Genome-centric view of carbon processing in thawing permafrost

Woodcroft, Ben J.; Singleton, Caitlin M.; Boyd, Joel A.; Evans, Paul N.; Emerson, Joanne B.; Zayed, Ahmed A.  F.; Hoelzle, Robert D.; Lamberton, Timothy O.; McCalley, Carmody K.; Hodgkins, Suzanne B.; Wilson, Rachel M.; Purvine, Samuel O.; Nicora, Carrie D.; Li, Changsheng; Frolking, Steve; Chanton, Jeffrey P.; Crill, Patrick M.; Saleska, Scott R.; Rich, Virginia I.; Tyson, Gene W.

doi:10.1038/s41586-018-0338-1

Genome-centric view of carbon processing in thawing permafrost

Journal Article · Mon Jul 16 00:00:00 EDT 2018 · Nature (London)

DOI:https://doi.org/10.1038/s41586-018-0338-1· OSTI ID:1481643

^[1]; ^[2]; Boyd, Joel A. ^[2]; Evans, Paul N. ^[2]; ^[3]; ^[4]; ^[2]; Lamberton, Timothy O. ^[2]; ^[5]; ^[6]; Wilson, Rachel M. ^[6]; ^[7]; ^[7]; Li, Changsheng ^[8]; Frolking, Steve ^[8]; Chanton, Jeffrey P. ^[6]; Crill, Patrick M. ^[9]; ^[10]; ^[4]; ^[2]

Univ. of Queensland, Brisbane, QLD (Australia); The University of Queensland
Univ. of Queensland, Brisbane, QLD (Australia)
The Ohio State Univ., Columbus, OH (United States); Univ. of California, Davis, CA (United States)
The Ohio State Univ., Columbus, OH (United States)
Rochester Institute of Technology, Rochester, NY (United States)
Florida State Univ., Tallahassee, FL (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Univ. of New Hampshire, Durham, NH (United States)
Stockholm Univ., Stockholm (Sweden)
Univ. of Arizona, Tucson, AZ (United States)

As global temperatures rise, large amounts of carbon sequestered in permafrost are becoming available for microbial degradation. Accurate prediction of carbon gas emissions from thawing permafrost is limited by our understanding of these microbial communities. Here we use metagenomic sequencing of 214 samples from a permafrost thaw gradient to recover 1,529 metagenome-assembled genomes, including many from phyla with poor genomic representation. These genomes reflect the diversity of this complex ecosystem, with genus-level representatives for more than sixty per cent of the community. Meta-omic analysis revealed key populations involved in the degradation of organic matter, including bacteria whose genomes encode a previously undescribed fungal pathway for xylose degradation. Microbial and geochemical data highlight lineages that correlate with the production of greenhouse gases and indicate novel syntrophic relationships. Lastly, our findings link changing biogeochemistry to specific microbial lineages involved in carbon processing, and provide key information for predicting the effects of climate change on permafrost systems.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Arizona, Tucson, AZ (United States); The Ohio State Univ., Columbus, OH (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Contributing Organization:: Univ. of Queensland, Brisbane, QLD (Australia). Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences

Grant/Contract Number:: SC0010580; SC0016440

OSTI ID:: 1481643

Alternate ID(s):: OSTI ID: 1503613

Journal Information:: Nature (London), Journal Name: Nature (London) Journal Issue: 7716 Vol. 560; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (95)

