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; Crits-Christoph, Alexander; Burstein, David; Anantharaman, Karthik; Lane, Katherine R.; Thomas, Brian C.; Pan, Chongle; Northen, Trent R.; Banfield, Jillian F.

doi:10.1038/s41564-019-0449-y

Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms

Journal Article · Mon May 20 00:00:00 EDT 2019 · Nature Microbiology

DOI:https://doi.org/10.1038/s41564-019-0449-y· OSTI ID:1542407

^[1]; Andeer, Peter F. ^[2]; Li, Zhou ^[3]; Crits-Christoph, Alexander ^[1]; Burstein, David ^[4]; ^[5]; Lane, Katherine R. ^[1]; Thomas, Brian C. ^[1]; Pan, Chongle ^[6]; ^[7]; ^[1]

Univ. of California, Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of California, Berkeley, CA (United States) ; Tel Aviv Univ., Ramat Aviv (Israel)
Univ. of California, Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Oklahoma, Norman, OK (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Soil microbial activity drives the carbon and nitrogen cycles and is an important determinant of atmospheric trace gas turnover, yet most soils are dominated by microorganisms with unknown metabolic capacities. Even Acidobacteria, among the most abundant bacteria in soil, remain poorly characterized, and functions across groups such as Verrucomicrobia, Gemmatimonadetes, Chloroflexi and Rokubacteria are understudied. Here, we have resolved 60 metagenomic and 20 proteomic data sets from a Mediterranean grassland soil ecosystem and recovered 793 near-complete microbial genomes from 18 phyla, representing around one-third of all microorganisms detected. Importantly, this enabled extensive genomics-based metabolic predictions for these communities. Acidobacteria from multiple previously unstudied classes have genomes that encode large enzyme complements for complex carbohydrate degradation. In contrast, most microorganisms encode carbohydrate esterases that strip readily accessible methyl and acetyl groups from polymers like pectin and xylan, forming methanol and acetate, the availability of which could explain the high prevalence of C₁ metabolism and acetate utilization in genomes. Microorganism abundances among samples collected at three soil depths and under natural and amended rainfall regimes indicate statistically higher associations of inorganic nitrogen metabolism and carbon degradation in deep and shallow soils, respectively. This partitioning decreased in samples under extended spring rainfall, indicating that long-term climate alteration can affect both carbon and nitrogen cycling. As a whole, by leveraging natural and experimental gradients with genome-resolved metabolic profiles, we link microorganisms lacking prior genomic characterization to specific roles in complex carbon, C₁, nitrate and ammonia transformations, and constrain factors that impact their distributions in soil.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1542407

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 8 Vol. 4; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (107)

