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Title: Back to the future of soil metagenomics

Abstract

Here, direct extraction and characterization of microbial community DNA through PCR amplicon surveys and metagenomics has revolutionized the study of environmental microbiology and microbial ecology. In particular, metagenomic analysis of nucleic acids provides direct access to the genomes of the “uncultivated majority.” Accelerated by advances in sequencing technology, microbiologists have discovered more novel phyla, classes, genera, and genes from microorganisms in the first decade and a half of the twenty-first century than since these “many very little living animalcules” were first discovered by van Leeuwenhoek (Table 1). The unsurpassed diversity of soils promises continued exploration of a range of industrial, agricultural, and environmental functions. The ability to explore soil microbial communities with increasing capacity offers the highest promise for answering many outstanding who, what, where, when, why, and with whom questions such as: Which microorganisms are linked to which soil habitats? How do microbial abundances change with changing edaphic conditions? How do microbial assemblages interact and influence one another synergistically or antagonistically? What is the full extent of soil microbial diversity, both functionally and phylogenetically? What are the dynamics of microbial communities in space and time? How sensitive are microbial communities to a changing climate? What is the role ofmore » horizontal gene transfer in the stability of microbial communities? Do highly diverse microbial communities confer resistance and resilience in soils?« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [10];  [11];  [12];  [13];  [14];  [15];  [16];  [17];  [18];  [19];  [20] more »;  [21];  [22];  [23];  [24];  [25];  [26];  [27];  [28];  [29];  [30];  [25];  [31];  [32];  [33];  [34];  [35];  [36];  [37];  [38];  [14];  [39];  [30];  [40];  [41];  [41];  [42];  [43];  [14] « less
+ Show Author Affiliations
  1. Univ. de Lyon, Ecully (France); Helmholtz Zentrum Munchen Deutsches Forschungszentrum fur Gesundheit und Umwelt (GmbH), Neuherberg (Germany)
  2. Aix-Marseille Univ., Saint-Paul-lez Durance (France)
  3. Catholic Univ. of Louvain, Louvain-la-Neuve (Belgium); Yachay Tech Univ., Urcuqui (Ecuador)
  4. Centre for Ecology and Hydrology, Oxford (United Kingdom)
  5. Institute of Microbiology of the Czech Academy of Sciences, Praha (Czech Republic)
  6. Centre National de Genotypage, Evry (France)
  7. Norwegian Univ. of Life Sciences, Aas (Norway)
  8. Aix-Marseille Univ., Saint-Paul-lez-Durance (France)
  9. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  10. The Hebrew Univ. of Jerusalem, Rehovot (Israel)
  11. Technical Research Centre of Finland, Espoo (Finland)
  12. Utrecht Univ., Utrecht (Netherlands)
  13. Univ. Nacional de La Plata, La Plata (Argentina)
  14. Swansea Univ., Swansea (United Kingdom)
  15. Univ. de Bourgogne, Dijon (France)
  16. Univ. d'Evry Val d'Essonne, Evry (France)
  17. Univ. of Ljubljana, Ljubljana (Slovenia)
  18. Univ. of East Anglia, Norwich (United Kingdom)
  19. Oregon State Univ., Corvallis, OR (United States)
  20. NALINOV, Dremil Lafage (France)
  21. Univ. of Florence, Florence (Italy)
  22. Univ. of Waterloo, Waterloo, ON (Canada)
  23. National Univ. of Ireland, Cork (Ireland); Curtin Univ., Perth, WA (Australia)
  24. National Ecological Observatory Network, Boulder, CO (United States)
  25. Bielefeld Univ., Bielefeld (Germany)
  26. Rene Rachou Research Centre - CPqRR/FIOCRUZ, Belo Horizonte (Brazil)
  27. Consejo Superior de Investigaciones Cientificas, Granada (Spain)
  28. Federal Univ. of Pampa, Sao Gabriel (Brazil)
  29. Helmholtz Zentrum Munchen Deutsches Forschungszentrum fur Gesundheit und Umwelt (GmbH), Neuherberg (Germany)
  30. Univ. of Vienna, Vienna (Austria)
  31. AIT Austrian Institute of Technology GmbH, Tulln (Austria)
  32. Sodertorn Univ., Huddinge (Sweden)
  33. Univ. of Copenhagen, Frederiksberg (Denmark)
  34. Univ. of Copenhagen, Copenhagen (Denmark)
  35. Thunen-Institute of Biodiversity, Braunschweig (Germany)
  36. Univ. of Western Ontario, London, ON (Canada)
  37. Univ. of Patras, Agrinio (Greece)
  38. Univ. of Groningen, Groningen (Netherlands)
  39. Institute of Sustainability Sciences, Zurich (Switzerland)
  40. The Univ. of Hong Kong, Hong Kong (China)
  41. Shanghai Jiao Tong Univ., Shanghai (China)
  42. Chinese Academy of Sciences (CAS), Xiamen (China)
  43. Univ. de Lyon, Ecully (France)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1337254
Report Number(s):
PNNL-SA-116061
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
58 GEOSCIENCES; 59 BASIC BIOLOGICAL SCIENCES; metagenomic; soil microbiology; terrestrial microbiology; soil ecology; microbial ecology

