The soil microbiome — from metagenomics to metaphenomics

Jansson, Janet K.; Hofmockel, Kirsten S.

doi:10.1016/J.MIB.2018.01.013

Title: The soil microbiome — from metagenomics to metaphenomics

Journal Article · 15 February 2018 · Current Opinion in Microbiology

DOI: https://doi.org/10.1016/J.MIB.2018.01.013 · OSTI ID:1437832

Jansson, Janet K. ^[1]; Hofmockel, Kirsten S. ^[2]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Iowa State Univ., Ames, IA (United States). Dept. of Ecology, Evolution and Organismal Biology

Soil microorganisms carry out important processes, including support of plant growth and cycling of carbon and other nutrients. However, the majority of soil microbes have not yet been isolated and their functions are largely unknown. Although metagenomic sequencing reveals microbial identities and functional gene information, it includes DNA from microbes with vastly varying physiological states. Therefore, metagenomics is only predictive of community functional potential. We posit that the next frontier lies in understanding the metaphenome, the product of the combined genetic potential of the microbiome and available resources. Here in this paper we describe examples of opportunities towards gaining understanding of the soil metaphenome.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

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

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1437832

Alternate ID(s):: OSTI ID: 1422511

Report Number(s):: PNNL-SA-132057; PII: S1369527417302205

Journal Information:: Current Opinion in Microbiology, Vol. 43, Issue C; ISSN 1369-5274

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 211 works

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Web of Science

References (44)