A Second Molybdoprotein Aldehyde Dehydrogenase fromAmycolatopsis methanolicaNCIB 11946 Kim, Si W.; Luykx, Dion M. A. M.; de Vries, Simon Archives of Biochemistry and Biophysics, Vol. 325, Issue 1 https://doi.org/10.1006/abbi.1996.0001	journal	January 1996
PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim Applied Microbiology and Biotechnology, Vol. 98, Issue 14 https://doi.org/10.1007/s00253-014-5766-8	journal	May 2014
Stability of YREE complexes with the trihydroxamate siderophore desferrioxamine B at seawater ionic strength Christenson, Emily A.; Schijf, Johan Geochimica et Cosmochimica Acta, Vol. 75, Issue 22 https://doi.org/10.1016/j.gca.2011.09.022	journal	November 2011
Molecular structure of La3+-induced methanol dehydrogenase-like protein in Methylobacterium radiotolerans Hibi, Yoshihisa; Asai, Kentaro; Arafuka, Hiroshi Journal of Bioscience and Bioengineering, Vol. 111, Issue 5 https://doi.org/10.1016/j.jbiosc.2010.12.017	journal	May 2011
Soil organic carbon stock in grasslands: Effects of inorganic fertilizers, liming and grazing in different climate settings Eze, Samuel; Palmer, Sheila M.; Chapman, Pippa J. Journal of Environmental Management, Vol. 223 https://doi.org/10.1016/j.jenvman.2018.06.013	journal	October 2018
Towards a Natural History of Soil Bacterial Communities Martiny, Jennifer B. H.; Walters, Kendra E. Trends in Microbiology, Vol. 26, Issue 4 https://doi.org/10.1016/j.tim.2018.02.010	journal	April 2018
The importance of grasslands for animal production and other functions: a review on management and methodological progress in the tropics Boval, M.; Dixon, R. M. animal, Vol. 6, Issue 05 https://doi.org/10.1017/s1751731112000304	journal	February 2012
Large-scale analysis of the yeast proteome by multidimensional protein identification technology Washburn, Michael P.; Wolters, Dirk; Yates, John R. Nature Biotechnology, Vol. 19, Issue 3 https://doi.org/10.1038/85686	journal	March 2001
Energy from thin air Cowan, Don A.; Makhalanyane, Thulani P. Nature, Vol. 552, Issue 7685 https://doi.org/10.1038/d41586-017-07579-w	journal	December 2017
Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea Alves, Ricardo J. Eloy; Wanek, Wolfgang; Zappe, Anna The ISME Journal, Vol. 7, Issue 8 https://doi.org/10.1038/ismej.2013.35	journal	March 2013
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
Diverse and divergent protein post-translational modifications in two growth stages of a natural microbial community Li, Zhou; Wang, Yingfeng; Yao, Qiuming Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5405	journal	July 2014
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Elias, Joshua E.; Gygi, Steven P. Nature Methods, Vol. 4, Issue 3 https://doi.org/10.1038/nmeth1019	journal	February 2007
Embracing the unknown: disentangling the complexities of the soil microbiome Fierer, Noah Nature Reviews Microbiology, Vol. 15, Issue 10 https://doi.org/10.1038/nrmicro.2017.87	journal	August 2017
Metabolic coupling on roots Beattie, Gwyn A. Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0139-1	journal	March 2018
Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis Crits-Christoph, Alexander; Diamond, Spencer; Butterfield, Cristina N. Nature, Vol. 558, Issue 7710 https://doi.org/10.1038/s41586-018-0207-y	journal	June 2018
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens Papalexi, Efthymia; Mimitou, Eleni P.; Butler, Andrew W. Nature Genetics, Vol. 53, Issue 3 https://doi.org/10.1038/s41588-021-00778-2	journal	March 2021
Effects of timber harvesting on the genetic potential for carbon and nitrogen cycling in five North American forest ecozones Cardenas, Erick; Orellana, Luis H.; Konstantinidis, Konstantinos T. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-21197-0	journal	February 2018
Analyses of soil microbial community compositions and functional genes reveal potential consequences of natural forest succession Cong, Jing; Yang, Yunfeng; Liu, Xueduan Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep10007	journal	May 2015
Ecology's most general, yet protean 1 pattern: the species-area relationship Lomolino, Mark V. Journal of Biogeography, Vol. 27, Issue 1 https://doi.org/10.1046/j.1365-2699.2000.00377.x	journal	January 2000
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups Placella, S. A.; Brodie, E. L.; Firestone, M. K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1204306109	journal	June 2012
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
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets Wu, Yu-Wei; Simmons, Blake A.; Singer, Steven W. Bioinformatics, Vol. 32, Issue 4 https://doi.org/10.1093/bioinformatics/btv638	journal	October 2015
Sipros Ensemble improves database searching and filtering for complex metaproteomics Guo, Xuan; Li, Zhou; Yao, Qiuming Bioinformatics, Vol. 34, Issue 5 https://doi.org/10.1093/bioinformatics/btx601	journal	September 2017
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
UniProt: the universal protein knowledgebase No authors listed Nucleic Acids Research, Vol. 45, Issue D1, p. D158-D169 https://doi.org/10.1093/nar/gkw1099	journal	November 2016
dbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation Huang, Le; Zhang, Han; Wu, Peizhi Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx894	journal	October 2017
dbCAN2: a meta server for automated carbohydrate-active enzyme annotation Zhang, Han; Yohe, Tanner; Huang, Le Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky418	journal	May 2018
Accurate, multi-kb reads resolve complex populations and detect rare microorganisms Sharon, Itai; Kertesz, Michael; Hug, Laura A. Genome Research, Vol. 25, Issue 4 https://doi.org/10.1101/gr.183012.114	journal	February 2015
Soil microbial community composition in tallgrass prairie restorations converge with remnants across a 27‐year chronosequence Barber, Nicholas A.; Chantos‐Davidson, Karley M.; Amel Peralta, Rene Environmental Microbiology, Vol. 19, Issue 8 https://doi.org/10.1111/1462-2920.13785	journal	July 2017
Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments : Genomic insights into acidobacteria Eichorst, Stephanie A.; Trojan, Daniela; Roux, Simon Environmental Microbiology, Vol. 20, Issue 3 https://doi.org/10.1111/1462-2920.14043	journal	March 2018