Citation Formats

Nesme, Joseph, Achouak, Wafa, Agathos, Spiros N., Bailey, Mark, Baldrian, Petr, Brunel, Dominique, Frostegard, Asa, Heulin, Thierry, Jansson, Janet K., Jurkevitch, Edouard, Kruus, Kristiina L., Kowalchuk, George A., Lagares, Antonio, Lappin-Scott, Hilary M., Lemanceau, Philippe, Le Paslier, Denis, Mandic-Mulec, Ines, Murrell, J. Colin, Myrold, David D., Nalin, Renaud, Nannipieri, Paolo, Neufeld, Josh D., O'Gara, Fergal, Parnell, John J., Puhler, Alfred, Pylro, Victor, Ramos, Juan L., Roesch, Luiz F. W., Schloter, Michael, Schleper, Christa, Sczyrba, Alexander, Sessitsch, Angela, Sjoling, Sara, Sorensen, Jan, Sorensen, Soren J., Tebbe, Christoph C., Topp, Edward, Tsiamis, George, van Elsas, Jan Dirk, van Keulen, Geertje, Widmer, Franco, Wagner, Michael, Zhang, Tong, Zhang, Xiaojun, Zhao, Liping, Zhu, Yong -Guan, Vogel, Timothy M., and Simonet, Pascal. Back to the future of soil metagenomics. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00073.
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Nesme, Joseph, Achouak, Wafa, Agathos, Spiros N., Bailey, Mark, Baldrian, Petr, Brunel, Dominique, Frostegard, Asa, Heulin, Thierry, Jansson, Janet K., Jurkevitch, Edouard, Kruus, Kristiina L., Kowalchuk, George A., Lagares, Antonio, Lappin-Scott, Hilary M., Lemanceau, Philippe, Le Paslier, Denis, Mandic-Mulec, Ines, Murrell, J. Colin, Myrold, David D., Nalin, Renaud, Nannipieri, Paolo, Neufeld, Josh D., O'Gara, Fergal, Parnell, John J., Puhler, Alfred, Pylro, Victor, Ramos, Juan L., Roesch, Luiz F. W., Schloter, Michael, Schleper, Christa, Sczyrba, Alexander, Sessitsch, Angela, Sjoling, Sara, Sorensen, Jan, Sorensen, Soren J., Tebbe, Christoph C., Topp, Edward, Tsiamis, George, van Elsas, Jan Dirk, van Keulen, Geertje, Widmer, Franco, Wagner, Michael, Zhang, Tong, Zhang, Xiaojun, Zhao, Liping, Zhu, Yong -Guan, Vogel, Timothy M., & Simonet, Pascal. Back to the future of soil metagenomics. United States. https://doi.org/10.3389/fmicb.2016.00073
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Nesme, Joseph, Achouak, Wafa, Agathos, Spiros N., Bailey, Mark, Baldrian, Petr, Brunel, Dominique, Frostegard, Asa, Heulin, Thierry, Jansson, Janet K., Jurkevitch, Edouard, Kruus, Kristiina L., Kowalchuk, George A., Lagares, Antonio, Lappin-Scott, Hilary M., Lemanceau, Philippe, Le Paslier, Denis, Mandic-Mulec, Ines, Murrell, J. Colin, Myrold, David D., Nalin, Renaud, Nannipieri, Paolo, Neufeld, Josh D., O'Gara, Fergal, Parnell, John J., Puhler, Alfred, Pylro, Victor, Ramos, Juan L., Roesch, Luiz F. W., Schloter, Michael, Schleper, Christa, Sczyrba, Alexander, Sessitsch, Angela, Sjoling, Sara, Sorensen, Jan, Sorensen, Soren J., Tebbe, Christoph C., Topp, Edward, Tsiamis, George, van Elsas, Jan Dirk, van Keulen, Geertje, Widmer, Franco, Wagner, Michael, Zhang, Tong, Zhang, Xiaojun, Zhao, Liping, Zhu, Yong -Guan, Vogel, Timothy M., and Simonet, Pascal. Wed . "Back to the future of soil metagenomics". United States. https://doi.org/10.3389/fmicb.2016.00073. https://www.osti.gov/servlets/purl/1337254.
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@article{osti_1337254,
