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Title: Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms

Abstract

Abstract Land use change is one of the greatest environmental impacts worldwide, especially to tropical forests. The Amazon rainforest has been subject to particularly high rates of land use change, primarily to cattle pasture. A commonly observed response to cattle pasture establishment in the Amazon is the conversion of soil from a methane sink in rainforest, to a methane source in pasture. However, it is not known how the microorganisms that mediate methane flux are altered by land use change. Here, we use the deepest metagenomic sequencing of Amazonian soil to date to investigate differences in methane‐cycling microorganisms and their traits across rainforest and cattle pasture soils. We found that methane‐cycling microorganisms responded to land use change, with the strongest responses exhibited by methane‐consuming, rather than methane‐producing, microorganisms. These responses included a reduction in the relative abundance of methanotrophs and a significant decrease in the abundance of genes encoding particulate methane monooxygenase. We also observed compositional changes to methanotroph and methanogen communities as well as changes to methanotroph life history strategies. Our observations suggest that methane‐cycling microorganisms are vulnerable to land use change, and this vulnerability may underlie the response of methane flux to land use change in Amazon soils.

Authors:
ORCiD logo [1];  [1];  [2];  [3];  [4];  [5];  [6];  [1]
  1. Univ. of Oregon, Eugene, OR (United States)
  2. Univ. of California, Davis, CA (United States)
  3. Univ. of Massachusetts, Amherst, MA (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Utah State Univ., Logan, UT (United States)
  6. Michigan State Univ., East Lansing, MI (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1379749
Alternate Identifier(s):
OSTI ID: 1401889
Grant/Contract Number:  
AC02-05CH11231; DE‐AC02‐05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Ecology
Additional Journal Information:
Journal Volume: 26; Journal Issue: 6; Journal ID: ISSN 0962-1083
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; land use change; metagenomics; methane; microbial ecology; traits

Citation Formats

Meyer, Kyle M., Klein, Ann M., Rodrigues, Jorge L. M., Nusslein, Klaus, Tringe, Susannah G., Mirza, Babur S., Tiedje, James M., and Bohannan, Brendan J. M. Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms. United States: N. p., 2017. Web. doi:10.1111/mec.14011.
Meyer, Kyle M., Klein, Ann M., Rodrigues, Jorge L. M., Nusslein, Klaus, Tringe, Susannah G., Mirza, Babur S., Tiedje, James M., & Bohannan, Brendan J. M. Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms. United States. https://doi.org/10.1111/mec.14011
Meyer, Kyle M., Klein, Ann M., Rodrigues, Jorge L. M., Nusslein, Klaus, Tringe, Susannah G., Mirza, Babur S., Tiedje, James M., and Bohannan, Brendan J. M. Wed . "Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms". United States. https://doi.org/10.1111/mec.14011. https://www.osti.gov/servlets/purl/1379749.
@article{osti_1379749,
title = {Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms},
author = {Meyer, Kyle M. and Klein, Ann M. and Rodrigues, Jorge L. M. and Nusslein, Klaus and Tringe, Susannah G. and Mirza, Babur S. and Tiedje, James M. and Bohannan, Brendan J. M.},
abstractNote = {Abstract Land use change is one of the greatest environmental impacts worldwide, especially to tropical forests. The Amazon rainforest has been subject to particularly high rates of land use change, primarily to cattle pasture. A commonly observed response to cattle pasture establishment in the Amazon is the conversion of soil from a methane sink in rainforest, to a methane source in pasture. However, it is not known how the microorganisms that mediate methane flux are altered by land use change. Here, we use the deepest metagenomic sequencing of Amazonian soil to date to investigate differences in methane‐cycling microorganisms and their traits across rainforest and cattle pasture soils. We found that methane‐cycling microorganisms responded to land use change, with the strongest responses exhibited by methane‐consuming, rather than methane‐producing, microorganisms. These responses included a reduction in the relative abundance of methanotrophs and a significant decrease in the abundance of genes encoding particulate methane monooxygenase. We also observed compositional changes to methanotroph and methanogen communities as well as changes to methanotroph life history strategies. Our observations suggest that methane‐cycling microorganisms are vulnerable to land use change, and this vulnerability may underlie the response of methane flux to land use change in Amazon soils.},
doi = {10.1111/mec.14011},
journal = {Molecular Ecology},
number = 6,
volume = 26,
place = {United States},
year = {Wed Jan 18 00:00:00 EST 2017},
month = {Wed Jan 18 00:00:00 EST 2017}
}

Journal Article:
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Cited by: 43 works
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Figures / Tables:

