Microbial Ecology of Permafrost Soils: Populations, Processes, and Perspectives

Waldrop, Mark P.; Ernakovich, Jessica Gilman; Vishnivetskaya, Tatiana A.; Schaefer, Sean R.; Mackelprang, Rachel; Barta, Jiri; O′Brien, Joy M.; Winkel, Matthias; Barbato, Robyn A.; Heffernan, Liam; Leewis, Mary‐Cathrine; Hewitt, Rebecca E.; Hultman, Jenni; Sun, Yanchen; Biasi, Christina; Bradley, James A.; Liebner, Susanne; Ricketts, Michael P.; Muscarella, Mario E.; Schütte, Ursel; Abuah, Fumnanya; Whalen, Emily; Timling, Ina; Voigt, Carolina; Taş, Neslihan; Lloyd, Karen G.; Siljanen, Henri M. P.; Rivkina, Elizaveta M.; Voříšková, Jana; Tao, Jing; Liang, Renxing; Li, Zhen; Lennon, Jay T.; Onstott, T. C.

doi:10.1002/ppp.2264

Title: Microbial Ecology of Permafrost Soils: Populations, Processes, and Perspectives

Journal Article · Mon Jan 13 00:00:00 UTC 2025 · Permafrost and Periglacial Processes

DOI: https://doi.org/10.1002/ppp.2264 · OSTI ID:2564962

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US Geological Survey, CA (United States)
Univ. of New Hampshire, Durham, NH (United States)
Univ. of Tennessee, Knoxville, TN (United States)
California State University, Northridge (CSUN), CA (United States)
University of South Bohemia, České Budějovice (Czech Republic)
Indiana Univ., Bloomington, IN (United States)
German Federal Institute for Risk Assessment, Berlin (Germany)
Cold Regions Research and Engineering Laboratory, NH (United States)
Vrije Univ., Amsterdam (Netherlands)
Agriculture and Agri‐Food Canada, Quebec City, QC (Canada)
Amherst College, MA (United States)
Natural Resources Institute Finland, Helsinki (Finland)
Woods Hole Oceanographic Institution, Falmouth, MA (United States)
Univ. Innsbruck (Austria); Univ. of Eastern Finland, Kuopio (Finland)
Aix-Marseille Univ., Marseille (France); Centre National de la Recherche Scientifique (CNRS) (France); Queen Mary Univ. of London (United Kingdom)
GFZ Helmholtz Centre for Geosciences, Potsdam (Germany)
Argonne National Laboratory (ANL), Argonne, IL (United States)
Univ. of Alaska, Fairbanks, AK (United States)
Univ. of Hamburg (Germany)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Univ. of Eastern Finland, Kuopio (Finland)
Institute of Physicochemical and Biological Problems in Soil Science, Moscow (Russian Federation)
Czech Academy of Sciences (CAS), Prague (Czech Republic). Institute of Microbiology
China University of Geosciences, Wuhan (China)
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Princeton Univ., NJ (United States)

Permafrost microbial research has flourished in the past decades, due in part to improvements in sampling and molecular techniques, but also the increased focus on the permafrost greenhouse gas feedback to climate change and other ecological processes in high latitude and alpine permafrost soils. Permafrost microorganisms are adapted to these extreme environments and remain active at low temperatures and when resources are limited. They are also an important component of global elemental cycles as they regulate organic matter turnover and greenhouse gas production, particularly as permafrost thaws. Here we review the permafrost microbiology literature coupled with an exploration of its historical aspects, with a particular focus on a new understanding advanced by molecular biology techniques. We further identify knowledge gaps and ways forward to improve our understanding of microbial contributions to ecosystem biogeochemistry of permafrost-affected systems.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); University of Tennessee, Knoxville, TN (United States)

Sponsoring Organization:: US Department of Energy; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231; AC02-06CH11357; AC52-07NA27344; SC0020369

OSTI ID:: 2564962

Report Number(s):: LLNL--JRNL-2004999; LLNL--JRNL-872115

Journal Information:: Permafrost and Periglacial Processes, Journal Name: Permafrost and Periglacial Processes Journal Issue: 2 Vol. 36; ISSN 1045-6740