Soil and human security in the 21st century Amundson, R.; Berhe, A. A.; Hopmans, J. W. Science, Vol. 348, Issue 6235 https://doi.org/10.1126/science.1261071	journal	May 2015
Effectiveness of ecological rescue for altered soil microbial communities and functions Calderón, Kadiya; Spor, Aymé; Breuil, Marie-Christine The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.86	journal	June 2016
Quantifying global soil carbon losses in response to warming Crowther, T. W.; Todd-Brown, K. E. O.; Rowe, C. W. Nature, Vol. 540, Issue 7631 https://doi.org/10.1038/nature20150	journal	November 2016
Stabilization and destabilization of soil organic matter: mechanisms and controls Sollins, Phillip; Homann, Peter; Caldwell, Bruce A. Geoderma, Vol. 74, Issue 1-2 https://doi.org/10.1016/S0016-7061(96)00036-5	journal	November 1996
A new antibiotic kills pathogens without detectable resistance Ling, Losee L.; Schneider, Tanja; Peoples, Aaron J. Nature, Vol. 517, Issue 7535 https://doi.org/10.1038/nature14098	journal	January 2015
A communal catalogue reveals Earth’s multiscale microbial diversity Thompson, Luke R.; Sanders, Jon G.; McDonald, Daniel Nature, Vol. 551, Issue 7681 https://doi.org/10.1038/nature24621	journal	November 2017
Identification of the Core Set of Carbon-Associated Genes in a Bioenergy Grassland Soil Howe, Adina; Yang, Fan; Williams, Ryan J. PLOS ONE, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pone.0166578	journal	November 2016
A genomic perspective on stoichiometric regulation of soil carbon cycling Hartman, Wyatt H.; Ye, Rongzhong; Horwath, William R. The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.115	journal	July 2017
Schrödinger’s microbes: Tools for distinguishing the living from the dead in microbial ecosystems Emerson, Joanne B.; Adams, Rachel I.; Román, Clarisse M. Betancourt Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0285-3	journal	August 2017
The biofilm matrix Flemming, Hans-Curt; Wingender, Jost Nature Reviews Microbiology, Vol. 8, Issue 9 https://doi.org/10.1038/nrmicro2415	journal	August 2010
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
Metagenomics and the Units of Biological Organization Doolittle, W. Ford; Zhaxybayeva, Olga BioScience, Vol. 60, Issue 2 https://doi.org/10.1525/bio.2010.60.2.5	journal	February 2010
A multi-omic future for microbiome studies Jansson, Janet K.; Baker, Erin S. Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.49	journal	April 2016
Modelling the dynamic physical protection of soil organic carbon: Insights into carbon predictions and explanation of the priming effect Luo, Zhongkui; Baldock, Jeff; Wang, Enli Global Change Biology, Vol. 23, Issue 12 https://doi.org/10.1111/gcb.13793	journal	July 2017
Greatest soil microbial diversity found in micro-habitats Bach, Elizabeth M.; Williams, Ryan J.; Hargreaves, Sarah K. Soil Biology and Biochemistry, Vol. 118 https://doi.org/10.1016/j.soilbio.2017.12.018	journal	March 2018
Physical and chemical protection in hierarchical soil aggregates regulates soil carbon and nitrogen recovery in restored perennial grasslands O'Brien, Sarah L.; Jastrow, Julie D. Soil Biology and Biochemistry, Vol. 61 https://doi.org/10.1016/j.soilbio.2013.01.031	journal	June 2013
Soil aggregates as massively concurrent evolutionary incubators Rillig, Matthias C.; Muller, Ludo AH; Lehmann, Anika The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.56	journal	April 2017
Microbial interactions and community assembly at microscales Cordero, Otto X.; Datta, Manoshi S. Current Opinion in Microbiology, Vol. 31 https://doi.org/10.1016/j.mib.2016.03.015	journal	June 2016
The Potential of Metagenomic Approaches for Understanding Soil Microbial Processes Myrold, David D.; Zeglin, Lydia H.; Jansson, Janet K. Soil Science Society of America Journal, Vol. 78, Issue 1 https://doi.org/10.2136/sssaj2013.07.0287dgs	journal	January 2014
Permafrost Meta-Omics and Climate Change Mackelprang, Rachel; Saleska, Scott R.; Jacobsen, Carsten Suhr Annual Review of Earth and Planetary Sciences, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-earth-060614-105126	journal	June 2016
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
Long-term forest soil warming alters microbial communities in temperate forest soils DeAngelis, Kristen M.; Pold, Grace; TopÃ§uoÄŸlu, BegÃ¼m D. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00104	journal	February 2015
Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems López-Mondéjar, Rubén; Zühlke, Daniela; Becher, Dörte Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25279	journal	April 2016
Enzyme activities of aerobic lignocellulolytic bacteria isolated from wet tropical forest soils Woo, Hannah L.; Hazen, Terry C.; Simmons, Blake A. Systematic and Applied Microbiology, Vol. 37, Issue 1 https://doi.org/10.1016/j.syapm.2013.10.001	journal	February 2014
The ecology of the microbiome: Networks, competition, and stability Coyte, K. Z.; Schluter, J.; Foster, K. R. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aad2602	journal	November 2015
Networking in the Plant Microbiome van der Heijden, Marcel G. A.; Hartmann, Martin PLOS Biology, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pbio.1002378	journal	February 2016
Chemical communication connects soil food webs DeAngelis, Kristen M. Soil Biology and Biochemistry, Vol. 102 https://doi.org/10.1016/j.soilbio.2016.06.024	journal	November 2016
Exometabolite niche partitioning among sympatric soil bacteria Baran, Richard; Brodie, Eoin L.; Mayberry-Lewis, Jazmine Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9289	journal	September 2015
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions Jacoby, Richard; Peukert, Manuela; Succurro, Antonella Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01617	journal	September 2017
Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization Varman, Arul M.; He, Lian; Follenfant, Rhiannon Proceedings of the National Academy of Sciences, Vol. 113, Issue 40 https://doi.org/10.1073/pnas.1606043113	journal	September 2016
From DNA to FBA: How to Build Your Own Genome-Scale Metabolic Model Cuevas, Daniel A.; Edirisinghe, Janaka; Henry, Chris S. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00907	journal	June 2016
Chemical-biogeographic survey of secondary metabolism in soil Charlop-Powers, Zachary; Owen, Jeremy G.; Reddy, Boojala Vijay B. Proceedings of the National Academy of Sciences, Vol. 111, Issue 10 https://doi.org/10.1073/pnas.1318021111	journal	February 2014
Global biogeography of microbial nitrogen-cycling traits in soil Nelson, Michaeline B.; Martiny, Adam C.; Martiny, Jennifer B. H. Proceedings of the National Academy of Sciences, Vol. 113, Issue 29 https://doi.org/10.1073/pnas.1601070113	journal	July 2016
Microbial Community Metabolic Modeling: A Community Data-Driven Network Reconstruction: COMMUNITY DATA-DRIVEN METABOLIC NETWORK MODELING Henry, Christopher S.; Bernstein, Hans C.; Weisenhorn, Pamela Journal of Cellular Physiology, Vol. 231, Issue 11 https://doi.org/10.1002/jcp.25428	journal	June 2016
Integrating ion mobility spectrometry into mass spectrometry-based exposome measurements: what can it add and how far can it go? Metz, Thomas O.; Baker, Erin S.; Schymanski, Emma L. Bioanalysis, Vol. 9, Issue 1 https://doi.org/10.4155/bio-2016-0244	journal	January 2017
Metabolic interactions in microbial communities: untangling the Gordian knot Ponomarova, Olga; Patil, Kiran Raosaheb Current Opinion in Microbiology, Vol. 27 https://doi.org/10.1016/j.mib.2015.06.014	journal	October 2015
Underlying mechanisms for syntrophic metabolism of essential enzyme cofactors in microbial communities Romine, Margaret F.; Rodionov, Dmitry A.; Maezato, Yukari The ISME Journal, Vol. 11, Issue 6 https://doi.org/10.1038/ismej.2017.2	journal	February 2017
Elucidation of roles for vitamin B ₁₂ in regulation of folate, ubiquinone, and methionine metabolism Romine, Margaret F.; Rodionov, Dmitry A.; Maezato, Yukari Proceedings of the National Academy of Sciences, Vol. 114, Issue 7 https://doi.org/10.1073/pnas.1612360114	journal	January 2017
Microbiome-on-a-Chip: New Frontiers in Plant–Microbiota Research Stanley, Claire E.; van der Heijden, Marcel G. A. Trends in Microbiology, Vol. 25, Issue 8 https://doi.org/10.1016/j.tim.2017.05.001	journal	August 2017
Trophic interactions induce spatial self-organization of microbial consortia on rough surfaces Wang, Gang; Or, Dani Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06757	journal	October 2014
Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil Pepe-Ranney, Charles; Campbell, Ashley N.; Koechli, Chantal N. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00703	journal	May 2016
Capturing the genetic makeup of the active microbiome in situ Singer, Esther; Wagner, Michael; Woyke, Tanja The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.59	journal	June 2017
The past, present and future of microbiome analyses White, Richard Allen; Callister, Stephen J.; Moore, Ronald J. Nature Protocols, Vol. 11, Issue 11 https://doi.org/10.1038/nprot.2016.148	journal	September 2016

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Zones of influence for soil organic matter dynamics: A conceptual framework for data and models Cagnarini, Claudia; Blyth, Eleanor; Emmett, Bridget A. Global Change Biology, Vol. 25, Issue 12 https://doi.org/10.1111/gcb.14787	journal	August 2019
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