The effects of warming and soil chemistry on bacterial community structure in Arctic tundra soils

Ricketts, Michael P.; Matamala, Roser; Jastrow, Julie D.; Antonopoulos, Dionysios A.; Koval, Jason; Ping, Chien-Lu; Liang, Chao; Gonzalez-Meler, Miquel A.

doi:10.1016/j.soilbio.2020.107882

The effects of warming and soil chemistry on bacterial community structure in Arctic tundra soils

Journal Article · Tue Jun 23 00:00:00 EDT 2020 · Soil Biology and Biochemistry

DOI:https://doi.org/10.1016/j.soilbio.2020.107882· OSTI ID:1658898

Ricketts, Michael P. ^[1]; Matamala, Roser ^[2]; Jastrow, Julie D. ^[2]; Antonopoulos, Dionysios A. ^[2]; Koval, Jason ^[2]; Ping, Chien-Lu ^[3]; Liang, Chao ^[4]; Gonzalez-Meler, Miquel A. ^[5]

Univ. of Chicago, IL (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)
Univ. of Alaska, Fairbanks, AK (United States)
Chinese Academy of Sciences (CAS), Shenyang, Liaoning (China)
Univ. of Chicago, IL (United States)

Soil microbial communities in the Arctic play a critical role in regulating the global carbon (C) cycle. Vast amounts of C are stored in northern latitude soils, and rising temperatures in the Arctic threaten to thaw permafrost, making relatively inaccessible C sources more available for mineralization by soil microbes. Few studies have characterized how microbial community structure responds to thawing permafrost in the context of varying soil chemistries associated with contrasting tundra landscapes. Here, we subjected active layer and permafrost soils from upland and lowland tundra sites on the North Slope of Alaska to a soil-warming incubation experiment and compared soil bacterial community profiles (obtained by 16S rRNA amplicon sequencing) before and after incubation. The influence of soil composition (characterized by mid-infrared [MIR] spectroscopy) on bacterial community structure and class abundance was analyzed using redundancy and correlation analyses. We found increased abundances of Alphaproteobacteria, Gammaproteobacteria, and Bacteroidetes [Sphingobacteriia] post incubation, particularly in permafrost soils. The categorical descriptors site and soil layer had the most explanatory power in our predictive models of bacterial community structure, highlighting the close relationship between soil bacteria and the soil environment. Specific soil chemical attributes characterizing the soil environments that were found to be the best predictors include MIR spectral bands associated with inorganic C, silicates, amide II (C=N stretch), and carboxylics (C-O stretch), and MIR peak ratios representing C substrate quality. Overall, these results further characterize soil bacterial community shifts that may occur as a frozen environment with limited access to C sources, such as is found in undisturbed permafrost, transitions to warmer and more C-available environments, such as is predicted in thawing permafrost due to climate change.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1658898

Alternate ID(s):: OSTI ID: 1809302

Journal Information:: Soil Biology and Biochemistry, Journal Name: Soil Biology and Biochemistry Vol. 148; ISSN 0038-0717