Publisher:: Wiley - International Permafrost AssociationCopyright Statement

Country of Publication:: United States

Language:: English

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Permafrost collapse alters soil carbon stocks, respiration, CH ₄ , and N ₂ O in upland tundra Abbott, Benjamin W.; Jones, Jeremy B. Global Change Biology, Vol. 21, Issue 12 https://doi.org/10.1111/gcb.13069	journal	November 2015
Methane oxidation in contrasting soil types: responses to experimental warming with implication for landscape-integrated CH ₄ budget D'Imperio, Ludovica; Nielsen, Cecilie Skov; Westergaard-Nielsen, Andreas Global Change Biology, Vol. 23, Issue 2 https://doi.org/10.1111/gcb.13400	journal	July 2016
Microbiome assembly in thawing permafrost and its feedbacks to climate Ernakovich, Jessica G.; Barbato, Robyn A.; Rich, Virginia I. Global Change Biology, Vol. 28, Issue 17 https://doi.org/10.1111/gcb.16231	journal	June 2022
Microbial methane cycling in sediments of Arctic thermokarst lagoons Yang, Sizhong; Anthony, Sara E.; Jenrich, Maren Global Change Biology, Vol. 29, Issue 10 https://doi.org/10.1111/gcb.16649	journal	March 2023
Methanogenic activity and biomass in Holocene permafrost deposits of the Lena Delta, Siberian Arctic and its implication for the global methane budget Wagner, Dirk; Gattinger, Andreas; Embacher, Arndt Global Change Biology, Vol. 13, Issue 5 https://doi.org/10.1111/j.1365-2486.2007.01331.x	journal	May 2007
Molecular investigations into a globally important carbon pool: permafrost-protected carbon in Alaskan soils Waldrop, M. P.; Wickland, K. P.; White Iii, R. Global Change Biology https://doi.org/10.1111/j.1365-2486.2009.02141.x	journal	February 2010
A High Arctic soil ecosystem resists long-term environmental manipulations: ARCTIC SOIL RESISTS ENVIRONMENTAL CHANGE Lamb, Eric G.; Han, Sukkyun; Lanoil, Brian D. Global Change Biology, Vol. 17, Issue 10 https://doi.org/10.1111/j.1365-2486.2011.02431.x	journal	April 2011
Hot spots for nitrous oxide emissions found in different types of permafrost peatlands: NITROUS OXIDE FLUXES FROM PERMAFROST PEATLANDS Marushchak, M. E.; PitkÄMÄKi, A.; Koponen, H. Global Change Biology, Vol. 17, Issue 8 https://doi.org/10.1111/j.1365-2486.2011.02442.x	journal	May 2011
Methane oxidation associated with submerged brown mosses reduces methane emissions from Siberian polygonal tundra: Moss-associated methane oxidation Liebner, Susanne; Zeyer, Josef; Wagner, Dirk Journal of Ecology, Vol. 99, Issue 4 https://doi.org/10.1111/j.1365-2745.2011.01823.x	journal	March 2011
Abundance, distribution and potential activity of methane oxidizing bacteria in permafrost soils from the Lena Delta, Siberia Liebner, Susanne; Wagner, Dirk Environmental Microbiology, Vol. 9, Issue 1 https://doi.org/10.1111/j.1462-2920.2006.01120.x	journal	January 2007
Viability, diversity and composition of the bacterial community in a high Arctic permafrost soil from Spitsbergen, Northern Norway Hansen, Aviaja A.; Herbert, Rodney A.; Mikkelsen, Karina Environmental Microbiology, Vol. 9, Issue 11 https://doi.org/10.1111/j.1462-2920.2007.01403.x	journal	November 2007
Bioavailability of soil organic matter and microbial community dynamics upon permafrost thaw: Bioavailability of permafrost organic matter Coolen, Marco J. L.; van de Giessen, Jeroen; Zhu, Elizabeth Y. Environmental Microbiology, Vol. 13, Issue 8 https://doi.org/10.1111/j.1462-2920.2011.02489.x	journal	May 2011
Growth kinetics of microorganisms isolated from Alaskan soil and permafrost in solid media frozen down to â35Â°C: Growth kinetics in frozen media Panikov, Nicolai S.; Sizova, Maria V. FEMS Microbiology Ecology, Vol. 59, Issue 2 https://doi.org/10.1111/j.1574-6941.2006.00210.x	journal	February 2007
Characterization of the microbial diversity in a permafrost sample from the Canadian high Arctic using culture-dependent and culture-independent methods: Microbial diversity in Canadian high Arctic permafrost Steven, Blaire; Briggs, Geoffrey; McKay, Chris P. FEMS Microbiology Ecology, Vol. 59, Issue 2 https://doi.org/10.1111/j.1574-6941.2006.00247.x	journal	February 2007
