Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone

Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F.; Spaulding, Susan; Thomas, Brian C.; Singh, Andrea; Hettich, Robert L.; Suttle, Kenwyn B.; Probst, Alexander J.; Tringe, Susannah G.; Northen, Trent; Pan, Chongle; Banfield, Jillian F.

doi:10.7717/peerj.2687

Title: Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone

Journal Article · Tue Nov 08 00:00:00 EST 2016 · PeerJ

DOI:https://doi.org/10.7717/peerj.2687· OSTI ID:1354646

Butterfield, Cristina N. ^[1]; Li, Zhou ^[2]; Andeer, Peter F. ^[3]; Spaulding, Susan ^[1]; Thomas, Brian C. ^[1]; Singh, Andrea ^[1]; Hettich, Robert L. ^[2]; Suttle, Kenwyn B. ^[4]; Probst, Alexander J. ^[1]; Tringe, Susannah G. ^[5]; Northen, Trent ^[3]; Pan, Chongle ^[2]; Banfield, Jillian F. ^[6]

Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Sciences
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Santa Cruz, CA (United States). Dept. of Ecology and Evolutionary Biology
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Annually, half of all plant-derived carbon is added to soil where it is microbially respired to CO₂. However, understanding of the microbiology of this process is limited because most culture-independent methods cannot link metabolic processes to the organisms present, and this link to causative agents is necessary to predict the results of perturbations on the system. We collected soil samples at two sub-root depths (10–20 cm and 30–40 cm) before and after a rainfall-driven nutrient perturbation event in a Northern California grassland that experiences a Mediterranean climate. From ten samples, we reconstructed 198 metagenome-assembled genomes that represent all major phylotypes. We also quantified 6,835 proteins and 175 metabolites and showed that after the rain event the concentrations of many sugars and amino acids approach zero at the base of the soil profile. Unexpectedly, the genomes of novel members of the Gemmatimonadetes and Candidate Phylum Rokubacteria phyla encode pathways for methylotrophy. We infer that these abundant organisms contribute substantially to carbon turnover in the soil, given that methylotrophy proteins were among the most abundant proteins in the proteome. Previously undescribed Bathyarchaeota and Thermoplasmatales archaea are abundant in deeper soil horizons and are inferred to contribute appreciably to aromatic amino acid degradation. Many of the other bacteria appear to breakdown other components of plant biomass, as evidenced by the prevalence of various sugar and amino acid transporters and corresponding hydrolyzing machinery in the proteome. Overall, our work provides organism-resolved insight into the spatial distribution of bacteria and archaea whose activities combine to degrade plant-derived organics, limiting the transport of methanol, amino acids and sugars into underlying weathered rock. The new insights into the soil carbon cycle during an intense period of carbon turnover, including biogeochemical roles to previously little known soil microbes, were made possible via the combination of metagenomics, proteomics, and metabolomics.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1354646

Alternate ID(s):: OSTI ID: 1378973

Journal Information:: PeerJ, Vol. 4; ISSN 2167-8359

Publisher:: PeerJ Inc.Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 70 works

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References (104)