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Temperature sensitivity of soil organic matter decomposition—what do we know? von Lützow, Margit; Kögel-Knabner, Ingrid Biology and Fertility of Soils, Vol. 46, Issue 1 https://doi.org/10.1007/s00374-009-0413-8	journal	October 2009
Polar amplification of climate change in coupled models Holland, M. M.; Bitz, C. M. Climate Dynamics, Vol. 21, Issue 3-4 https://doi.org/10.1007/s00382-003-0332-6	journal	September 2003
Biological indicators of soil quality and soil organic matter characteristics in an agricultural management continuum Veum, Kristen S.; Goyne, Keith W.; Kremer, Robert J. Biogeochemistry, Vol. 117, Issue 1 https://doi.org/10.1007/s10533-013-9868-7	journal	June 2013
Redox and temperature-sensitive changes in microbial communities and soil chemistry dictate greenhouse gas loss from thawed permafrost Ernakovich, Jessica G.; Lynch, Laurel M.; Brewer, Paul E. Biogeochemistry, Vol. 134, Issue 1-2 https://doi.org/10.1007/s10533-017-0354-5	journal	July 2017
Expert assessment of vulnerability of permafrost carbon to climate change Schuur, E. A. G.; Abbott, B. W.; Bowden, W. B. Climatic Change, Vol. 119, Issue 2 https://doi.org/10.1007/s10584-013-0730-7	journal	March 2013
A Caution Regarding Rules of Thumb for Variance Inflation Factors O’brien, Robert M. Quality & Quantity, Vol. 41, Issue 5 https://doi.org/10.1007/s11135-006-9018-6	journal	March 2007
Linking microbial community composition to function in a tropical soil Waldrop, M. P.; Balser, T. C.; Firestone, M. K. Soil Biology and Biochemistry, Vol. 32, Issue 13 https://doi.org/10.1016/S0038-0717(00)00157-7	journal	November 2000
Temperature controls of microbial respiration in arctic tundra soils above and below freezing Mikan, Carl J.; Schimel, Joshua P.; Doyle, Allen P. Soil Biology and Biochemistry, Vol. 34, Issue 11 https://doi.org/10.1016/S0038-0717(02)00168-2	journal	November 2002
Microbial diversity and function in soil: from genes to ecosystems Torsvik, Vigdis; Øvreås, Lise Current Opinion in Microbiology, Vol. 5, Issue 3, p. 240-245 https://doi.org/10.1016/S1369-5274(02)00324-7	journal	June 2002
Evaluation of sewage sludge-based compost by FT-IR spectroscopy Grube, M.; Lin, J. G.; Lee, P. H. Geoderma, Vol. 130, Issue 3-4 https://doi.org/10.1016/j.geoderma.2005.02.005	journal	February 2006
Substrate utilisation profiles of microbial communities in peat are depth dependent and correlate with whole soil FTIR profiles Artz, R.; Chapman, S.; Campbell, C. Soil Biology and Biochemistry, Vol. 38, Issue 9 https://doi.org/10.1016/j.soilbio.2006.04.017	journal	September 2006
FTIR spectroscopy can be used as a screening tool for organic matter quality in regenerating cutover peatlands Artz, Rebekka R. E.; Chapman, Stephen J.; Jean Robertson, A. H. Soil Biology and Biochemistry, Vol. 40, Issue 2 https://doi.org/10.1016/j.soilbio.2007.09.019	journal	February 2008
Pyrosequencing and mid-infrared spectroscopy reveal distinct aggregate stratification of soil bacterial communities and organic matter composition Davinic, Marko; Fultz, Lisa M.; Acosta-Martinez, Veronica Soil Biology and Biochemistry, Vol. 46 https://doi.org/10.1016/j.soilbio.2011.11.012	journal	March 2012
Predicting the decomposability of arctic tundra soil organic matter with mid infrared spectroscopy Matamala, Roser; Jastrow, Julie D.; Calderón, Francisco J. Soil Biology and Biochemistry, Vol. 129 https://doi.org/10.1016/j.soilbio.2018.10.014	journal	February 2019
Mineral weathering by bacteria: ecology, actors and mechanisms Uroz, Stéphane; Calvaruso, Christophe; Turpault, Marie-Pierre Trends in Microbiology, Vol. 17, Issue 8 https://doi.org/10.1016/j.tim.2009.05.004	journal	August 2009
The Mineralosphere Concept: Mineralogical Control of the Distribution and Function of Mineral-associated Bacterial Communities Uroz, Stephane; Kelly, Laura Catherine; Turpault, Marie-Pierre Trends in Microbiology, Vol. 23, Issue 12 https://doi.org/10.1016/j.tim.2015.10.004	journal	December 2015
Soil organic carbon and CO ₂ respiration at subzero temperature in soils of Arctic Alaska Michaelson, G. J. Journal of Geophysical Research, Vol. 108, Issue D2 https://doi.org/10.1029/2001JD000920	journal	January 2003
Environmental microarray analyses of Antarctic soil microbial communities Yergeau, Etienne; Schoondermark-Stolk, Sung A.; Brodie, Eoin L. The ISME Journal, Vol. 3, Issue 3 https://doi.org/10.1038/ismej.2008.111	journal	November 2008
Examining the global distribution of dominant archaeal populations in soil Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory The ISME Journal, Vol. 5, Issue 5 https://doi.org/10.1038/ismej.2010.171	journal	November 2010
