold-shock response of Shewanella oneidensis MR-1 and mutational analysis of its classical cold-shock proteins. J Bacteriol 188:4560–4569

    Article  PubMed  CAS  Google Scholar 

  • Gilichinsky D, Vorobyova EA, Erokhina LG, Fedorov-Davydov DG, Chaikovskaya NR (1992) Long-term preservation of microbial ecosystems in permafrost. Adv Space Res 12:255–263

    Article  PubMed  CAS  Google Scholar 

  • Gilichinsky D, Rivkina E, Shcherbakova V, Laurinavichuis K, Tiedje J (2003) Supercooled water brines within permafrost — an unknown ecological niche for microorganisms: a model for astrobiology. Astrobiology 3:331–341

    Article  PubMed  CAS  Google Scholar 

  • Gilichinsky D, Rivkina E, Bakermans C, Shcherbakova V, Petrovskaya L, Ozerskaya S, Ivanushkina N, Kochkina G, Laurinavichuis K, Pecheritsina S. et al (2005) Biodiversity of cryopegs in permafrost. FEMS Microbiol Ecol 53:117–128

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg D, Azar I, Oppenheim AB, Brandi A, Pon CL, Gualerzi CO (1997) Role of Escherichia coli cspA promoter sequences and adaptation of translational apparatus in the cold-shock response. Mol Gen Genet 256:282–290

    Article  PubMed  CAS  Google Scholar 

  • Goodchild A, Saunders NFW, Ertan H, Raftery M, Guilhaus M, Curmi PMG, Cavicchioli R (2004) A proteomic determination of cold adaptation in the Antarctic archaeon, Methanococcoides burtonii. Mol Microbiol 53:309–321

    Article  PubMed  CAS  Google Scholar 

  • Gosink J, Woese C, Staley J (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

    Article  PubMed  Google Scholar 

  • He HJ, Gordon R, Gow JA (2001) The effect of temperature on the fatty acids and isozymes of a psychrotrophic and two mesophilic species of Xenorhabdus, a bacterial symbiont of entomopathogenic nematodes. Can J Microbiol 47:382–391

    Article  PubMed  CAS  Google Scholar 

  • Iost I, Dreyfus M (2006) DEAD-box RNA helicases in Escherichia coli. Nucl Acids Res 34:4189–4197

    Article  PubMed  CAS  Google Scholar 

  • Ishii A, Ochiai T, Imagawa S, Fukunaga N, Sasaki S, Minowa O, Mizuno Y, Shiokawa H (1987) Isozymes of isocitrate dehydrogenase from an obligately psychrophilic bacterium, Vibrio sp strain Abe-1 — purification, and modulation of activities by growth-conditions. J Biochem 102:1489–1498

    PubMed  CAS  Google Scholar 

  • Jiang W, Hou Y, Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272:196–202

    Article  PubMed  CAS  Google Scholar 

  • Johnson S, Hebsgaard M, Christensen T, Mastepanov M, Nielsen R, Munch K, Brand T, Gilbert M, Zuber M, Bunce M et al (2007) Ancient bacteria show evidence of DNA repair. Proc Natl Acad Sci USA 104:14401–14405

    Article  PubMed  CAS  Google Scholar 

  • Lim J, Thomas T, Cavicchioli R (2000) Low temperature regulated DEAD-box RNA helicase from the antarctic archaeon, Methanococcoides burtonii1. J Mol Biol 297:553–567

    Article  PubMed  CAS  Google Scholar 

  • Maruyama A, Honda D, Yamamoto K, Kitamura K, Higashihara T (2000) Phylogenetic analysis of psychrophilic bacteria isolated from the Japan Trench, including a description of the deepsea species Psychrobacter pacificensis sp. nov. Int J Syst Evol Microbiol 50:835–846

    PubMed  CAS  Google Scholar 

  • Medigue C, Krin E, Pascal G, Barbe V, Bernsei A, Bertin PN, Cheung F, Cruveiller S, D’Amico S, Duilio A et al (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15:1325–1335

    Article  PubMed  CAS  Google Scholar 

  • Methe BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X, Moult J, Madupu R, Nelson WC, Dodson RJ et al (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci USA 102:10913–10918

    Article  PubMed  CAS  Google Scholar 

  • Ochiai T, Fukunaga N, Sasaki S (1979) Purification and some properties of two NADP + -specific isocitrate dehydrogenases from an obligately psychrophilic marine bacterium, Vibrio sp. strain Abe-1. J Biochem 86:377–384

    PubMed  CAS  Google Scholar 

  • Ochiai T, Fukunaga N, Sasaki S (1984) Two structurally different NADP-specific isocitrate dehydrogenases in an obligately psychrophilic bacterium, Vibrio sp strain Abe-1. J Gen Appl Microbiol 30:479–487

    Article  CAS  Google Scholar 

  • Phadtare S, Inouye M (2004) Genome-wide transcriptional analysis of the cold-shock response in wild-type and cold-sensitive, quadruple-csp-deletion strains of Escherichia coli. J Bacteriol 186:7007–7014

    Article  PubMed  CAS  Google Scholar 

  • Phadtare S, Inouye M, Severinov K (2002) The nucleic acid melting activity of Escherichia coli CspE is critical for transcription antitermination and cold acclimation of cells. J Biol Chem 277:7239–7245