Permafrost-thaw-induced land-cover change in the Canadian subarctic: implications for water resources Quinton, W. L.; Hayashi, M.; Chasmer, L. E. Hydrological Processes, Vol. 25, Issue 1 https://doi.org/10.1002/hyp.7894	journal	November 2010
RStudio: A Platform-Independent IDE for R and Sweave: SOFTWARE REVIEW Racine, Jeffrey S. Journal of Applied Econometrics, Vol. 27, Issue 1 https://doi.org/10.1002/jae.1278	journal	October 2011
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas Rai, Aditi; Bhattacharjee, Arindam Archives of Microbiology, Vol. 203, Issue 6 https://doi.org/10.1007/s00203-021-02278-7	journal	April 2021
Distribution of cell wall components in Sphagnum hyaline cells and in liverwort and hornwort elaters Kremer, Celeste; Pettolino, Filomena; Bacic, Antony Planta, Vol. 219, Issue 6 https://doi.org/10.1007/s00425-004-1308-4	journal	July 2004
The Effects of Permafrost Thaw on Soil Hydrologic, Thermal, and Carbon Dynamics in an Alaskan Peatland O’Donnell, Jonathan A.; Jorgenson, M. Torre; Harden, Jennifer W. Ecosystems, Vol. 15, Issue 2 https://doi.org/10.1007/s10021-011-9504-0	journal	November 2011
Genetic analysis of D-xylose metabolism pathways in Gluconobacter oxydans 621H Zhang, Minhua; Wei, Liujing; Zhou, Yi Journal of Industrial Microbiology & Biotechnology, Vol. 40, Issue 3-4 https://doi.org/10.1007/s10295-013-1231-4	journal	February 2013
Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples Wagner, Günter P.; Kin, Koryu; Lynch, Vincent J. Theory in Biosciences, Vol. 131, Issue 4 https://doi.org/10.1007/s12064-012-0162-3	journal	August 2012
Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation—Isotope evidence Whiticar, M. J.; Faber, E.; Schoell, M. Geochimica et Cosmochimica Acta, Vol. 50, Issue 5 https://doi.org/10.1016/0016-7037(86)90346-7	journal	May 1986
Methane release rate and methanogenic bacterial populations in lake sediments Lay, Jiunn-Jyi; Miyahara, Takashi; Noike, Tatsuya Water Research, Vol. 30, Issue 4 https://doi.org/10.1016/0043-1354(95)00254-5	journal	April 1996
Cloning and sequence determination of the gene encoding sorbitol dehydrogenase from Saccharomyces cerevisiae Sarthy, Aparna V.; Schopp, Cynthia; Idler, Kenneth B. Gene, Vol. 140, Issue 1 https://doi.org/10.1016/0378-1119(94)90741-2	journal	January 1994
Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane Whiticar, Michael J. Chemical Geology, Vol. 161, Issue 1-3, p. 291-314 https://doi.org/10.1016/S0009-2541(99)00092-3	journal	September 1999
The use of underloaded C18 solid-phase extraction plates increases reproducibility of analysis of tryptic peptides from unfractionated human plasma Guo, Xiaofeng; Kristal, Bruce S. Analytical Biochemistry, Vol. 426, Issue 1 https://doi.org/10.1016/j.ab.2012.04.003	journal	July 2012
Glycerol fermentation to hydrogen by Thermotoga maritima: Proposed pathway and bioenergetic considerations Maru, B. T.; Bielen, A. A. M.; Constantí, M. International Journal of Hydrogen Energy, Vol. 38, Issue 14 https://doi.org/10.1016/j.ijhydene.2013.02.130	journal	May 2013
pH controls over anaerobic carbon mineralization, the efficiency of methane production, and methanogenic pathways in peatlands across an ombrotrophic–minerotrophic gradient Ye, Rongzhong; Jin, Qusheng; Bohannan, Brendan Soil Biology and Biochemistry, Vol. 54 https://doi.org/10.1016/j.soilbio.2012.05.015	journal	November 2012
Species diversity in space and time Paine, Robert T. Trends in Ecology & Evolution, Vol. 10, Issue 12 https://doi.org/10.1016/s0169-5347(00)89212-5	journal	December 1995
Permafrost Degradation and Ecological Changes Associated with a WarmingClimate in Central Alaska Jorgenson, M. Torre; Racine, Charles H.; Walters, James C. Climatic Change, Vol. 48, Issue 4, p. 551-579 https://doi.org/10.1023/A:1005667424292	journal	March 2001
Thawing sub-arctic permafrost: Effects on vegetation and methane emissions Christensen, Torben R. Geophysical Research Letters, Vol. 31, Issue 4 https://doi.org/10.1029/2003GL018680	journal	January 2004
Accelerated thawing of subarctic peatland permafrost over the last 50 years Payette, Serge Geophysical Research Letters, Vol. 31, Issue 18 https://doi.org/10.1029/2004GL020358	journal	January 2004