title = {Back to the future of soil metagenomics},
author = {Nesme, Joseph and Achouak, Wafa and Agathos, Spiros N. and Bailey, Mark and Baldrian, Petr and Brunel, Dominique and Frostegard, Asa and Heulin, Thierry and Jansson, Janet K. and Jurkevitch, Edouard and Kruus, Kristiina L. and Kowalchuk, George A. and Lagares, Antonio and Lappin-Scott, Hilary M. and Lemanceau, Philippe and Le Paslier, Denis and Mandic-Mulec, Ines and Murrell, J. Colin and Myrold, David D. and Nalin, Renaud and Nannipieri, Paolo and Neufeld, Josh D. and O'Gara, Fergal and Parnell, John J. and Puhler, Alfred and Pylro, Victor and Ramos, Juan L. and Roesch, Luiz F. W. and Schloter, Michael and Schleper, Christa and Sczyrba, Alexander and Sessitsch, Angela and Sjoling, Sara and Sorensen, Jan and Sorensen, Soren J. and Tebbe, Christoph C. and Topp, Edward and Tsiamis, George and van Elsas, Jan Dirk and van Keulen, Geertje and Widmer, Franco and Wagner, Michael and Zhang, Tong and Zhang, Xiaojun and Zhao, Liping and Zhu, Yong -Guan and Vogel, Timothy M. and Simonet, Pascal},
abstractNote = {Here, direct extraction and characterization of microbial community DNA through PCR amplicon surveys and metagenomics has revolutionized the study of environmental microbiology and microbial ecology. In particular, metagenomic analysis of nucleic acids provides direct access to the genomes of the “uncultivated majority.” Accelerated by advances in sequencing technology, microbiologists have discovered more novel phyla, classes, genera, and genes from microorganisms in the first decade and a half of the twenty-first century than since these “many very little living animalcules” were first discovered by van Leeuwenhoek (Table 1). The unsurpassed diversity of soils promises continued exploration of a range of industrial, agricultural, and environmental functions. The ability to explore soil microbial communities with increasing capacity offers the highest promise for answering many outstanding who, what, where, when, why, and with whom questions such as: Which microorganisms are linked to which soil habitats? How do microbial abundances change with changing edaphic conditions? How do microbial assemblages interact and influence one another synergistically or antagonistically? What is the full extent of soil microbial diversity, both functionally and phylogenetically? What are the dynamics of microbial communities in space and time? How sensitive are microbial communities to a changing climate? What is the role of horizontal gene transfer in the stability of microbial communities? Do highly diverse microbial communities confer resistance and resilience in soils?},
doi = {10.3389/fmicb.2016.00073},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Wed Feb 10 00:00:00 EST 2016},
month = {Wed Feb 10 00:00:00 EST 2016}
}
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Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.3389/fmicb.2016.00073
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Cited by: 84 works
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Figures / Tables:

