Skip to main content

When the Vital Signs of Microbial Life Go Cold, Does That Mean the Pulse Is Gone? Microbial Life Persists at the Limits of Cryoenvironments on Earth

  • Chapter
  • First Online:
Microbes: The Foundation Stone of the Biosphere

Part of the book series: Advances in Environmental Microbiology ((AEM,volume 8))

  • 879 Accesses

Abstract

Cryoenvironments on Earth represent a natural laboratory in which we can observe the natural constraints to microbial activity and survival at low temperature. Microorganisms in sub-zero environments must contend with numerous stressors, and though microorganisms are nearly ubiquitous on this planet, the question of their activity under extremes of temperature is an open one. This essay describes soils in University Valley, located in the McMurdo Dry Valleys of Antarctica—a rare site in which microbial activity cannot be measured. Though the signs of active life were absent, the region is by no means dead. Microbial life persists in this valley, as in other cryoenvironments, and potentially on other planetary bodies within our solar system.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
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

References

  • Bakermans C, Bergholz PW, Ayala-del-Río H, Tiedje J (2009) Genomic insights into cold adaptation of permafrost bacteria. In: Permafrost soils. Springer, pp 159–168

    Google Scholar 

  • Bakermans C, Bergholz PW, Rodrigues DF, Vishnivetskaya TA, Ayala-del-Río HL, Tiedje JM (2011) Genomic and expression analyses of cold-adapted microorganisms. Polar microbiology: life in a deep freeze: 126–155

    Google Scholar 

  • Bakermans C, Skidmore ML, Douglas S, McKay CP (2014) Molecular characterization of bacteria from permafrost of the Taylor Valley, Antarctica. FEMS Microbiol Ecol 89(2):331–346

    CAS  PubMed  Google Scholar 

  • Blazewicz SJ, Barnard RL, Daly RA, Firestone MK (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J 7(11):2061–2068. https://doi.org/10.1038/ismej.2013.102

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bradley JA, Amend JP, LaRowe DE (2019) Survival of the fewest: microbial dormancy and maintenance in marine sediments through deep time. Geobiology 17(1):43–59

    PubMed  Google Scholar 

  • Brady A, Goordial J, Sun H, Whyte L, Slater G (2018) Variability in carbon uptake and (re) cycling in Antarctic cryptoendolithic microbial ecosystems demonstrated through radiocarbon analysis of organic biomarkers. Geobiology 16(1):62–79

    CAS  PubMed  Google Scholar 

  • Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8(2):129–138

    CAS  PubMed  Google Scholar 

  • Cavicchioli R (2006) Cold-adapted archaea. Nat Rev Microbiol 4(5):331–343

    CAS  PubMed  Google Scholar 

  • Coleine C, Zucconi L, Onofri S, Pombubpa N, Stajich JE, Selbmann L (2018) Sun exposure shapes functional grouping of fungi in Cryptoendolithic Antarctic communities. Life (Basel) 8(2). https://doi.org/10.3390/life8020019

  • Collins M, Buick R (1989) Effect of temperature on the spoilage of stored peas by Rhodotorula glutinis. Food Microbiol 6(3):135–141

    Google Scholar 

  • Davis J, Balme M, Grindrod P, Williams R, Gupta S (2016) Extensive Noachian fluvial systems in Arabia Terra: implications for early Martian climate. Geology 44(10):847–850

    Google Scholar 

  • Denis Lacelle WP, Whyte L, Davila A, Andersen D, DeWitt R, Goordial J, Heldmann J, Marinova M, Zacny K, McKay C (2012) Origin, stability and habitability of ice-bearing permafrost in University Valley, McMurdo Dry Valleys, Antarctica: analogue for ground ice on Mars, vol 31. Canadian Polar Commission

    Google Scholar 

  • Dohm JM, Ferris J, Baker VR, Anderson R, Hare T, Strom R, Barlow N, Tanaka KL, Klemaszewski J, Scott D (2001) Ancient drainage basin of the Tharsis region, Mars: potential source for outflow channel systems and putative oceans or paleolakes. Journal of Geophysical Research: Planets 106(E12):32943–32958

    Google Scholar 

  • Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1(3):200–208. https://doi.org/10.1038/nrmicro773

    CAS  PubMed  Google Scholar 

  • Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215(4536):1045–1053

    CAS  PubMed  Google Scholar 

  • Friedmann EI, Hua M, Ocampo-Friedmann R (1988) 3.6 Cryptoendolithic lichen and cyanobacterial communities of the Ross Desert, Antarctica. Polarforschung 58(2/3):251–259