The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses Yergeau, Etienne; Hogues, Hervé; Whyte, Lyle G. The ISME Journal, Vol. 4, Issue 9 https://doi.org/10.1038/ismej.2010.41	journal	April 2010
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea McDonald, Daniel; Price, Morgan N.; Goodrich, Julia The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.139	journal	December 2011
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Microbial survival strategies in ancient permafrost: insights from metagenomics Mackelprang, Rachel; Burkert, Alexander; Haw, Monica The ISME Journal, Vol. 11, Issue 10 https://doi.org/10.1038/ismej.2017.93	journal	July 2017
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change Davidson, Eric A.; Janssens, Ivan A. Nature, Vol. 440, Issue 7081 https://doi.org/10.1038/nature04514	journal	March 2006
Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M. Nature, Vol. 480, Issue 7377 https://doi.org/10.1038/nature10576	journal	November 2011
Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14238	journal	March 2015
Climate change and the permafrost carbon feedback Schuur, E. A. G.; McGuire, A. D.; Schädel, C. Nature, Vol. 520, Issue 7546 https://doi.org/10.1038/nature14338	journal	April 2015
High stocks of soil organic carbon in the North American Arctic region Ping, Chien-Lu; Michaelson, Gary J.; Jorgenson, Mark T. Nature Geoscience, Vol. 1, Issue 9 https://doi.org/10.1038/ngeo284	journal	August 2008
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Microbial degradation of aromatic compounds — from one strategy to four Fuchs, Georg; Boll, Matthias; Heider, Johann Nature Reviews Microbiology, Vol. 9, Issue 11, p. 803-816 https://doi.org/10.1038/nrmicro2652	journal	October 2011
Long-term in situ permafrost thaw effects on bacterial communities and potential aerobic respiration Monteux, Sylvain; Weedon, James T.; Blume-Werry, Gesche The ISME Journal, Vol. 12, Issue 9 https://doi.org/10.1038/s41396-018-0176-z	journal	June 2018
Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests Kaiser, Kristin; Wemheuer, Bernd; Korolkow, Vera Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33696	journal	September 2016
Temperature dependence of metabolic rates for microbial growth, maintenance, and survival Price, P. B.; Sowers, T. Proceedings of the National Academy of Sciences, Vol. 101, Issue 13 https://doi.org/10.1073/pnas.0400522101	journal	March 2004
The diversity and biogeography of soil bacterial communities Fierer, N.; Jackson, R. B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0507535103	journal	January 2006
Ancient bacteria show evidence of DNA repair Johnson, S. S.; Hebsgaard, M. B.; Christensen, T. R. Proceedings of the National Academy of Sciences, Vol. 104, Issue 36 https://doi.org/10.1073/pnas.0706787104	journal	August 2007
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Distribution and Quality of the Organic Matter in Light and Heavy Fractions of a Red Latosol under Different Uses and Management Practices Assis, C. P.; Jucksch, I.; Mendonça, E. S. Communications in Soil Science and Plant Analysis, Vol. 43, Issue 5 https://doi.org/10.1080/00103624.2012.648469	journal	March 2012
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
PEAR: a fast and accurate Illumina Paired-End reAd mergeR Zhang, J.; Kobert, K.; Flouri, T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt593	journal	October 2013
Revisiting life strategy concepts in environmental microbial ecology Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fix006	journal	January 2017
Preservation of nucleic acids by freeze-drying for next generation sequencing analyses of soil microbial communities Weißbecker, Christina; Buscot, François; Wubet, Tesfaye Journal of Plant Ecology, Vol. 10, Issue 1 https://doi.org/10.1093/jpe/rtw042	journal	January 2017
Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation McCarthy, Davis J.; Chen, Yunshun; Smyth, Gordon K. Nucleic Acids Research, Vol. 40, Issue 10 https://doi.org/10.1093/nar/gks042	journal	January 2012
Disentangling the complexity of permafrost soil by using high resolution profiling of microbial community composition, key functions and respiration rates Müller, Oliver; Bang‐Andreasen, Toke; White, Richard Allen Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14348	journal	July 2018
Properties and bioavailability of particulate and mineral-associated organic matter in Arctic permafrost soils, Lower Kolyma Region, Russia: Organic matter stabilization in permafrost soils Gentsch, N.; Mikutta, R.; Shibistova, O. European Journal of Soil Science, Vol. 66, Issue 4 https://doi.org/10.1111/ejss.12269	journal	June 2015