Exhaustive database searching for amino acid mutations in proteomes Hyatt, Doug; Pan, Chongle Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts274	journal	May 2012
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
The structure and mechanism of methanol dehydrogenase Anthony, Christopher; Williams, Paul Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1647, Issue 1-2 https://doi.org/10.1016/S1570-9639(03)00042-6	journal	April 2003
Choline: Its role in the growth of filamentous fungi and the regulation of mycelial morphology Markham, Paul; Robson, Geoffrey D.; Bainbridge, Brian W. FEMS Microbiology Letters, Vol. 104, Issue 3-4 https://doi.org/10.1111/j.1574-6968.1993.tb05872.x	journal	April 1993
Soil phosphorus depletion and shifts in plant communities change bacterial community structure in a long-term grassland management trial: Soil bacteria impacted by long-term grassland management Adair, Karen L.; Wratten, Steve; Lear, Gavin Environmental Microbiology Reports, Vol. 5, Issue 3 https://doi.org/10.1111/1758-2229.12049	journal	April 2013
Litter Decomposability -- A Neglected Component of Plant Fitness Berendse, Frank The Journal of Ecology, Vol. 82, Issue 1 https://doi.org/10.2307/2261398	journal	March 1994
Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru Biddle, J. F.; Lipp, J. S.; Lever, M. A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 10 https://doi.org/10.1073/pnas.0600035103	journal	February 2006
The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes Beck, David A. C.; McTaggart, Tami L.; Setboonsarng, Usanisa PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0102458	journal	July 2014
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
Modularity of methylotrophy, revisited: Modularity of methylotrophy, revisited Chistoserdova, Ludmila Environmental Microbiology, Vol. 13, Issue 10 https://doi.org/10.1111/j.1462-2920.2011.02464.x	journal	March 2011
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
Microbial ecology in a future climate: effects of temperature and moisture on microbial communities of two boreal fens Peltoniemi, Krista; Laiho, Raija; Juottonen, Heli FEMS Microbiology Ecology, Vol. 91, Issue 7 https://doi.org/10.1093/femsec/fiv062	journal	June 2015
KEGG for integration and interpretation of large-scale molecular data sets Kanehisa, M.; Goto, S.; Sato, Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr988	journal	November 2011
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
Root turnover as determinant of the cycling of C, N, and P in a dry heathland ecosystem Aerts, R.; Bakker, C.; De Caluwe, H. Biogeochemistry, Vol. 15, Issue 3 https://doi.org/10.1007/BF00002935	journal	January 1992
Soil characteristics more strongly influence soil bacterial communities than land-use type Kuramae, Eiko E.; Yergeau, Etienne; Wong, Lina C. FEMS Microbiology Ecology, Vol. 79, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01192.x	journal	September 2011
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
KEGG: Kyoto Encyclopedia of Genes and Genomes Ogata, H.; Goto, S.; Sato, K. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/nar/27.1.29	journal	January 1999
Bouncing Back: Plant-Associated Soil Microbes Respond Rapidly to Prairie Establishment Herzberger, Anna J.; Duncan, David S.; Jackson, Randall D. PLoS ONE, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pone.0115775	journal	December 2014
Rare earth metals are essential for methanotrophic life in volcanic mudpots: Rare earth metals essential for methanotrophic life Pol, Arjan; Barends, Thomas R. M.; Dietl, Andreas Environmental Microbiology, Vol. 16, Issue 1 https://doi.org/10.1111/1462-2920.12249	journal	September 2013
Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant Brooks, Brandon; Mueller, Ryan S.; Young, Jacque C. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00654	journal	July 2015
Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C. Current Biology, Vol. 25, Issue 6 https://doi.org/10.1016/j.cub.2015.01.014	journal	March 2015
Cross-biome metagenomic analyses of soil microbial communities and their functional attributes Fierer, N.; Leff, J. W.; Adams, B. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 52 https://doi.org/10.1073/pnas.1215210110	journal	December 2012
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
Aerobic production of methane in the sea Karl, David M.; Beversdorf, Lucas; Björkman, Karin M. Nature Geoscience, Vol. 1, Issue 7 https://doi.org/10.1038/ngeo234	journal	June 2008