Exploring links between pH and bacterial community composition in soils from the Craibstone Experimental Farm Bartram, Andrea K.; Jiang, Xingpeng; Lynch, Michael D. J. FEMS Microbiology Ecology, Vol. 87, Issue 2 https://doi.org/10.1111/1574-6941.12231	journal	October 2013
Quantification of Burkholderia coxL Genes in Hawaiian Volcanic Deposits Weber, C. F.; King, G. M. Applied and Environmental Microbiology, Vol. 76, Issue 7 https://doi.org/10.1128/aem.01861-09	journal	February 2010
Identification of Unknown Carboxydovore Bacteria Dominant in Deciduous Forest Soil via Succession of Bacterial Communities, coxL Genotypes, and Carbon Monoxide Oxidation Activity in Soil Microcosms Lalonde, Isabelle; Constant, Philippe Applied and Environmental Microbiology, Vol. 82, Issue 4 https://doi.org/10.1128/aem.03595-15	journal	December 2015
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Conrad, R. Microbiological reviews, Vol. 60, Issue 4 https://doi.org/10.1128/mr.60.4.609-640.1996	journal	January 1996
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers Helen, Decleyre; Kim, Heylen; Tytgat, Bjorn BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2465-0	journal	February 2016
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
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
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Individual Comparisons by Ranking Methods Wilcoxon, Frank Biometrics Bulletin, Vol. 1, Issue 6 https://doi.org/10.2307/3001968	journal	December 1945
Land-use influences the distribution and activity of high affinity CO-oxidizing bacteria associated to type I-coxL genotype in soil Quiza, Liliana; Lalonde, Isabelle; Guertin, Claude Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00271	journal	June 2014
One Juliet and four Romeos: VeA and its methyltransferases Sarikaya-Bayram, Ã–zlem; Palmer, Jonathan M.; Keller, Nancy Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00001	journal	January 2015
The Ecology of Acidobacteria: Moving beyond Genes and Genomes Kielak, Anna M.; Barreto, Cristine C.; Kowalchuk, George A. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00744	journal	May 2016
Challenges in Identifying and Determining the Impacts of Infection with Pestiviruses on the Herd Health of Free Ranging Cervid Populations Ridpath, Julia F.; Neill, John D. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00921	journal	June 2016
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
The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems: Role of soil microbes in global carbon cycle: carbon tracking & agro-cosystem management Gougoulias, Christos; Clark, Joanna M.; Shaw, Liz J. Journal of the Science of Food and Agriculture, Vol. 94, Issue 12 https://doi.org/10.1002/jsfa.6577	journal	March 2014
ggplot2 Wickham, Hadley Springer New York, NY https://doi.org/10.1007/978-0-387-98141-3	book	January 2009
Individual Comparisons by Ranking Methods Wilcoxon, Frank Springer Series in Statistics https://doi.org/10.1007/978-1-4612-4380-9_16	book	January 1992
Contingency in the direction and mechanics of soil organic matter responses to increased rainfall Berhe, Asmeret Asefaw; Suttle, K. Blake; Burton, Sarah D. Plant and Soil, Vol. 358, Issue 1-2 https://doi.org/10.1007/s11104-012-1156-0	journal	March 2012
Assessment of potential reference sites for evaluating the ecological status of subtropical and temperate Brazilian lotic systems using the epilithic diatom community Freitas, Núbia Cristina Weber; Heinrich, Carla Giselda; Etges, Tanise Environmental Science and Pollution Research, Vol. 28, Issue 7 https://doi.org/10.1007/s11356-020-11136-w	journal	October 2020
Diversity and composition of the North Sikkim hot spring mycobiome using a culture-independent method Das, Sayak; Roy, Goshaidas; Najar, Ishfaq Nabi Folia Microbiologica, Vol. 66, Issue 3 https://doi.org/10.1007/s12223-021-00859-z	journal	March 2021
Microbial controls on phosphate and lanthanide distributions during granite weathering and soil formation Taunton, Anne E.; Welch, Susan A.; Banfield, Jillian F. Chemical Geology, Vol. 169, Issue 3-4 https://doi.org/10.1016/S0009-2541(00)00215-1	journal	September 2000
Structural diversity of carbohydrate esterases Nakamura, Aline M.; Nascimento, Alessandro S.; Polikarpov, Igor Biotechnology Research and Innovation, Vol. 1, Issue 1 https://doi.org/10.1016/j.biori.2017.02.001	journal	January 2017
Microbial carbohydrate esterases deacetylating plant polysaccharides Biely, Peter Biotechnology Advances, Vol. 30, Issue 6 https://doi.org/10.1016/j.biotechadv.2012.04.010	journal	November 2012
The importance of grasslands for animal production and other functions: a review on management and methodological progress in the tropics Boval, M.; Dixon, R. M. animal, Vol. 6, Issue 05 https://doi.org/10.1017/S1751731112000304	journal	February 2012
Warming enhances old organic carbon decomposition through altering functional microbial communities Cheng, Lei; Zhang, Naifang; Yuan, Mengting The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.48	journal	April 2017
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
Universal sample preparation method for proteome analysis Wiśniewski, Jacek R.; Zougman, Alexandre; Nagaraj, Nagarjuna Nature Methods, Vol. 6, Issue 5 https://doi.org/10.1038/nmeth.1322	journal	April 2009
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Optimizing respiratory virus surveillance networks using uncertainty propagation Pei, Sen; Teng, Xian; Lewis, Paul Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20399-3	journal	January 2021
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
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy Sieber, Christian M. K.; Probst, Alexander J.; Sharrar, Allison Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0171-1	journal	May 2018
Genome-centric view of carbon processing in thawing permafrost Woodcroft, Ben J.; Singleton, Caitlin M.; Boyd, Joel A. Nature, Vol. 560, Issue 7716 https://doi.org/10.1038/s41586-018-0338-1	journal	July 2018
Structure and function of the global topsoil microbiome Bahram, Mohammad; Hildebrand, Falk; Forslund, Sofia K. Nature, Vol. 560, Issue 7717 https://doi.org/10.1038/s41586-018-0386-6	journal	August 2018