Reduction of iron (III) and humic substances plays a major role in anaerobic respiration in an Arctic peat soil Lipson, David A.; Jha, Mony; Raab, Theodore K. Journal of Geophysical Research, Vol. 115 https://doi.org/10.1029/2009JG001147	journal	January 2010
Pyrosequencing enumerates and contrasts soil microbial diversity Roesch, Luiz F. W.; Fulthorpe, Roberta R.; Riva, Alberto The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.53	journal	July 2007
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
Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics Bertin, Philippe N.; Heinrich-Salmeron, Audrey; Pelletier, Eric The ISME Journal, Vol. 5, Issue 11 https://doi.org/10.1038/ismej.2011.51	journal	May 2011
Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms Tveit, Alexander; Schwacke, Rainer; Svenning, Mette M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.99	journal	September 2012
Methane dynamics regulated by microbial community response to permafrost thaw McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B. Nature, Vol. 514, Issue 7523 https://doi.org/10.1038/nature13798	journal	October 2014
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
Atmospheric trace gases support primary production in Antarctic desert surface soil Ji, Mukan; Greening, Chris; Vanwonterghem, Inka Nature, Vol. 552, Issue 7685 https://doi.org/10.1038/nature25014	journal	December 2017
A cross-platform toolkit for mass spectrometry and proteomics Chambers, Matthew C.; Maclean, Brendan; Burke, Robert Nature Biotechnology, Vol. 30, Issue 10 https://doi.org/10.1038/nbt.2377	journal	October 2012
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam Nature Biotechnology, Vol. 31, Issue 6 https://doi.org/10.1038/nbt.2579	journal	May 2013
Microbial diversity drives multifunctionality in terrestrial ecosystems Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10541	journal	January 2016
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Discovery of a novel methanogen prevalent in thawing permafrost Mondav, Rhiannon; Woodcroft, Ben J.; Kim, Eun-Hae Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4212	journal	February 2014
MS-GF+ makes progress towards a universal database search tool for proteomics Kim, Sangtae; Pevzner, Pavel A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6277	journal	October 2014
Humic substances as fully regenerable electron acceptors in recurrently anoxic environments Klüpfel, Laura; Piepenbrock, Annette; Kappler, Andreas Nature Geoscience, Vol. 7, Issue 3 https://doi.org/10.1038/ngeo2084	journal	February 2014
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Electron transfer in syntrophic communities of anaerobic bacteria and archaea Stams, Alfons J. M.; Plugge, Caroline M. Nature Reviews Microbiology, Vol. 7, Issue 8 https://doi.org/10.1038/nrmicro2166	journal	August 2009
The microbial ecology of permafrost Jansson, Janet K.; Taş, Neslihan Nature Reviews Microbiology, Vol. 12, Issue 6 https://doi.org/10.1038/nrmicro3262	journal	May 2014
Landscape topography structures the soil microbiome in arctic polygonal tundra Taş, Neslihan; Prestat, Emmanuel; Wang, Shi Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03089-z	journal	February 2018
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria Nature Microbiology, Vol. 2, Issue 11 https://doi.org/10.1038/s41564-017-0012-7	journal	September 2017
Estimation of methanotroph abundance in a freshwater lake sediment Costello, Andria M.; Auman, Ann J.; Macalady, Jennifer L. Environmental Microbiology, Vol. 4, Issue 8 https://doi.org/10.1046/j.1462-2920.2002.00318.x	journal	August 2002
Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2 Baani, M.; Liesack, W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 29 https://doi.org/10.1073/pnas.0702643105	journal	July 2008
Permafrost carbon-climate feedbacks accelerate global warming Koven, C. D.; Ringeval, B.; Friedlingstein, P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 36 https://doi.org/10.1073/pnas.1103910108	journal	August 2011
Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 16 https://doi.org/10.1073/pnas.1314641111	journal	April 2014