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes Pruesse, Elmar; Peplies, Jörg; Glöckner, Frank Oliver Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts252	journal	May 2012
Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments Kubo, Kyoko; Lloyd, Karen G.; F. Biddle, Jennifer The ISME Journal, Vol. 6, Issue 10 https://doi.org/10.1038/ismej.2012.37	journal	May 2012
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
Linking soil bacterial biodiversity and soil carbon stability Mau, Rebecca L.; Liu, Cindy M.; Aziz, Maliha The ISME Journal, Vol. 9, Issue 6 https://doi.org/10.1038/ismej.2014.205	journal	October 2014
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
Short-term utilization of carbon by the soil microbial community under future climatic conditions in a temperate heathland Reinsch, Sabine; Michelsen, Anders; Sárossy, Zsuzsa Soil Biology and Biochemistry, Vol. 68 https://doi.org/10.1016/j.soilbio.2013.09.014	journal	January 2014
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
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
Ecology of the methylotrophic bacteria on living leaf surfaces Corpe, W. FEMS Microbiology Letters, Vol. 62, Issue 4 https://doi.org/10.1016/0378-1097(89)90248-6	journal	June 1989
The reduction of water repellency by added clay is influenced by clay and soil properties McKissock, I.; Gilkes, R. J.; Walker, E. L. Applied Clay Science, Vol. 20, Issue 4-5 https://doi.org/10.1016/S0169-1317(01)00074-6	journal	January 2002
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
MUSCLE: a multiple sequence alignment method with reduced time and space complexity Edgar, Robert C. BMC Bioinformatics, Vol. 5, Issue 1, p. 113 https://doi.org/10.1186/1471-2105-5-113	journal	August 2004
Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages: N- and C-cycling organisms in the subsurface Hug, Laura A.; Thomas, Brian C.; Sharon, Itai Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12930	journal	July 2015
SIP metagenomics identifies uncultivated Methylophilaceae as dimethylsulphide degrading bacteria in soil and lake sediment Eyice, Özge; Namura, Motonobu; Chen, Yin The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.37	journal	March 2015
Synthesis of Methylphosphonic Acid by Marine Microbes: A Source for Methane in the Aerobic Ocean Metcalf, W. W.; Griffin, B. M.; Cicchillo, R. M. Science, Vol. 337, Issue 6098 https://doi.org/10.1126/science.1219875	journal	August 2012
Soil Microbial Community Successional Patterns during Forest Ecosystem Restoration Banning, Natasha C.; Gleeson, Deirdre B.; Grigg, Andrew H. Applied and Environmental Microbiology, Vol. 77, Issue 17 https://doi.org/10.1128/AEM.00764-11	journal	July 2011
VEGAN, a package of R functions for community ecology Dixon, Philip Journal of Vegetation Science, Vol. 14, Issue 6 https://doi.org/10.1111/j.1654-1103.2003.tb02228.x	journal	April 2003
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
Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils Jones, David L.; Shannon, David; V. Murphy, Daniel Soil Biology and Biochemistry, Vol. 36, Issue 5 https://doi.org/10.1016/j.soilbio.2004.01.003	journal	May 2004
Infernal 1.0: inference of RNA alignments Nawrocki, E. P.; Kolbe, D. L.; Eddy, S. R. Bioinformatics, Vol. 25, Issue 10 https://doi.org/10.1093/bioinformatics/btp157	journal	March 2009
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
Untargeted soil metabolomics methods for analysis of extractable organic matter Swenson, Tami L.; Jenkins, Stefan; Bowen, Benjamin P. Soil Biology and Biochemistry, Vol. 80 https://doi.org/10.1016/j.soilbio.2014.10.007	journal	January 2015
Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Evans, Sarah E.; Wallenstein, Matthew D. Biogeochemistry, Vol. 109, Issue 1-3 https://doi.org/10.1007/s10533-011-9638-3	journal	September 2011
amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions: Archaeal amoA phylogeny and diversity in soils Pester, Michael; Rattei, Thomas; Flechl, Stefan Environmental Microbiology, Vol. 14, Issue 2 https://doi.org/10.1111/j.1462-2920.2011.02666.x	journal	December 2011
Reconstructing rare soil microbial genomes using in situ enrichments and metagenomics Delmont, Tom O.; Eren, A. Murat; Maccario, Lorrie Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00358	journal	April 2015
Sensitivity of soil respiration and microbial communities to altered snowfall Aanderud, Zachary T.; Jones, Stuart E.; Schoolmaster, Donald R. Soil Biology and Biochemistry, Vol. 57 https://doi.org/10.1016/j.soilbio.2012.07.022	journal	February 2013