Long term crop rotation effect on subsequent soybean yield explained by soil and root-associated microbiomes and soil health indicators Neupane, Achal; Bulbul, Izzet; Wang, Ziyi Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-88784-6	journal	April 2021
Detecting protein and post-translational modifications in single cells with iDentification and qUantification sEparaTion (DUET) Zhang, Yandong; Sohn, Changho; Lee, Seoyeon Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-01132-8	journal	August 2020
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
Interpretation of Shotgun Proteomic Data: The Protein Inference Problem Nesvizhskii, Alexey I.; Aebersold, Ruedi Molecular & Cellular Proteomics, Vol. 4, Issue 10 https://doi.org/10.1074/mcp.R500012-MCP200	journal	July 2005
Use of Ranks in One-Criterion Variance Analysis Kruskal, William H.; Wallis, W. Allen Journal of the American Statistical Association, Vol. 47, Issue 260 https://doi.org/10.1080/01621459.1952.10483441	journal	December 1952
Hierarchical Grouping to Optimize an Objective Function Ward, Joe H. Journal of the American Statistical Association, Vol. 58, Issue 301 https://doi.org/10.1080/01621459.1963.10500845	journal	March 1963
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Bacterial molybdoenzymes: old enzymes for new purposes Leimkühler, Silke; Iobbi-Nivol, Chantal FEMS Microbiology Reviews, Vol. 40, Issue 1 https://doi.org/10.1093/femsre/fuv043	journal	October 2015
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.0955	journal	March 1997
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.955	journal	March 1997
UniProt: the Universal Protein knowledgebase Apweiler, R. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh131	journal	January 2004
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
UniProt: the universal protein knowledgebase UniProt Consortium, The Nucleic Acids Research, Vol. 46, Issue 5 https://doi.org/10.1093/nar/gky092	journal	February 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
XoxF encoding an alternative methanol dehydrogenase is widespread in coastal marine environments Taubert, Martin; Grob, Carolina; Howat, Alexandra M. Environmental Microbiology, Vol. 17, Issue 10 https://doi.org/10.1111/1462-2920.12896	journal	June 2015
An improved nonparametric lower bound of species richness via a modified good-turing frequency formula: An Improved Nonparametric Lower Bound of Species Richness Chiu, Chun-Huo; Wang, Yi-Ting; Walther, Bruno A. Biometrics, Vol. 70, Issue 3 https://doi.org/10.1111/biom.12200	journal	June 2014
Distribution and diversity of carbon monoxide-oxidizing bacteria and bulk bacterial communities across a succession gradient on a Hawaiian volcanic deposit: CO oxidizer diversity across a succession gradient Weber, C. F.; King, G. M. Environmental Microbiology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1462-2920.2010.02190.x	journal	April 2010
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Species Interactions Reverse Grassland Responses to Changing Climate Suttle, K. B.; Thomsen, M. A.; Power, M. E. Science, Vol. 315, Issue 5812 https://doi.org/10.1126/science.1136401	journal	February 2007
A global atlas of the dominant bacteria found in soil Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E. Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aap9516	journal	January 2018
Quantification of Burkholderia coxL Genes in Hawaiian Volcanic Deposits Weber, C. F.; King, G. M. Applied and Environmental Microbiology, Vol. 76, Issue 7 https://doi.org/10.1128/AEM.01861-09	journal	February 2010
Identification of Unknown Carboxydovore Bacteria Dominant in Deciduous Forest Soil via Succession of Bacterial Communities, coxL Genotypes, and Carbon Monoxide Oxidation Activity in Soil Microcosms Lalonde, Isabelle; Constant, Philippe Applied and Environmental Microbiology, Vol. 82, Issue 4 https://doi.org/10.1128/AEM.03595-15	journal	December 2015
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Conrad, R. Microbiological reviews, Vol. 60, Issue 4 https://doi.org/10.1128/MMBR.60.4.609-640.1996	journal	January 1996
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture Rajewski, Alex; Carter-House, Derreck; Stajich, Jason BMC Genomics, Vol. 22, Issue 1 https://doi.org/10.1186/s12864-021-07489-2	journal	March 2021
Apatite Replacement and Rare Earth Mobilization, Fractionation, and Fixation During Weathering Banfield, Jillian F. Clays and Clay Minerals, Vol. 37, Issue 2 https://doi.org/10.1346/CCMN.1989.0370202	journal	January 1989
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Feature Selection with the Boruta Package Kursa, Miron B.; Rudnicki, Witold R. Journal of Statistical Software, Vol. 36, Issue 11 https://doi.org/10.18637/jss.v036.i11	journal	January 2010
Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil Blazewicz, Steven J.; Schwartz, Egbert; Firestone, Mary K. Ecology, Vol. 95, Issue 5 https://doi.org/10.1890/13-1031.1	journal	May 2014
Use of Ranks in One-Criterion Variance Analysis Kruskal, William H.; Wallis, W. Allen Journal of the American Statistical Association, Vol. 47, Issue 260 https://doi.org/10.2307/2280779	journal	December 1952
Hierarchical Grouping to Optimize an Objective Function Ward, Joe H. Journal of the American Statistical Association, Vol. 58, Issue 301 https://doi.org/10.2307/2282967	journal	March 1963
On the Interpretation of χ 2 from Contingency Tables, and the Calculation of P Fisher, R. A. Journal of the Royal Statistical Society, Vol. 85, Issue 1 https://doi.org/10.2307/2340521	journal	January 1922
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
Reconstructing Rare Soil Microbial Genomes using in situ Enrichments and Metagenomics Delmont, Tom figshare https://doi.org/10.6084/m9.figshare.1320632	dataset	January 2015
Reconstructing Rare Soil Microbial Genomes using in situ Enrichments and Metagenomics Delmont, Tom figshare https://doi.org/10.6084/m9.figshare.1320632.v1	dataset	January 2015
Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil Blazewicz, Steven J.; Schwartz, Egbert; Firestone, Mary K. Figshare https://doi.org/10.6084/m9.figshare.c.3306693	collection	January 2016
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2687	journal	January 2016