Biogeochemistry of methane and methanogenic archaea in permafrost: Methane and methanogenic archaea in permafrost Rivkina, Elizaveta; Shcherbakova, Viktoria; Laurinavichius, Kestas FEMS Microbiology Ecology, Vol. 61, Issue 1 https://doi.org/10.1111/j.1574-6941.2007.00315.x	journal	July 2007
Long-term warming alters the composition of Arctic soil microbial communities Deslippe, Julie R.; Hartmann, Martin; Simard, Suzanne W. FEMS Microbiology Ecology, Vol. 82, Issue 2 https://doi.org/10.1111/j.1574-6941.2012.01350.x	journal	April 2012
Ancient fungi in Antarctic permafrost environments Kochkina, Galina; Ivanushkina, Natalya; Ozerskaya, Svetlana FEMS Microbiology Ecology, Vol. 82, Issue 2 https://doi.org/10.1111/j.1574-6941.2012.01442.x	journal	July 2012
Long-term experimental warming alters community composition of ascomycetes in Alaskan moist and dry arctic tundra Semenova, Tatiana A.; Morgado, Luis N.; Welker, Jeffrey M. Molecular Ecology, Vol. 24, Issue 2 https://doi.org/10.1111/mec.13045	journal	January 2015
Distinct microbial communities in the active and permafrost layers on the Tibetan Plateau Chen, Yong-Liang; Deng, Ye; Ding, Jin-Zhi Molecular Ecology, Vol. 26, Issue 23 https://doi.org/10.1111/mec.14396	journal	November 2017
Is Live Smallpox Lurking in the Arctic? Stone, Richard Science, Vol. 295, Issue 5562 https://doi.org/10.1126/science.295.5562.2002	journal	March 2002
The Genome Sequence of Psychrobacter arcticus 273-4, a Psychroactive Siberian Permafrost Bacterium, Reveals Mechanisms for Adaptation to Low-Temperature Growth Ayala-del-Rio, H. L.; Chain, P. S.; Grzymski, J. J. Applied and Environmental Microbiology, Vol. 76, Issue 7 https://doi.org/10.1128/AEM.02101-09	journal	February 2010
Changes in the Active, Dead, and Dormant Microbial Community Structure across a Pleistocene Permafrost Chronosequence Burkert, Alexander; Douglas, Thomas A.; Waldrop, Mark P. Applied and Environmental Microbiology, Vol. 85, Issue 7 https://doi.org/10.1128/AEM.02646-18	journal	January 2019
Stable Isotope Probing Analysis of the Diversity and Activity of Methanotrophic Bacteria in Soils from the Canadian High Arctic Martineau, C.; Whyte, L. G.; Greer, C. W. Applied and Environmental Microbiology, Vol. 76, Issue 17 https://doi.org/10.1128/AEM.03094-09	journal	July 2010
Metabolic Activity of Permafrost Bacteria below the Freezing Point Rivkina, E. M.; Friedmann, E. I.; McKay, C. P. Applied and Environmental Microbiology, Vol. 66, Issue 8 https://doi.org/10.1128/AEM.66.8.3230-3233.2000	journal	August 2000
Soil Type Is the Primary Determinant of the Composition of the Total and Active Bacterial Communities in Arable Soils Girvan, M. S.; Bullimore, J.; Pretty, J. N. Applied and Environmental Microbiology, Vol. 69, Issue 3 https://doi.org/10.1128/AEM.69.3.1800-1809.2003	journal	March 2003
Beringian Paleoecology Inferred from Permafrost-Preserved Fungal DNA Lydolph, Magnus C.; Jacobsen, Jonas; Arctander, Peter Applied and Environmental Microbiology, Vol. 71, Issue 2 https://doi.org/10.1128/AEM.71.2.1012-1017.2005	journal	February 2005
Survival of Acanthamoeba Cysts after Desiccation for More than 20 Years Sriram, Rama; Shoff, Megan; Booton, Gregory Journal of Clinical Microbiology, Vol. 46, Issue 12 https://doi.org/10.1128/JCM.01903-08	journal	December 2008
RNA Viruses Linked to Eukaryotic Hosts in Thawed Permafrost Wu, Ruonan; Bottos, Eric M.; Danna, Vincent G. mSystems, Vol. 7, Issue 6 https://doi.org/10.1128/msystems.00582-22	journal	December 2022
Microbial diversity of active layer and permafrost in an acidic wetland from the Canadian High Arctic Wilhelm, Roland C.; Niederberger, Thomas D.; Greer, Charles Canadian Journal of Microbiology, Vol. 57, Issue 4 https://doi.org/10.1139/w11-004	journal	April 2011
Maintenance of Plant Species Diversity by Pathogens Bever, James D.; Mangan, Scott A.; Alexander, Helen M. Annual Review of Ecology, Evolution, and Systematics, Vol. 46, Issue 1 https://doi.org/10.1146/annurev-ecolsys-112414-054306	journal	December 2015