An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics Osborn, A. Mark; Moore, Edward R. B.; Timmis, Kenneth N. Environmental Microbiology, Vol. 2, Issue 1 https://doi.org/10.1046/j.1462-2920.2000.00081.x	journal	February 2000
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
Smooth brome invasion increases rare soil bacterial species prevalence, bacterial species richness and evenness Piper, Candace L.; Siciliano, Steven D.; Winsley, Tristrom Journal of Ecology, Vol. 103, Issue 2 https://doi.org/10.1111/1365-2745.12356	journal	January 2015
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
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
Community proteogenomics reveals insights into the physiology of phyllosphere bacteria Delmotte, N.; Knief, C.; Chaffron, S. Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0905240106	journal	September 2009
Sipros/ProRata: a versatile informatics system for quantitative community proteomics Wang, Yingfeng; Ahn, Tae-Hyuk; Li, Zhou Bioinformatics, Vol. 29, Issue 16 https://doi.org/10.1093/bioinformatics/btt329	journal	June 2013
Aerobic methanol-oxidizing Bacteria â€ƒin soil Kolb, Steffen FEMS Microbiology Letters, Vol. 300, Issue 1 https://doi.org/10.1111/j.1574-6968.2009.01681.x	journal	November 2009
UniRef: comprehensive and non-redundant UniProt reference clusters Suzek, B. E.; Huang, H.; McGarvey, P. Bioinformatics, Vol. 23, Issue 10 https://doi.org/10.1093/bioinformatics/btm098	journal	March 2007
Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO ₂ concentrations : Genomic resolution of a high-CO Probst, Alexander J.; Castelle, Cindy J.; Singh, Andrea Environmental Microbiology, Vol. 19, Issue 2 https://doi.org/10.1111/1462-2920.13362	journal	July 2016
Soil Fertilization Leads to a Decline in Between-Samples Variability of Microbial Community δ13C Profiles in a Grassland Fertilization Experiment Veresoglou, Stavros D.; Thornton, Barry; Menexes, George PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0044203	journal	September 2012
Methanol oxidation by temperate soils and environmental determinants of associated methylotrophs Stacheter, Astrid; Noll, Matthias; Lee, Charles K. The ISME Journal, Vol. 7, Issue 5 https://doi.org/10.1038/ismej.2012.167	journal	December 2012
Molecular bacterial diversity of a forest soil under residue management regimes in subtropical Australia: Molecular bacterial diversity of a forest soil He, Jizheng; Xu, Zhihong; Hughes, Jane FEMS Microbiology Ecology, Vol. 55, Issue 1 https://doi.org/10.1111/j.1574-6941.2005.00006.x	journal	January 2006
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
Just add lanthanides Skovran, E.; Martinez-Gomez, N. C. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.aaa9091	journal	May 2015
Elevated temperature alters proteomic responses of individual organisms within a biofilm community Mosier, Annika C.; Li, Zhou; Thomas, Brian C. The ISME Journal, Vol. 9, Issue 1 https://doi.org/10.1038/ismej.2014.113	journal	July 2014
Aquifer environment selects for microbial species cohorts in sediment and groundwater Hug, Laura A.; Thomas, Brian C.; Brown, Christopher T. The ISME Journal, Vol. 9, Issue 8 https://doi.org/10.1038/ismej.2015.2	journal	February 2015
Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing c Radajewski, Stefan; Prosser, James I.; Nedwell, David B. Microbiology, Vol. 148, Issue 8 https://doi.org/10.1099/00221287-148-8-2331	journal	August 2002
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
Response of soil microbial biomass and enzyme activities to the transient elevation of carbon dioxide in a semi-arid grassland Kandeler, Ellen; Mosier, Arvin R.; Morgan, Jack A. Soil Biology and Biochemistry, Vol. 38, Issue 8 https://doi.org/10.1016/j.soilbio.2006.02.021	journal	August 2006
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
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic Op den Camp, Huub J. M.; Islam, Tajul; Stott, Matthew B. Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00022.x	journal	March 2009
Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide Prober, Suzanne M.; Leff, Jonathan W.; Bates, Scott T. Ecology Letters, Vol. 18, Issue 1 https://doi.org/10.1111/ele.12381	journal	November 2014
Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes White, Richard Allen; Bottos, Eric M.; Roy Chowdhury, Taniya mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00045-16	journal	June 2016