Cited By (7)

Environmental Drivers of Microbial Functioning in Mediterranean Forest Soils Brunel, Caroline; Da Silva, Anne-Marie Farnet; Gros, Raphael Microbial Ecology, Vol. 80, Issue 3 https://doi.org/10.1007/s00248-020-01518-5	journal	May 2020
Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil Starr, Evan P.; Nuccio, Erin E.; Pett-Ridge, Jennifer Proceedings of the National Academy of Sciences, Vol. 116, Issue 51 https://doi.org/10.1073/pnas.1908291116	journal	November 2019
Bacterial Secondary Metabolite Biosynthetic Potential in Soil Varies with Phylum, Depth, and Vegetation Type Sharrar, Allison M.; Crits-Christoph, Alexander; Méheust, Raphaël mBio, Vol. 11, Issue 3 https://doi.org/10.1128/mbio.00416-20	journal	June 2020
Combined analysis of microbial metagenomic and metatranscriptomic sequencing data to assess in situ physiological conditions in the premature infant gut Sher, Yonatan; Olm, Matthew R.; Raveh-Sadka, Tali PLOS ONE, Vol. 15, Issue 3 https://doi.org/10.1371/journal.pone.0229537	journal	March 2020
Trophic Status Is Associated With Community Structure and Metabolic Potential of Planktonic Microbiota in Plateau Lakes Shen, Mengyuan; Li, Qi; Ren, Minglei Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02560	journal	November 2019
Additional file 1 of Metagenomics insights into responses of rhizobacteria and their alleviation role in licorice allelopathy Liu, Yang; Wang, Hao; Qian, Xun figshare https://doi.org/10.6084/m9.figshare.23036019.v1	dataset	January 2023
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