    CAS  PubMed  Google Scholar 

  • Friedmann EI, Kappen L, Meyer M, Nienow JA (1993) Long-term productivity in the cryptoendolithic microbial community of the Ross Desert, Antarctica. Microb Ecol 25(1):51–69

    CAS  PubMed  Google Scholar 

  • Gilichinsky D, Wilson G, Friedmann E, McKay C, Sletten R, Rivkina E, Vishnivetskaya T, Erokhina L, Ivanushkina N, Kochkina G (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology 7(2):275–311

    CAS  PubMed  Google Scholar 

  • Goordial J, Davila A, Greer CW, Cannam R, DiRuggiero J, McKay CP, Whyte LG (2017) Comparative activity and functional ecology of permafrost soils and lithic niches in a hyper-arid polar desert. Environ Microbiol 19(2):443–458. https://doi.org/10.1111/1462-2920.13353

    CAS  PubMed  Google Scholar 

  • Goordial J, Davila A, Lacelle D, Pollard W, Marinova MM, Greer CW, DiRuggiero J, McKay CP, Whyte LG (2016) Nearing the cold-arid limits of microbial life in permafrost of an upper dry valley, Antarctica. ISME J 10(7):1613–1624. https://doi.org/10.1038/ismej.2015.239

    PubMed  PubMed Central  Google Scholar 

  • Goordial J, Lamarche-Gagnon G, Lay C-Y, Whyte L (2013) Left out in the cold: life in cryoenvironments. In: Polyextremophiles. Springer, Dordrecht, pp 335–363

    Google Scholar 

  • Goordial J, Raymond-Bouchard I, Riley R, Ronholm J, Shapiro N, Woyke T, LaButti KM, Tice H, Amirebrahimi M, Grigoriev IV (2016) Improved high-quality draft genome sequence of the eurypsychrophile Rhodotorula sp. JG1b, isolated from permafrost in the hyperarid upper-elevation mcmurdo dry valleys, Antarctica. Genome Announc 4(2)

    Google Scholar 

  • Goordial J, Raymond-Bouchard I, Ronholm J, Shapiro N, Woyke T, Whyte L, Bakermans C (2015) Improved-high-quality draft genome sequence of Rhodococcus sp. JG-3, a eurypsychrophilic Actinobacteria from Antarctic Dry Valley permafrost. Stand Genomic Sci 10(1):61

    PubMed  PubMed Central  Google Scholar 

  • Goordial J, Raymond-Bouchard I, Zolotarov Y, de Bethencourt L, Ronholm J, Shapiro N, Woyke T, Stromvik M, Greer CW, Bakermans C (2016) Cold adaptive traits revealed by comparative genomic analysis of the eurypsychrophile Rhodococcus sp. JG3 isolated from high elevation McMurdo Dry Valley permafrost, Antarctica. FEMS Microbiol Ecol 92(2)

    Google Scholar 

  • Goordial J, Whyte L (2014) Microbial life in Antarctic permafrost environments. In: Antarctic terrestrial microbiology. Springer, Berlin, Heidelberg, pp 217–232

    Google Scholar 

  • Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, Cook GM, Morales SE (2016) Genomic and metagenomic surveys of hydrogenase distribution indicate H 2 is a widely utilised energy source for microbial growth and survival. ISME J 10(3):761–777

    CAS  PubMed  Google Scholar 

  • Greening C, Grinter R, Chiri E (2019) Uncovering the metabolic strategies of the dormant microbial majority: towards integrative approaches. mSystems 4(3):e00107–e00119. https://doi.org/10.1128/mSystems.00107-19

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hallsworth JE, Yakimov MM, Golyshin PN, Gillion JLM, D'Auria G, De Lima Alves F, La Cono V, Genovese M, McKew BA, Hayes SL, Harris G, Giuliano L, Timmis KN, McGenity TJ (2007) Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ Microbiol 9(3):801–813. https://doi.org/10.1111/j.1462-2920.2006.01212.x

    CAS  PubMed  Google Scholar 

  • Head JW, Kreslavsky M, Hiesinger H, Ivanov M, Pratt S, Seibert N, Smith DE, Zuber MT (1998) Oceans in the past history of Mars: tests for their presence using Mars orbiter laser altimeter (MOLA) data. Geophys Res Lett 25(24):4401–4404

    Google Scholar 

  • Horowitz N, Cameron RE, Hubbard JS (1972) Microbiology of the dry valleys of Antarctica. Science 176(4032):242–245