Tackling soil diversity with the assembly of large, complex metagenomes Howe, Adina Chuang; Jansson, Janet K.; Malfatti, Stephanie A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 13 https://doi.org/10.1073/pnas.1402564111	journal	March 2014
Shannon's Formula as a Measure of Specific Diversity: Its Use and Misuse Pielou, E. C. The American Naturalist, Vol. 100, Issue 914 https://doi.org/10.1086/282439	journal	September 1966
Biogeochemistry of Methane Exchange between Natural Wetlands and the Atmosphere Whalen, S. C. Environmental Engineering Science, Vol. 22, Issue 1 https://doi.org/10.1089/ees.2005.22.73	journal	January 2005
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts611	journal	October 2012
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
The ENZYME database in 2000 Bairoch, A. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.304	journal	January 2000
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins Pruitt, K. D. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki025	journal	December 2004
NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins Pruitt, K. D.; Tatusova, T.; Maglott, D. R. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl842	journal	January 2007
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
2016 update of the PRIDE database and its related tools Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1145	journal	November 2015
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
2016 update of the PRIDE database and its related tools Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi Nucleic Acids Research, Vol. 44, Issue 22 https://doi.org/10.1093/nar/gkw880	journal	September 2016
GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes Boyd, Joel A.; Woodcroft, Ben J.; Tyson, Gene W. Nucleic Acids Research, Vol. 46, Issue 10 https://doi.org/10.1093/nar/gky174	journal	March 2018
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Decadal vegetation changes in a northern peatland, greenhouse gas fluxes and net radiative forcing Johansson, TorbjÖRn; Malmer, Nils; Crill, Patrick M. Global Change Biology, Vol. 12, Issue 12 https://doi.org/10.1111/j.1365-2486.2006.01267.x	journal	December 2006
Bacterial populations and environmental factors controlling cellulose degradation in an acidic Sphagnum peat: Cellulose degradation in acidic peat Pankratov, Timofey A.; Ivanova, Anastasia O.; Dedysh, Svetlana N. Environmental Microbiology, Vol. 13, Issue 7 https://doi.org/10.1111/j.1462-2920.2011.02491.x	journal	May 2011
Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments Conrad, R. FEMS Microbiology Ecology, Vol. 28, Issue 3 https://doi.org/10.1111/j.1574-6941.1999.tb00575.x	journal	March 1999
Stress response of methanogenic archaea from Siberian permafrost compared with methanogens from nonpermafrost habitats: Stress response of methanogenic archaea from permafrost Morozova, Daria; Wagner, Dirk FEMS Microbiology Ecology, Vol. 61, Issue 1 https://doi.org/10.1111/j.1574-6941.2007.00316.x	journal	July 2007
Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate Welsh, David T. FEMS Microbiology Reviews, Vol. 24, Issue 3 https://doi.org/10.1111/j.1574-6976.2000.tb00542.x	journal	July 2000
Identification of microbial populations driving biopolymer degradation in acidic peatlands by metatranscriptomic analysis Ivanova, Anastasia A.; Wegner, Carl-Eric; Kim, Yongkyu Molecular Ecology, Vol. 25, Issue 19 https://doi.org/10.1111/mec.13806	journal	September 2016
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics Evans, P. N.; Parks, D. H.; Chadwick, G. L. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac7745	journal	October 2015
Metatranscriptomic Analysis of Arctic Peat Soil Microbiota Tveit, Alexander T.; Urich, Tim; Svenning, Mette M. Applied and Environmental Microbiology, Vol. 80, Issue 18 https://doi.org/10.1128/AEM.01030-14	journal	July 2014
Purification and partial characterization of an aldo-keto reductase from Saccharomyces cerevisiae. Kuhn, A.; van Zyl, C.; van Tonder, A. Applied and environmental microbiology, Vol. 61, Issue 4 https://doi.org/10.1128/AEM.61.4.1580-1585.1995	journal	January 1995
Hydrogenotrophic Methanogenesis by Moderately Acid-Tolerant Methanogens of a Methane-Emitting Acidic Peat Horn, M. A.; Matthies, C.; Kusel, K. Applied and Environmental Microbiology, Vol. 69, Issue 1 https://doi.org/10.1128/AEM.69.1.74-83.2003	journal	January 2003