Figure 1 Figure 1: The proportion of methanotrophs differs between forest and pasture. A. The proportion of methanotrophs in the methane-cycling community: methanotrophs/(methanotrophs + methanogens) calculated from rRNA organismal annotations. B. The proportion of methane monooxygenase (MMO) genes within the genes unique to methane-cycling: MMO/(MMO + MCR). MMO is methane mono-oxygenase; amore » methanotrophy gene marker. MCR is methyl-coenzyme M reductase; a methanogenesis gene marker. Significant differences between forest and pasture are denoted as: * P < 0.05.« less

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Works referenced in this record:

Exploration of community traits as ecological markers in microbial metagenomes: METAGENOMIC COMMUNITY TRAITS
journal, November 2011


Soil microbiome responses to the short-term effects of Amazonian deforestation
journal, April 2015

  • Navarrete, Acacio A.; Tsai, Siu M.; Mendes, Lucas W.
  • Molecular Ecology, Vol. 24, Issue 10
  • DOI: 10.1111/mec.13172

Consequence of forest-to-pasture conversion on CH 4 fluxes in the Brazilian Amazon Basin
journal, August 1996

  • Steudler, Paul A.; Melillo, Jerry M.; Feigl, Brigitte J.
  • Journal of Geophysical Research: Atmospheres, Vol. 101, Issue D13
  • DOI: 10.1029/96JD01551

Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities
journal, December 2012

  • Rodrigues, J. L. M.; Pellizari, V. H.; Mueller, R.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 3
  • DOI: 10.1073/pnas.1220608110

Acute impact of agriculture on high-affinity methanotrophic bacterial populations
journal, July 2008


Land-Use Change and Biogeochemical Controls of Methane Fluxes in Soils of Eastern Amazonia
journal, January 2000

  • Verchot, Louis V.; Davidson, Eric A.; Cattânio, J. Henrique
  • Ecosystems, Vol. 3, Issue 1
  • DOI: 10.1007/s100210000009

Biological Survey of a Low-Productivity Pasture in Rondônia State, Brazil
journal, September 2006


Changes in land use alter the structure of bacterial communities in Western Amazon soils
journal, May 2009

  • da C. Jesus, Ederson; Marsh, Terence L.; Tiedje, James M.
  • The ISME Journal, Vol. 3, Issue 9
  • DOI: 10.1038/ismej.2009.47

Seasonal variation of soil chemical properties and CO2 and CH4 fluxes in unfertilized and P-fertilized pastures in an Ultisol of the Brazilian Amazon
journal, June 2002


Evidence for the Existence of Three Primary Strategies in Plants and Its Relevance to Ecological and Evolutionary Theory
journal, November 1977

  • Grime, J. P.
  • The American Naturalist, Vol. 111, Issue 982
  • DOI: 10.1086/283244

Biogeochemical dynamics following land use change from forest to pasture in a humid tropical area (Rondônia, Brazil): a multi-element approach by means of XRF-spectroscopy
journal, March 2002

  • Herpin, Uwe; Cerri, Carlos C.; Conceição Santana Carvalho, Maria
  • Science of The Total Environment, Vol. 286, Issue 1-3
  • DOI: 10.1016/S0048-9697(01)00967-6

Structural and functional response of methane-consuming microbial communities to different flooding regimes in riparian soils: Response of Methane Oxidation to Flooding
journal, December 2011

  • Bodelier, Paul L. E.; Bär-Gilissen, Marie-Jose; Meima-Franke, Marion
  • Ecology and Evolution, Vol. 2, Issue 1
  • DOI: 10.1002/ece3.34

Trait-based approaches for understanding microbial biodiversity and ecosystem functioning
journal, May 2014


Correlation of Methane Production and Functional Gene Transcriptional Activity in a Peat Soil
journal, September 2009

  • Freitag, T. E.; Prosser, J. I.
  • Applied and Environmental Microbiology, Vol. 75, Issue 21
  • DOI: 10.1128/AEM.01021-09

An Ordination of the Upland Forest Communities of Southern Wisconsin
journal, February 1957

  • Bray, J. Roger; Curtis, J. T.
  • Ecological Monographs, Vol. 27, Issue 4
  • DOI: 10.2307/1942268

Long-term effects of mineral versus organic fertilizers on activity and structure of the methanotrophic community in agricultural soils
journal, October 2003


Diversity of Methanotrophic Bacteria in Tropical Upland Soils under Different Land Uses
journal, July 2005


Microbial minorities modulate methane consumption through niche partitioning
journal, June 2013

  • Bodelier, Paul LE; Meima-Franke, Marion; Hordijk, Cornelis A.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.99

Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs
journal, May 2000

  • Dedysh, S. N.; Liesack, W.; Khmelenina, V. N.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 3
  • DOI: 10.1099/00207713-50-3-955

Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies: Functional traits of methane-oxidizing bacteria
journal, August 2012


The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools
journal, January 2012