Epidemiology ofRhodotorula: An Emerging Pathogen Wirth, Fernanda; Goldani, Luciano Z. Interdisciplinary Perspectives on Infectious Diseases, Vol. 2012 https://doi.org/10.1155/2012/465717	journal	January 2012
Warming changes the composition and diversity of fungal communities in permafrost Jiang, Yunbing; Yang, Libin; Wu, Song Annals of Microbiology, Vol. 73, Issue 1 https://doi.org/10.1186/s13213-022-01707-2	journal	February 2023
Active virus-host interactions at sub-freezing temperatures in Arctic peat soil Trubl, Gareth; Kimbrel, Jeffrey A.; Liquet-Gonzalez, Jose Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-021-01154-2	journal	October 2021
In-depth characterization of denitrifier communities across different soil ecosystems in the tundra Pessi, Igor S.; Viitamäki, Sirja; Virkkala, Anna-Maria Environmental Microbiome, Vol. 17, Issue 1 https://doi.org/10.1186/s40793-022-00424-2	journal	June 2022
Metagenomic Insights into Anaerobic Metabolism along an Arctic Peat Soil Profile Lipson, David A.; Haggerty, John Matthew; Srinivas, Archana PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0064659	journal	May 2013
Diversity and potential activity of methanotrophs in high methane-emitting permafrost thaw ponds Crevecoeur, Sophie; Vincent, Warwick F.; Comte, Jérôme PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0188223	journal	November 2017
The role of changing temperature in microbial metabolic processes during permafrost thaw Messan, Komi S.; Jones, Robert M.; Doherty, Stacey J. PLOS ONE, Vol. 15, Issue 4 https://doi.org/10.1371/journal.pone.0232169	journal	April 2020
The Evolution and Genetics of Virus Host Shifts Longdon, Ben; Brockhurst, Michael A.; Russell, Colin A. PLoS Pathogens, Vol. 10, Issue 11 https://doi.org/10.1371/journal.ppat.1004395	journal	November 2014
Zoonotic spillover: Understanding basic aspects for better prevention Ellwanger, Joel Henrique; Chies, José Artur Bogo Genetics and Molecular Biology, Vol. 44, Issue 1 suppl 1 https://doi.org/10.1590/1678-4685-gmb-2020-0355	journal	January 2021
Resistance of Acanthamoeba castellanii Cysts to Physical, Chemical, and Radiological Conditions Aksozek, A.; McClellan, K.; Howard, K. Journal of Parasitology, Vol. 88, Issue 3 https://doi.org/10.1645/0022-3395(2002)088[0621:ROACCT]2.0.CO;2	journal	June 2002
The transcriptional response of microbial communities in thawing Alaskan permafrost soils Coolen, Marco J. L.; Orsi, William D. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00197	journal	March 2015
Shifts in methanogenic community composition and methane fluxes along the degradation of discontinuous permafrost Liebner, Susanne; Ganzert, Lars; Kiss, Andrea Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00356	journal	May 2015
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker Knief, Claudia Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01346	journal	December 2015
NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient Penton, C. Ryan; Yang, Caiyun; Wu, Liyou Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01894	journal	November 2016
Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence Leewis, Mary-Cathrine; Berlemont, Renaud; Podgorski, David C. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01753	journal	July 2020
Soil Disturbance Affects Plant Productivity via Soil Microbial Community Shifts Seitz, Taylor J.; Schütte, Ursel M. E.; Drown, Devin M. Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.619711	journal	February 2021
Anthrax and the Geochemistry of Soils in the Contiguous United States Griffin, Dale; Silvestri, Erin; Bowling, Charlena Geosciences, Vol. 4, Issue 3 https://doi.org/10.3390/geosciences4030114	journal	August 2014
Rapid Permafrost Thaw Removes Nitrogen Limitation and Rises the Potential for N2O Emissions Wegner, Rica; Fiencke, Claudia; Knoblauch, Christian Nitrogen, Vol. 3, Issue 4 https://doi.org/10.3390/nitrogen3040040	journal	November 2022
An Update on Eukaryotic Viruses Revived from Ancient Permafrost Alempic, Jean-Marie; Lartigue, Audrey; Goncharov, Artemiy E. Viruses, Vol. 15, Issue 2 https://doi.org/10.3390/v15020564	journal	February 2023

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