    Article  PubMed  CAS  Google Scholar 

  • Ponder MA, Gilmour SJ, Bergholz PW, Mindock CA, Hollingsworth R, Thomashow MF, Tiedje JM (2005) Characterization of potential stress responses in ancient Siberian permafrost psychroactive bacteria. FEMS Microbiol Ecol 53:103–115

    Article  PubMed  CAS  Google Scholar 

  • Rabus R, Ruepp A, Frickey T, Rattei T, Fartmann B, Stark M, Bauer M, Zibat A, Lombardot T, Becker I et al (2004) The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol 6:887–902

    Article  PubMed  CAS  Google Scholar 

  • Read TD, Brunham RC, Shen C, Gill SR, Heidelberg JF, White O, Hickey EK, Peterson J, Utterback T, Berry K et al (2000) Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucl Acids Res 28:1397–1406

    Article  PubMed  CAS  Google Scholar 

  • Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA (2000) Metabolic activity of permafrost bacteria below the freezing point. Appl Environ Microbiol 66:3230–3233

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues D (2007) Ecology, physiology and metabolism of cold-adapted microorganisms from the Siberian permafrost. PhD Thesis, Michigan State University, East Lansing, USA

    Google Scholar 

  • Romanenko LA, Schumann P, Rohde M, Lysenko AM, Mikhailov VV, Stakebrandt E (2002) Psychrobacter submarinus sp. nov. and Psychrobacter marincola sp. nov., psychrophilic halophiles from marine environments. Int J Syst Evol Microbiol 52:1291–1297

    Article  PubMed  CAS  Google Scholar 

  • Russell NJ (1990) Cold adaptation of microorganisms. Proc Natl Acad Sci USA 326:595–608

    CAS  Google Scholar 

  • Russell NJ (1997) Psychrophilic bacteria — Molecular adaptations of membrane lipids. Comp Biochem Physiol Part A: Physiol 118:489–493

    Article  CAS  Google Scholar 

  • Russell NJ (2000) Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4:83–90

    Article  PubMed  CAS  Google Scholar 

  • Saunders NFW, Thomas T, Curmi PMG, Mattick JS, Kuczek E, Slade R, Davis J, Franzmann PD, Boone D, Rusterholtz K et al (2003) Mechanisms of thermal adaptation revealed from the genomes of the Antarctic archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13:1580–1588

    Article  PubMed  CAS  Google Scholar 

  • Sher AV, Virina EI, Zazhigin VS (1977) Stratigraphy, paleomagnetism, and fauna of mammals of Pliocene-Upper Quanternary beds in Kolyma lower reaches. Doklady Akademii Nauk Sssr 234:1171–1174

    Google Scholar 

  • Shi T, Reeves RH, Gilichinsky DA, Friedmann EI (1997) Characterization of viable bacteria from Siberian permafrost by 16S rDNA sequencing. Microb Ecol 33:169–179

    Article  PubMed  CAS  Google Scholar 

  • Singer GAC, Hickey DA (2003) Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene 317:39–47

    Article  PubMed  CAS  Google Scholar 

  • Strocchi M, Ferrer M, Timmis KN, Golyshin PN (2006) Low temperature-induced systems failure in Escherichia coli: insights from rescue by cold-adapted chaperones. Proteomics 6:193–206

    Article  PubMed  CAS  Google Scholar 

  • Vishnivetskaya T, Kathariou S, McGrath J, Gilichinsky D, Tiedje JM (2000) Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments. Extremophiles 4:165–173

    Article  PubMed  CAS  Google Scholar 

  • Whyte LG, Inniss WE (1992) Cold-shock proteins and cold-acclimation proteins in a psychrotrophic bacterium. Can J Microbiol 38:1281–1285

    Article  CAS  Google Scholar 

  • Yao X, Jericho M, Pink D, Beveridge T (1999) Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy. J Bacteriol 181:6865–6875

    PubMed  CAS  Google Scholar 

  • Yumoto I, Hirota K, Sogabe Y, Nodasaka Y, Yokota Y, Hoshino T (2003) Psychrobacter okhotskensis sp. nov., a lipase-producing facultative psychrophile isolated from the coast of the Okhotsk Sea. Int J Syst Evol Microbiol 53:1985–19899

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Earth Sciences, Montana State University, P.O. Box 173480, Bozeman, MT, 59717, USA

    Corien Bakermans

  2. Department of Crop and Soil Sciences, Cornell University, Ithaca, NY, USA

    Peter W. Bergholz

  3. Department of Biology, University of Puerto Rico at Humacao, Humacao, PR, USA

    Hector Ayala-del-Río

  4. Center for Microbial Ecology, Michigan State University, East Lansing, MI, USA

    James Tiedje

Authors
  1. Corien Bakermans
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter W. Bergholz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hector Ayala-del-Río
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James Tiedje
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Corien Bakermans .

Editor information

Editors and Affiliations

  1. Institute of Microbiology, University of Innsbruck, Technikerstr. 25, 6020, Innsbruck, Austria

    Rosa Margesin

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Bakermans, C., Bergholz, P.W., Ayala-del-Río, H., Tiedje, J. (2009). Genomic Insights into Cold Adaptation of Permafrost Bacteria. In: Margesin, R. (eds) Permafrost Soils. Soil Biology, vol 16. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-69371-0_11

Download citation

Publish with us

Policies and ethics

Search

Navigation