Assimilation of Carbon by Methylotrophs
book, January 1991


Global State of Biodiversity and Loss
journal, November 2003


The arcsine is asinine: the analysis of proportions in ecology
journal, January 2011

  • Warton, David I.; Hui, Francis K. C.
  • Ecology, Vol. 92, Issue 1
  • DOI: 10.1890/10-0340.1

Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

Methane dynamics regulated by microbial community response to permafrost thaw
journal, October 2014

  • McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B.
  • Nature, Vol. 514, Issue 7523
  • DOI: 10.1038/nature13798

Wide Distribution of a Novel pmoA-Like Gene Copy among Type II Methanotrophs, and Its Expression in Methylocystis Strain SC2
journal, September 2003


Effect of Afforestation and Reforestation of Pastures on the Activity and Population Dynamics of Methanotrophic Bacteria
journal, June 2007

  • Singh, B. K.; Tate, K. R.; Kolipaka, G.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00620-07

The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013

  • Overbeek, Ross; Olson, Robert; Pusch, Gordon D.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1226

Soil Carbon and Nitrogen Stocks Following Forest Clearing for Pasture in the Southwestern Brazilian Amazon
journal, November 1997


The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes
journal, September 2008


Links between plant and fungal communities across a deforestation chronosequence in the Amazon rainforest
journal, January 2014

  • Mueller, Rebecca C.; Paula, Fabiana S.; Mirza, Babur S.
  • The ISME Journal, Vol. 8, Issue 7
  • DOI: 10.1038/ismej.2013.253

Response of Free-Living Nitrogen-Fixing Microorganisms to Land Use Change in the Amazon Rainforest
journal, October 2013

  • Mirza, Babur S.; Potisap, Chotima; Nüsslein, Klaus
  • Applied and Environmental Microbiology, Vol. 80, Issue 1
  • DOI: 10.1128/AEM.02362-13

Differential Response of Acidobacteria Subgroups to Forest-to-Pasture Conversion and Their Biogeographic Patterns in the Western Brazilian Amazon
journal, December 2015

  • Navarrete, Acacio A.; Venturini, Andressa M.; Meyer, Kyle M.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01443

Evidence of Microbial Regulation of Biogeochemical Cycles from a Study on Methane Flux and Land Use Change
journal, April 2013

  • Nazaries, Loïc; Pan, Yao; Bodrossy, Levente
  • Applied and Environmental Microbiology, Vol. 79, Issue 13
  • DOI: 10.1128/AEM.00095-13

Agricultural expansion and its impacts on tropical nature
journal, February 2014

  • Laurance, William F.; Sayer, Jeffrey; Cassman, Kenneth G.
  • Trends in Ecology & Evolution, Vol. 29, Issue 2
  • DOI: 10.1016/j.tree.2013.12.001

Microbial Biogeography: From Taxonomy to Traits
journal, May 2008


Land use change alters functional gene diversity, composition and abundance in Amazon forest soil microbial communities
journal, June 2014

  • Paula, Fabiana S.; Rodrigues, Jorge L. M.; Zhou, Jizhong
  • Molecular Ecology, Vol. 23, Issue 12
  • DOI: 10.1111/mec.12786

Soil properties under Amazon forest and changes due to pasture installation in Rondônia, Brazil
journal, March 1996


Toward an Ecological Classification of soil Bacteria
journal, June 2007

  • Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
  • Ecology, Vol. 88, Issue 6
  • DOI: 10.1890/05-1839

Global Consequences of Land Use
journal, July 2005


Methanotrophic bacteria.
journal, January 1996


Characterization of Methanotrophic Bacterial Populations in Soils Showing Atmospheric Methane Uptake
journal, August 1999


Ordination
book, March 1995


Works referencing / citing this record:

Deforestation impacts network co-occurrence patterns of microbial communities in Amazon soils
journal, November 2018

  • Khan, M. A. Wadud; Bohannan, Brendan J. M.; Nüsslein, Klaus
  • FEMS Microbiology Ecology, Vol. 95, Issue 2
  • DOI: 10.1093/femsec/fiy230

Facultative methanotrophs are abundant at terrestrial natural gas seeps
journal, June 2018

  • Farhan Ul Haque, Muhammad; Crombie, Andrew T.; Ensminger, Scott A.
  • Microbiome, Vol. 6, Issue 1
  • DOI: 10.1186/s40168-018-0500-x

Novel facultative Methylocella strains are active methane consumers at terrestrial natural gas seeps
journal, October 2019

  • Farhan Ul Haque, Muhammad; Crombie, Andrew T.; Murrell, J. Colin
  • Microbiome, Vol. 7, Issue 1
  • DOI: 10.1186/s40168-019-0741-3

Use of RNA and DNA to Identify Mechanisms of Bacterial Community Homogenization
journal, September 2019


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.