Temperature response of permafrost soil carbon is attenuated by mineral protection Gentsch, Norman; Wild, Birgit; Mikutta, Robert Global Change Biology, Vol. 24, Issue 8 https://doi.org/10.1111/gcb.14316	journal	June 2018
Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils Wallenstein, Matthew D.; Mcmahon, Shawna K.; Schimel, Joshua P. Global Change Biology, Vol. 15, Issue 7 https://doi.org/10.1111/j.1365-2486.2008.01819.x	journal	July 2009
Soil organic matter turnover is governed by accessibility not recalcitrance Dungait, Jennifer A. J.; Hopkins, David W.; Gregory, Andrew S. Global Change Biology, Vol. 18, Issue 6 https://doi.org/10.1111/j.1365-2486.2012.02665.x	journal	March 2012
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
Ecosystem-level controls on root-rhizosphere respiration Hopkins, Francesca; Gonzalez-Meler, Miquel A.; Flower, Charles E. New Phytologist, Vol. 199, Issue 2 https://doi.org/10.1111/nph.12271	journal	April 2013
Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale Lauber, C. L.; Hamady, M.; Knight, R. Applied and Environmental Microbiology, Vol. 75, Issue 15 https://doi.org/10.1128/AEM.00335-09	journal	June 2009
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
Psychrophilic bacteria. Morita, R. Y. Bacteriological Reviews, Vol. 39, Issue 2 https://doi.org/10.1128/MMBR.39.2.144-167.1975	journal	January 1975
Toward an Ecological Classification of soil Bacteria Fierer, Noah; Bradford, Mark A.; Jackson, Robert B. Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/05-1839	journal	June 2007
Humic-Acid Transformation during Composting of Municipal Solid Waste Chefetz, Benny; Adani, Fabrizio; Genevini, Pierluigi Journal of Environmental Quality, Vol. 27, Issue 4 https://doi.org/10.2134/jeq1998.00472425002700040011x	journal	July 1998
Solid-state Carbon-13 Nuclear Magnetic Resonance and Infrared Spectroscopy of Composted Organic Matter Inbar, Y.; Chen, Y.; Hadar, Y. Soil Science Society of America Journal, Vol. 53, Issue 6 https://doi.org/10.2136/sssaj1989.03615995005300060014x	journal	January 1989
Mineral Transformations in Permafrost-Affected Soils, North Kolyma Lowland, Russia Alekseev, A.; Alekseeva, T.; Ostroumov, V. Soil Science Society of America Journal, Vol. 67, Issue 2 https://doi.org/10.2136/sssaj2003.5960	journal	March 2003
Clay Mineralogy in Arctic Tundra Gelisols, Northern Alaska Borden, Patrick W.; Ping, Chien-Lu; McCarthy, Paul J. Soil Science Society of America Journal, Vol. 74, Issue 2 https://doi.org/10.2136/sssaj2009.0187	journal	January 2010
Soils Associated with Biotic Activity on Frost Boils in Arctic Alaska Michaelson, G. J.; Ping, C. L.; Walker, D. A. Soil Science Society of America Journal, Vol. 76, Issue 6 https://doi.org/10.2136/sssaj2012.0064	journal	January 2012
Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities Flynn, Theodore M.; Koval, Jason C.; Greenwald, Stephanie M. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02321	journal	November 2017
Reporting Key Features in Cold-Adapted Bacteria Tribelli, Paula; López, Nancy Life, Vol. 8, Issue 1 https://doi.org/10.3390/life8010008	journal	March 2018
Storage and transformation of organic matter fractions in cryoturbated permafrost soils across the Siberian Arctic Gentsch, N.; Mikutta, R.; Alves, R. J. E. Biogeosciences, Vol. 12, Issue 14 https://doi.org/10.5194/bg-12-4525-2015	journal	January 2015
Permafrost soils and carbon cycling Ping, C. L.; Jastrow, J. D.; Jorgenson, M. T. SOIL, Vol. 1, Issue 1 https://doi.org/10.5194/soil-1-147-2015	journal	January 2015
Soil bacterial community and functional shifts in response to altered snowpack in moist acidic tundra of northern Alaska Ricketts, Michael P.; Poretsky, Rachel S.; Welker, Jeffrey M. SOIL, Vol. 2, Issue 3 https://doi.org/10.5194/soil-2-459-2016	journal	January 2016
Recent applications of vibrational mid-Infrared (IR) spectroscopy for studying soil components: a review Tinti, Anna; Tugnoli, Vitaliano; Bonora, Sergio Journal of Central European Agriculture, Vol. 16, Issue 1 https://doi.org/10.5513/JCEA01/16.1.1535	journal	January 2015

Similar Records

Shifts of tundra bacterial and archaeal communities along a permafrost thaw gradient in A laska

Journal Article · Tue Dec 30 19:00:00 EST 2014 · Molecular Ecology · OSTI ID:1400676

Related Subjects

16S rRNA sequencing
59 BASIC BIOLOGICAL SCIENCES
Arctic tundra soil incubations
Bacterial community structure
Mid-infrared spectroscopy
Permafrost carbon
Soil organic matter chemistry

The effects of warming and soil chemistry on bacterial community structure in Arctic tundra soils

Citation Formats

References (65)

Similar Records

Related Subjects