TABLE 1 TABLE 1: Timeline of advances in genomic and metagenomic methods and large-scale projects focusing on soil biodiversity analysis: cracking the soil black box.
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Works referenced in this record:

TerraGenome: a consortium for the sequencing of a soil metagenome
journal, April 2009

  • Vogel, Timothy M.; Simonet, Pascal; Jansson, Janet K.
  • Nature Reviews Microbiology, Vol. 7, Issue 4
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Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products
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Tackling soil diversity with the assembly of large, complex metagenomes
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  • Howe, Adina Chuang; Jansson, Janet K.; Malfatti, Stephanie A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 13
  • DOI: 10.1073/pnas.1402564111

Ecology and exploration of the rare biosphere
journal, March 2015

  • Lynch, Michael D. J.; Neufeld, Josh D.
  • Nature Reviews Microbiology, Vol. 13, Issue 4
  • DOI: 10.1038/nrmicro3400

Soil eukaryotic functional diversity, a metatranscriptomic approach
journal, September 2007

  • Bailly, Julie; Fraissinet-Tachet, Laurence; Verner, Marie-Christine
  • The ISME Journal, Vol. 1, Issue 7
  • DOI: 10.1038/ismej.2007.68

Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes
journal, March 2015

  • Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel
  • Nature, Vol. 521, Issue 7551
  • DOI: 10.1038/nature14238

Comparative Metagenomics of Microbial Communities
journal, April 2005

Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes
journal, May 2013

  • Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam
  • Nature Biotechnology, Vol. 31, Issue 6
  • DOI: 10.1038/nbt.2579

Brazilian Microbiome Project: Revealing the Unexplored Microbial Diversity—Challenges and Prospects
journal, October 2013

  • Pylro, Victor Satler; Roesch, Luiz Fernando Wurdig; Ortega, José Miguel
  • Microbial Ecology, Vol. 67, Issue 2
  • DOI: 10.1007/s00248-013-0302-4

Meeting Report: The Terabase Metagenomics Workshop and the Vision of an Earth Microbiome Project
journal, January 2010

  • Gilbert, Jack A.; Meyer, Folker; Antonopoulos, Dion
  • Standards in Genomic Sciences, Vol. 3, Issue 3
  • DOI: 10.4056/sigs.1433550

Structure, fluctuation and magnitude of a natural grassland soil metagenome
journal, February 2012

  • Delmont, Tom O.; Prestat, Emmanuel; Keegan, Kevin P.
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2011.197

Archaea predominate among ammonia-oxidizing prokaryotes in soils
journal, August 2006

Mastering methodological pitfalls for surviving the metagenomic jungle: Prospects & Overviews
journal, June 2013

Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
journal, October 2013

The Earth Microbiome project: successes and aspirations
journal, August 2014

Detection of micro-organisms in soil after in situ hybridization with rRNA-targeted, fluorescently labelled oligonucleotides
journal, May 1992

Characterization of Denitrification Gene Clusters of Soil Bacteria via a Metagenomic Approach
journal, November 2008

  • Demaneche, S.; Philippot, L.; David, M. M.
  • Applied and Environmental Microbiology, Vol. 75, Issue 2
  • DOI: 10.1128/AEM.01706-08

Isolation of bacterial DNA from soil
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Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Reconstructing rare soil microbial genomes using in situ enrichments and metagenomics
journal, April 2015

Brazilian Microbiome Project: Revealing the Unexplored Microbial Diversity—Challenges and Prospects
journal, October 2013