    CAS  PubMed  Google Scholar 

  • Horowitz N, Hobby G, Hubbard J (1976) The Viking carbon assimilation experiments: interim report. Science 194(4271):1321–1322

    CAS  PubMed  Google Scholar 

  • Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, Montgomery K, Lines T, Beardall J, van Dorst J, Snape I, Stott MB, Hugenholtz P, Ferrari BC (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 552(7685):400–403. https://doi.org/10.1038/nature25014

    CAS  PubMed  Google Scholar 

  • Johnson SS, Hebsgaard MB, Christensen TR, Mastepanov M, Nielsen R, Munch K, Brand T, Gilbert MTP, Zuber MT, Bunce M, Rønn R, Gilichinsky D, Froese D, Willerslev E (2007) Ancient bacteria show evidence of DNA repair. Proc Natl Acad Sci 104(36):14401–14405. https://doi.org/10.1073/pnas.0706787104

    PubMed  Google Scholar 

  • Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci 107(13):5881–5886

    CAS  PubMed  Google Scholar 

  • Junge K, Eicken H, Deming JW (2004) Bacterial activity at− 2 to− 20 C in Arctic wintertime sea ice. Appl Environ Microbiol 70(1):550–557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lacelle D, Davila AF, Fisher D, Pollard WH, DeWitt R, Heldmann J, Marinova MM, McKay CP (2013) Excess ground ice of condensation–diffusion origin in University Valley, dry valleys of Antarctica: evidence from isotope geochemistry and numerical modeling. Geochim Cosmochim Acta 120:280–297. https://doi.org/10.1016/j.gca.2013.06.032

    CAS  Google Scholar 

  • Lee CK, Barbier BA, Bottos EM, McDonald IR, Cary SC (2012) The inter-valley soil comparative survey: the ecology of Dry Valley edaphic microbial communities. ISME J 6(5):1046–1057

    CAS  PubMed  Google Scholar 

  • Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9(2):119–130

    CAS  PubMed  Google Scholar 

  • Levy J (2013) How big are the McMurdo Dry Valleys? Estimating ice-free area using Landsat image data. Antarct Sci 25(1):119

    Google Scholar 

  • Lynch RC, Darcy JL, Kane NC, Nemergut DR, Schmidt SK (2014) Metagenomic evidence for metabolism of trace atmospheric gases by high-elevation desert Actinobacteria. Front Microbiol 5(698). https://doi.org/10.3389/fmicb.2014.00698

  • Lynch RC, King AJ, Farías ME, Sowell P, Vitry C, Schmidt SK (2012) The potential for microbial life in the highest-elevation (>6000 m.a.s.l.) mineral soils of the Atacama region. J Geophys Res Biogeo 117(G2). https://doi.org/10.1029/2012jg001961

  • Mackelprang R, Burkert A, Haw M, Mahendrarajah T, Conaway CH, Douglas TA, Waldrop MP (2017) Microbial survival strategies in ancient permafrost: insights from metagenomics. ISME J 11(10):2305–2318. https://doi.org/10.1038/ismej.2017.93

    CAS  PubMed  PubMed Central  Google Scholar 

  • Makhalanyane TP, Pointing SB, Cowan DA (2014) Lithobionts: cryptic and refuge niches. In: Antarctic terrestrial microbiology. Springer, pp 163–179

    Google Scholar 

  • Marchant DR, Head JW III (2007) Antarctic dry valleys: microclimate zonation, variable geomorphic processes, and implications for assessing climate change on Mars. Icarus 192(1):187–222

    Google Scholar 

  • Marinova MM, Mckay CP, Pollard WH, Heldmann JL, Davila AF, Andersen DT, Jackson WA, Lacelle D, Paulsen G, Zacny K (2013) Distribution of depth to ice-cemented soils in the high-elevation Quartermain Mountains, McMurdo Dry Valleys, Antarctica. Antarct Sci 25(4):575

    Google Scholar 

  • McEwen AS, Ojha L, Dundas CM, Mattson SS, Byrne S, Wray JJ, Cull SC, Murchie SL, Thomas N, Gulick VC (2011) Seasonal flows on warm Martian slopes. Science 333(6043):740–743

    CAS  PubMed  Google Scholar 

  • McKay CP, Balaban E, Abrahams S, Lewis N (2019) Dry permafrost over ice-cemented ground at Elephant Head, Ellsworth Land, Antarctica. Antarct Sci 31(5):263–270