Coaggregation Facilitates Interspecies Hydrogen Transfer between Pelotomaculum thermopropionicum and Methanothermobacter thermautotrophicus Ishii, S.; Kosaka, T.; Hori, K. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.7838-7845.2005	journal	December 2005
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/MMBR.60.2.439-471.1996	journal	January 1996
The changing landscape of Canada's western boreal forest: the current dynamics of permafrost Vitt, Dale H.; Halsey, Linda A.; Zoltai, Stephen C. Canadian Journal of Forest Research, Vol. 30, Issue 2 https://doi.org/10.1139/x99-214	journal	February 2000
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-538	journal	October 2010
Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: A genome and transcriptome approach Rodrigues, Debora F.; Ivanova, Natalia; He, Zhili BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-547	journal	January 2008
CopyRighter: a rapid tool for improving the accuracy of microbial community profiles through lineage-specific gene copy number correction Angly, Florent E.; Dennis, Paul G.; Skarshewski, Adam Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-11	journal	April 2014
Polinton-like viruses are abundant in aquatic ecosystems Bellas, Christopher M.; Sommaruga, Ruben Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00956-0	journal	January 2021
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Solid-phase organic matter reduction regulates anaerobic decomposition in bog soil Keller, Jason K.; Takagi, Kimberly K. Ecosphere, Vol. 4, Issue 5 https://doi.org/10.1890/ES12-00382.1	journal	May 2013
Upgrading of Anaerobic Digestion of Waste Activated Sludge by Thermal Pretreatment Li, Y-. Y.; Noike, T. Water Science and Technology, Vol. 26, Issue 3-4 https://doi.org/10.2166/wst.1992.0466	journal	August 1992
Cyclic Development of Permafrost in the Peatlands of Northwestern Alberta, Canada Zoltai, S. C. Arctic and Alpine Research, Vol. 25, Issue 3 https://doi.org/10.2307/1551820	journal	August 1993
Species Diversity in Space and Time Maurer, Brian A.; Rosenzweig, Michael L. Ecology, Vol. 77, Issue 4 https://doi.org/10.2307/2265609	journal	June 1996
Species Diversity in Space and Time. Magurran, A. E.; Rosenzweig, M. The Journal of Applied Ecology, Vol. 33, Issue 1 https://doi.org/10.2307/2405034	journal	February 1996
Metabolic engineering of yeasts by heterologous enzyme production for degradation of cellulose and hemicellulose from biomass: a perspective Kricka, William; Fitzpatrick, James; Bond, Ursula Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00174	journal	April 2014
Metagenomics Reveals Pervasive Bacterial Populations and Reduced Community Diversity across the Alaska Tundra Ecosystem Johnston, Eric R.; Rodriguez-R, Luis M.; Luo, Chengwei Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00579	journal	April 2016
Present state of global wetland extent and wetland methane modelling: methodology of a model inter-comparison project (WETCHIMP) Wania, R.; Melton, J. R.; Hodson, Elke L. ETH Zurich https://doi.org/10.3929/ethz-b-000070026	text	January 2013
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia arXiv https://doi.org/10.48550/arxiv.1003.5943	preprint	January 2010
Present state of global wetland extent and wetland methane modelling: conclusions from a model inter-comparison project (WETCHIMP) Melton, J. R.; Wania, R.; Hodson, E. L. Biogeosciences, Vol. 10, Issue 2 https://doi.org/10.5194/bg-10-753-2013	journal	January 2013
Present state of global wetland extent and wetland methane modelling: conclusions from a model intercomparison project (WETCHIMP) Melton, J. R.; Wania, R.; Hodson, E. L. Biogeosciences Discussions, Vol. 9, Issue 8 https://doi.org/10.5194/bgd-9-11577-2012	journal	January 2012
Present state of global wetland extent and wetland methane modelling: methodology of a model inter-comparison project (WETCHIMP) Wania, R.; Melton, J. R.; Hodson, E. L. Geoscientific Model Development, Vol. 6, Issue 3 https://doi.org/10.5194/gmd-6-617-2013	journal	January 2013
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015