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
Methane-cycling microorganisms in soils of a high-alpine altitudinal gradient Hofmann, Katrin; Pauli, Harald; Praeg, Nadine FEMS Microbiology Ecology, Vol. 92, Issue 3 https://doi.org/10.1093/femsec/fiw009	journal	January 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 D1 https://doi.org/10.1093/nar/gkv1145	journal	November 2015
DFT Study of the Active Site of the XoxF-Type Natural, Cerium-Dependent Methanol Dehydrogenase Enzyme Bogart, Justin A.; Lewis, Andrew J.; Schelter, Eric J. Chemistry - A European Journal, Vol. 21, Issue 4 https://doi.org/10.1002/chem.201405159	journal	November 2014
Species effects on nitrogen cycling: a test with perennial grasses Wedin, David A.; Tilman, David Oecologia, Vol. 84, Issue 4 https://doi.org/10.1007/BF00328157	journal	October 1990
Microbial control over carbon cycling in soil Schimel, Joshua P.; Schaeffer, Sean M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00348	journal	January 2012
Differential Growth Responses of Soil Bacterial Taxa to Carbon Substrates of Varying Chemical Recalcitrance Goldfarb, Katherine C.; Karaoz, Ulas; Hanson, China A. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00094	journal	January 2011
Molecular Structure in Soil Humic Substances: The New View Sutton, Rebecca; Sposito, Garrison Environmental Science & Technology, Vol. 39, Issue 23 https://doi.org/10.1021/es050778q	journal	December 2005
Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland Cruz-Martínez, Karelyn; Suttle, K. Blake; Brodie, Eoin L. The ISME Journal, Vol. 3, Issue 6 https://doi.org/10.1038/ismej.2009.16	journal	March 2009
Predominant archaea in marine sediments degrade detrital proteins Lloyd, Karen G.; Schreiber, Lars; Petersen, Dorthe G. Nature, Vol. 496, Issue 7444 https://doi.org/10.1038/nature12033	journal	March 2013
Microbial uptake of low-molecular-weight organic substances out-competes sorption in soil Fischer, H.; Ingwersen, J.; Kuzyakov, Y. European Journal of Soil Science, Vol. 61, Issue 4 https://doi.org/10.1111/j.1365-2389.2010.01244.x	journal	June 2010
Scaling metagenome sequence assembly with probabilistic de Bruijn graphs Pell, J.; Hintze, A.; Canino-Koning, R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 33 https://doi.org/10.1073/pnas.1121464109	journal	July 2012
Molecular Characterization of Functional and Phylogenetic Genes from Natural Populations of Methanotrophs in Lake Sediments Costello, Andria M.; Lidstrom, Mary E. Applied and Environmental Microbiology, Vol. 65, Issue 11 https://doi.org/10.1128/AEM.65.11.5066-5074.1999	journal	November 1999
Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Muyzer, G.; de Waal, E. C.; Uitterlinden, A. G. Applied and Environmental Microbiology, Vol. 59, Issue 3 https://doi.org/10.1128/AEM.59.3.695-700.1993	journal	January 1993
Infernal 1.0: inference of RNA alignments Nawrocki, E. P.; Kolbe, D. L.; Eddy, S. R. Bioinformatics, Vol. 25, Issue 13 https://doi.org/10.1093/bioinformatics/btp326	journal	June 2009
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
VEGAN, a package of R functions for community ecology Dixon, Philip Journal of Vegetation Science, Vol. 14, Issue 6 https://doi.org/10.1658/1100-9233(2003)014[0927:vaporf]2.0.co;2	journal	January 2003
A sand fly salivary protein acts as a neutrophil chemoattractant Guimaraes-Costa, Anderson B.; Shannon, John P.; Waclawiak, Ingrid Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-23002-5	journal	May 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
Aging features of the migratory locust at physiological and transcriptional levels Guo, Siyuan; Yang, Pengcheng; Liang, Bo BMC Genomics, Vol. 22, Issue 1 https://doi.org/10.1186/s12864-021-07585-3	journal	April 2021
Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru M., Elvert,; F., Fredricks, H.; L., Sogin, M. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/5wp0-2232	text	January 2006
Community proteogenomics reveals insights into the physiology of phyllosphere bacteria Delmotte, N.; Knief, C.; Chaffron, S. National Academy of Sciences https://doi.org/10.5167/uzh-27245	text	January 2009
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
Interactome analysis reveals that lncRNA HULC promotes aerobic glycolysis through LDHA and PKM2 Wang, Chunqing; Li, Yongmei; Yan, Shuai Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16966-3	journal	June 2020
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