    Google Scholar 

  • McKay CP, Stoker CR, Glass BJ, Davé AI, Davila AF, Heldmann JL, Marinova MM, Fairen AG, Quinn RC, Zacny KA (2013) The icebreaker life Mission to Mars: a search for biomolecular evidence for life. Astrobiology 13(4):334–353

    CAS  PubMed  Google Scholar 

  • Monteiro M, S Baptista M, Séneca J, Torgo L, K Lee C, Cary SC, Magalhães C (2020) Understanding the response of nitrifying communities to disturbance in the McMurdo Dry Valleys, Antarctica. Microorganisms 8(3):404

    CAS  PubMed Central  Google Scholar 

  • Mykytczuk NC, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG (2013) Bacterial growth at− 15 C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7(6):1211–1226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nagy B, Ignéczi Á, Kovács J, Szalai Z, Mari L (2019) Shallow ground temperature measurements on the highest volcano on Earth, Mt. Ojos del Salado, arid Andes, Chile. Permafr Periglac Process 30(1):3–18

    Google Scholar 

  • Pontefract A, Zhu TF, Walker VK, Hepburn H, Lui C, Zuber MT, Ruvkun G, Carr CE (2017) Microbial diversity in a hypersaline sulfate lake: a terrestrial analog of ancient Mars. Front Microbiol 8(1819). https://doi.org/10.3389/fmicb.2017.01819

  • Price PB, Sowers T (2004) Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci 101(13):4631–4636

    CAS  PubMed  Google Scholar 

  • Raymond-Bouchard I, Goordial J, Zolotarov Y, Ronholm J, Stromvik M, Bakermans C, Whyte LG (2018) Conserved genomic and amino acid traits of cold adaptation in subzero-growing Arctic permafrost bacteria. In: FEMS microbiology ecology 94 (4):fiy023

    Google Scholar 

  • Raymond-Bouchard I, Whyte LG (2017) From transcriptomes to metatranscriptomes: cold adaptation and active metabolisms of psychrophiles from cold environments. In: Psychrophiles: from biodiversity to biotechnology. Springer, pp 437–457

    Google Scholar 

  • Schaefer CEGR, Michel RFM, Delpupo C, Senra EO, Bremer UF, Bockheim JG (2017) Active layer thermal monitoring of a Dry Valley of the Ellsworth Mountains, continental Antarctica. Catena 149:603–615. https://doi.org/10.1016/j.catena.2016.07.020

    Google Scholar 

  • Seckbach J (2013) Life on the edge and astrobiology: who is who in the polyextremophiles world? In: Polyextremophiles. Springer, pp 61–79

    Google Scholar 

  • Selbmann L, De Hoog G, Mazzaglia A, Friedmann E, Onofri S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Stud Mycol 51 (1):1–32

    Google Scholar 

  • Siliakus MF, van der Oost J, Kengen SWM (2017) Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure. Extremophiles 21(4):651–670. https://doi.org/10.1007/s00792-017-0939-x

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stofan ER, Elachi C, Lunine JI, Lorenz RD, Stiles B, Mitchell K, Ostro S, Soderblom L, Wood C, Zebker H (2007) The lakes of Titan. Nature 445(7123):61–64

    CAS  PubMed  Google Scholar 

  • Sun HJ, Friedmann EI (1999) Growth on geological time scales in the Antarctic cryptoendolithic microbial community. Geomicrobiol J 16(2):193–202

    Google Scholar 

  • Sun HJ, Nienow JA, McKay C (2010) Antarctic cryptoendolithic microbial systems. In: Life in Antarctic deserts and other cold dry environments: astrobiological analogs. Cambridge University Press. In: p 307

    Google Scholar 

  • Williams TJ, Lauro FM, Ertan H, Burg DW, Poljak A, Raftery MJ, Cavicchioli R (2011) Defining the response of a microorganism to temperatures that span its complete growth temperature range (− 2 C to 28 C) using multiplex quantitative proteomics. Environ Microbiol 13(8):2186–2203

    CAS  PubMed  Google Scholar 

  • Zuber MT (2018) Oceans on Mars formed early. Nature Publishing Group

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jacqueline Marie Goordial .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Goordial, J.M. (2021). When the Vital Signs of Microbial Life Go Cold, Does That Mean the Pulse Is Gone? Microbial Life Persists at the Limits of Cryoenvironments on Earth. In: Hurst, C.J. (eds) Microbes: The Foundation Stone of the Biosphere. Advances in Environmental Microbiology, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-030-63512-1_6

Download citation

Publish with us

Policies and ethics