  • Pylro, Victor Satler; Roesch, Luiz Fernando Wurdig; Ortega, José Miguel
  • Microbial Ecology, Vol. 67, Issue 2
  • DOI: 10.1007/s00248-013-0302-4

Isolation of bacterial DNA from soil
journal, January 1980

Soil eukaryotic functional diversity, a metatranscriptomic approach
journal, September 2007

  • Bailly, Julie; Fraissinet-Tachet, Laurence; Verner, Marie-Christine
  • The ISME Journal, Vol. 1, Issue 7
  • DOI: 10.1038/ismej.2007.68

Structure, fluctuation and magnitude of a natural grassland soil metagenome
journal, February 2012

  • Delmont, Tom O.; Prestat, Emmanuel; Keegan, Kevin P.
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2011.197

Archaea predominate among ammonia-oxidizing prokaryotes in soils
journal, August 2006

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes
journal, March 2015

  • Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel
  • Nature, Vol. 521, Issue 7551
  • DOI: 10.1038/nature14238

Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes
journal, May 2013

  • Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam
  • Nature Biotechnology, Vol. 31, Issue 6
  • DOI: 10.1038/nbt.2579

Ecology and exploration of the rare biosphere
journal, March 2015

  • Lynch, Michael D. J.; Neufeld, Josh D.
  • Nature Reviews Microbiology, Vol. 13, Issue 4
  • DOI: 10.1038/nrmicro3400

Tackling soil diversity with the assembly of large, complex metagenomes
journal, March 2014

  • Howe, Adina Chuang; Jansson, Janet K.; Malfatti, Stephanie A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 13
  • DOI: 10.1073/pnas.1402564111

Detection of micro-organisms in soil after in situ hybridization with rRNA-targeted, fluorescently labelled oligonucleotides
journal, May 1992

Comparative Metagenomics of Microbial Communities
journal, April 2005

Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
journal, October 2013

High diversity in DNA of soil bacteria.
journal, January 1990

The Earth Microbiome project: successes and aspirations
journal, August 2014

Reconstructing rare soil microbial genomes using in situ enrichments and metagenomics
journal, April 2015

Meeting Report: The Terabase Metagenomics Workshop and the Vision of an Earth Microbiome Project
journal, January 2010

  • Gilbert, Jack A.; Meyer, Folker; Antonopoulos, Dion
  • Standards in Genomic Sciences, Vol. 3, Issue 3
  • DOI: 10.4056/sigs.1433550
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    Muddy Waters: Unintentional Consequences of Blue Carbon Research Obscure Our Understanding of Organic Carbon Dynamics in Seagrass Ecosystems
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    Advancements in Microbial Genome Sequencing and Microbial Community Characterization
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    New approaches for metagenome assembly with short reads
    journal, February 2019

    • Ayling, Martin; Clark, Matthew D.; Leggett, Richard M.
    • Briefings in Bioinformatics, Vol. 21, Issue 2
    • DOI: 10.1093/bib/bbz020

    Analysis of soil eDNA functional genes: potential to increase profitability and sustainability of pastoral agriculture
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    book, January 2017

    Phylogenetic diversity and metabolic potential of microbiome of natural healing clay from Chamliyal (J&K)
    journal, July 2018

    Microbial indicators for soil quality
    journal, October 2017

    • Schloter, Michael; Nannipieri, Paolo; Sørensen, Søren J.
    • Biology and Fertility of Soils, Vol. 54, Issue 1
    • DOI: 10.1007/s00374-017-1248-3

    Biophysical processes supporting the diversity of microbial life in soil
    journal, August 2017

    Biophysical processes supporting the diversity of microbial life in soil
    text, January 2017

    Biophysical processes supporting the diversity of microbial life in soil
    journal, August 2017

    Trees, fungi and bacteria: tripartite metatranscriptomics of a root microbiome responding to soil contamination
    journal, March 2018

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