Cited By (42)

Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments Vigneron, Adrien; Alsop, Eric B.; Cruaud, Perrine mSystems, Vol. 4, Issue 1 https://doi.org/10.1128/msystems.00091-18	journal	February 2019
Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes Zhang, Ximei; Johnston, Eric R.; Wang, Yaosheng mSystems, Vol. 4, Issue 5 https://doi.org/10.1128/msystems.00374-19	journal	October 2019
The Signal and the Noise: Characteristics of Antisense RNA in Complex Microbial Communities Michaelsen, Thomas Yssing; Brandt, Jakob; Singleton, Caitlin Margaret mSystems, Vol. 5, Issue 1 https://doi.org/10.1128/msystems.00587-19	journal	February 2020
Consistent Metagenome-Derived Metrics Verify and Delineate Bacterial Species Boundaries Olm, Matthew R.; Crits-Christoph, Alexander; Diamond, Spencer mSystems, Vol. 5, Issue 1 https://doi.org/10.1128/msystems.00731-19	journal	January 2020
Long-read based de novo assembly of low-complexity metagenome samples results in finished genomes and reveals insights into strain diversity and an active phage system Somerville, Vincent; Lutz, Stefanie; Schmid, Michael BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1500-0	journal	June 2019
Genomic and in-situ Transcriptomic Characterization of the Candidate Phylum NPL-UPL2 From Highly Alkaline Highly Reducing Serpentinized Groundwater Suzuki, Shino; Nealson, Kenneth H.; Ishii, Shun’ichi Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03141	journal	December 2018
Identification of Molecular Markers That Are Specific to the Class Thermoleophilia Hu, Danyu; Zang, Yang; Mao, Yingjin Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01185	journal	May 2019
Distinct Taxonomic and Functional Profiles of the Microbiome Associated With Different Soil Horizons of a Moist Tussock Tundra in Alaska Tripathi, Binu M.; Kim1, Hye Min; Jung, Ji Young Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01442	journal	June 2019
Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake Vigneron, Adrien; Lovejoy, Connie; Cruaud, Perrine Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01656	journal	July 2019
Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial Phylum Candidatus Eremiobacterota (WPS-2) Ward, Lewis M.; Cardona, Tanai; Holland-Moritz, Hannah Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01658	journal	July 2019
Implication of Viral Infections for Greenhouse Gas Dynamics in Freshwater Wetlands: Challenges and Perspectives Bonetti, Giuditta; Trevathan-Tackett, Stacey M.; Carnell, Paul E. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01962	journal	August 2019
Microbial Community Structure and Methane Cycling Potential along a Thermokarst Pond-Peatland Continuum Vigneron, Adrien; Cruaud, Perrine; Bhiry, Najat Microorganisms, Vol. 7, Issue 11 https://doi.org/10.3390/microorganisms7110486	journal	October 2019
Additional file 2 of High-quality bacterial genomes of a partial-nitritation/anammox system by an iterative hybrid assembly method Liu, Lei; Wang, Yulin; Che, You figshare https://doi.org/10.6084/m9.figshare.13203415	dataset	January 2020
Additional file 3 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608591	dataset	January 2021
Additional file 4 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608594	dataset	January 2021
Additional file 5 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608597	dataset	January 2021
Additional file 7 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608603.v1	dataset	January 2021
Additional file 8 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608606	dataset	January 2021
Non‐cyanobacterial diazotrophs dominate nitrogen‐fixing communities in permafrost thaw ponds Fernandez, Leyden; Bertilsson, Stefan; Peura, Sari Limnology and Oceanography, Vol. 65, Issue S1 https://doi.org/10.1002/lno.11243	journal	January 2020
Ontogenic succession of thermokarst thaw ponds is linked to dissolved organic matter quality and microbial degradation potential Peura, Sari; Wauthy, Maxime; Simone, Domenico Limnology and Oceanography, Vol. 65, Issue S1 https://doi.org/10.1002/lno.11349	journal	January 2020
Think global, act local: The small‐scale environment mainly influences microbial community development and function in lake sediment Orland, Chloé; Yakimovich, Kurt M.; Mykytczuk, Nadia C. S. Limnology and Oceanography, Vol. 65, Issue S1 https://doi.org/10.1002/lno.11370	journal	January 2020
Linking metagenomics to aquatic microbial ecology and biogeochemical cycles Grossart, Hans‐Peter; Massana, Ramon; McMahon, Katherine D. Limnology and Oceanography, Vol. 65, Issue S1 https://doi.org/10.1002/lno.11382	journal	January 2020
Methane Production Pathway Regulated Proximally by Substrate Availability and Distally by Temperature in a High‐Latitude Mire Complex Chang, Kuang‐Yu; Riley, William J.; Brodie, Eoin L. Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 10 https://doi.org/10.1029/2019jg005355	journal	October 2019
Methanotrophy across a natural permafrost thaw environment Singleton, Caitlin M.; McCalley, Carmody K.; Woodcroft, Ben J. The ISME Journal, Vol. 12, Issue 10 https://doi.org/10.1038/s41396-018-0065-5	journal	June 2018
Niche differentiation is spatially and temporally regulated in the rhizosphere Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0582-x	journal	January 2020
Host-linked soil viral ecology along a permafrost thaw gradient Emerson, Joanne B.; Roux, Simon; Brum, Jennifer R. Nature Microbiology, Vol. 3, Issue 8 https://doi.org/10.1038/s41564-018-0190-y	journal	July 2018
Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms Diamond, Spencer; Andeer, Peter F.; Li, Zhou Nature Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/s41564-019-0449-y	journal	May 2019
Climate change microbiology — problems and perspectives Hutchins, David A.; Jansson, Janet K.; Remais, Justin V. Nature Reviews Microbiology, Vol. 17, Issue 6 https://doi.org/10.1038/s41579-019-0178-5	journal	May 2019
Scientists’ warning to humanity: microorganisms and climate change Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N. Nature Reviews Microbiology, Vol. 17, Issue 9 https://doi.org/10.1038/s41579-019-0222-5	journal	June 2019
Soil microbiomes and climate change Jansson, Janet K.; Hofmockel, Kirsten S. Nature Reviews Microbiology, Vol. 18, Issue 1 https://doi.org/10.1038/s41579-019-0265-7	journal	October 2019
Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths Johnston, Eric R.; Hatt, Janet K.; He, Zhili Proceedings of the National Academy of Sciences, Vol. 116, Issue 30 https://doi.org/10.1073/pnas.1901307116	journal	July 2019
The known and the unknown in soil microbial ecology Baldrian, Petr FEMS Microbiology Ecology, Vol. 95, Issue 2 https://doi.org/10.1093/femsec/fiz005	journal	January 2019
Untapped viral diversity in global soil metagenomes Graham, Emily B.; Paez-Espino, David; Brislawn, Colin BioRxiv https://doi.org/10.1101/583997	posted_content	January 2019
Soil carbon loss with warming: New evidence from carbon‐degrading enzymes Chen, Ji; Elsgaard, Lars; Groenigen, Kees Jan Global Change Biology, Vol. 26, Issue 4 https://doi.org/10.1111/gcb.14986	journal	April 2020
Ecological and Genomic Attributes of Novel Bacterial Taxa That Thrive in Subsurface Soil Horizons Brewer, Tess E.; Aronson, Emma L.; Arogyaswamy, Keshav mBio, Vol. 10, Issue 5 https://doi.org/10.1128/mbio.01318-19	journal	October 2019
To Dereplicate or Not To Dereplicate? Evans, Jacob T.; Denef, Vincent J. mSphere, Vol. 5, Issue 3 https://doi.org/10.1128/msphere.00971-19	journal	June 2020
Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing Trubl, Gareth; Jang, Ho Bin; Roux, Simon mSystems, Vol. 3, Issue 5 https://doi.org/10.1128/msystems.00076-18	journal	October 2018
Microbiome of vineyard soils is shaped by geography and management Coller, Emanuela; Cestaro, Alessandro; Zanzotti, Roberto Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0758-7	journal	November 2019
Think global, act local: The small-scale environment mainly influences microbial community development and function in lake sediment Orland, C.; Yakimovich, Km; Mykytczuk, Ncs Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.44763	text	January 2020
Scientists’ warning to humanity: microorganisms and climate change Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N. ETH Zurich https://doi.org/10.3929/ethz-b-000350779	text	January 2019
Large carbon cycle sensitivities to climate across a permafrost thaw gradient in subarctic Sweden Chang, Kuang-Yu; Riley, William J.; Crill, Patrick M. The Cryosphere, Vol. 13, Issue 2 https://doi.org/10.5194/tc-13-647-2019	journal	January 2019
Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils Trubl, Gareth; Roux, Simon; Solonenko, Natalie PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7265	journal	January 2019

Similar Records

Genome-centric view of carbon processing in thawing permafrost

Journal Article · Mon Jul 16 00:00:00 EDT 2018 · Nature (London) · OSTI ID:1503613

Discovery of a novel methanogen prevalent in thawing permafrost

Journal Article · Thu Feb 13 23:00:00 EST 2014 · Nature Communications · OSTI ID:1602278

Pathways to Carbon Liberation: A Systems Approach to Understanding Carbon Transformations and Losses from Thawing Permafrost

Technical Report · Mon Apr 01 00:00:00 EDT 2019 · OSTI ID:1506685

Related Subjects

54 ENVIRONMENTAL SCIENCES
58 GEOSCIENCES
59 BASIC BIOLOGICAL SCIENCES
Archaea
Bacteria
Biogeochemistry
Metagenomics
Metaproteomics
Metatranscriptomics
Permafrost

Genome-centric view of carbon processing in thawing permafrost

Citation Formats

References (95)

Cited By (42)

Linked Research (1)

Similar Records

Related Subjects