H2-saturation of high affinity H2-oxidizing bacteria alters the ecological niche of soil microorganisms unevenly among taxonomic groups
Abstract
Soil microbial communities are continuously exposed to H2 diffusing into the soil from the atmosphere. N2-fixing nodules represent a peculiar microniche in soil where H2 can reach concentrations up to 20,000 fold higher than in the global atmosphere (0.530 ppmv). In this study, we investigated the impact of H2 exposure on soil bacterial community structure using dynamic microcosm chambers simulating soil H2 exposure from the atmosphere and N2-fixing nodules. Biphasic kinetic parameters governing H2 oxidation activity in soil changed drastically upon elevated H2 exposure, corresponding to a slight but significant decay of high affinity H2-oxidizing bacteria population, accompanied by an enrichment or activation of microorganisms displaying low-affinity for H2. In contrast to previous studies that unveiled limited response by a few species, the relative abundance of 958 bacterial ribotypes distributed among various taxonomic groups, rather than a few distinct taxa, was influenced by H2 exposure. Furthermore, correlation networks showed important alterations of ribotype covariation in response to H2 exposure, suggesting that H2 affects microbe-microbe interactions in soil. Taken together, our results demonstrate that H2-rich environments exert a direct influence on soil H2-oxidizing bacteria in addition to indirect effects on other members of the bacterial communities.
- Authors:
-
- INRS-Institut Armand-Frappier, Laval, Quebec (Canada)
- Biomonitoring National Research Council Canada, Montreal, Quebec (Canada)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (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:
- 1378719
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PeerJ
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 3; Journal ID: ISSN 2167-8359
- Publisher:
- PeerJ Inc.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Soil; Microbial ecology; Correlation network
Citation Formats
Piché-Choquette, Sarah, Tremblay, Julien, Tringe, Susannah G., and Constant, Philippe. H2-saturation of high affinity H2-oxidizing bacteria alters the ecological niche of soil microorganisms unevenly among taxonomic groups. United States: N. p., 2016.
Web. doi:10.7717/peerj.1782.
Piché-Choquette, Sarah, Tremblay, Julien, Tringe, Susannah G., & Constant, Philippe. H2-saturation of high affinity H2-oxidizing bacteria alters the ecological niche of soil microorganisms unevenly among taxonomic groups. United States. https://doi.org/10.7717/peerj.1782
Piché-Choquette, Sarah, Tremblay, Julien, Tringe, Susannah G., and Constant, Philippe. Thu .
"H2-saturation of high affinity H2-oxidizing bacteria alters the ecological niche of soil microorganisms unevenly among taxonomic groups". United States. https://doi.org/10.7717/peerj.1782. https://www.osti.gov/servlets/purl/1378719.
@article{osti_1378719,
title = {H2-saturation of high affinity H2-oxidizing bacteria alters the ecological niche of soil microorganisms unevenly among taxonomic groups},
author = {Piché-Choquette, Sarah and Tremblay, Julien and Tringe, Susannah G. and Constant, Philippe},
abstractNote = {Soil microbial communities are continuously exposed to H2 diffusing into the soil from the atmosphere. N2-fixing nodules represent a peculiar microniche in soil where H2 can reach concentrations up to 20,000 fold higher than in the global atmosphere (0.530 ppmv). In this study, we investigated the impact of H2 exposure on soil bacterial community structure using dynamic microcosm chambers simulating soil H2 exposure from the atmosphere and N2-fixing nodules. Biphasic kinetic parameters governing H2 oxidation activity in soil changed drastically upon elevated H2 exposure, corresponding to a slight but significant decay of high affinity H2-oxidizing bacteria population, accompanied by an enrichment or activation of microorganisms displaying low-affinity for H2. In contrast to previous studies that unveiled limited response by a few species, the relative abundance of 958 bacterial ribotypes distributed among various taxonomic groups, rather than a few distinct taxa, was influenced by H2 exposure. Furthermore, correlation networks showed important alterations of ribotype covariation in response to H2 exposure, suggesting that H2 affects microbe-microbe interactions in soil. Taken together, our results demonstrate that H2-rich environments exert a direct influence on soil H2-oxidizing bacteria in addition to indirect effects on other members of the bacterial communities.},
doi = {10.7717/peerj.1782},
journal = {PeerJ},
number = 3,
volume = 4,
place = {United States},
year = {Thu Mar 10 00:00:00 EST 2016},
month = {Thu Mar 10 00:00:00 EST 2016}
}
Web of Science
Works referenced in this record:
UCHIME improves sensitivity and speed of chimera detection
journal, June 2011
- Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C.
- Bioinformatics, Vol. 27, Issue 16
Plant growth promoting H<sub>2</sub>-oxidizing bacteria as seed inoculants for cereal crops
journal, January 2012
- Golding, Amber-Leigh; Zou, Yinan; Yang, Xuan
- Agricultural Sciences, Vol. 03, Issue 04
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006
- DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
- Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
Breathing air to save energy - new insights into the ecophysiological role of high-affinity [NiFe]-hydrogenase in Streptomyces avermitilis
journal, November 2015
- Liot, Quentin; Constant, Philippe
- MicrobiologyOpen, Vol. 5, Issue 1
Genome Data Mining and Soil Survey for the Novel Group 5 [NiFe]-Hydrogenase To Explore the Diversity and Ecological Importance of Presumptive High-Affinity H 2 -Oxidizing Bacteria
journal, July 2011
- Constant, Philippe; Chowdhury, Soumitra Paul; Hesse, Laura
- Applied and Environmental Microbiology, Vol. 77, Issue 17
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
journal, August 2013
- Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
- Nature Biotechnology, Vol. 31, Issue 9
A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases
journal, March 2014
- Greening, C.; Berney, M.; Hards, K.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 11
Gas Exchange of Legume Nodules and the Regulation of Nitrogenase Activity
journal, June 1993
- Hunt, S.; Layzell, D. B.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 44, Issue 1
Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2
journal, July 2011
- Zhou, Jizhong; Deng, Ye; Luo, Feng
- mBio, Vol. 2, Issue 4
WGCNA: an R package for weighted correlation network analysis
journal, December 2008
- Langfelder, Peter; Horvath, Steve
- BMC Bioinformatics, Vol. 9, Issue 1
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival
journal, September 2015
- Greening, Chris; Biswas, Ambarish; Carere, Carlo R.
- The ISME Journal, Vol. 10, Issue 3
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
Co-localization of atmospheric H2 oxidation activity and high affinity H2-oxidizing bacteria in non-axenic soil and sterile soil amended with Streptomyces sp. PCB7
journal, September 2011
- Constant, Philippe; Chowdhury, Soumitra Paul; Hesse, Laura
- Soil Biology and Biochemistry, Vol. 43, Issue 9
Ecologically meaningful transformations for ordination of species data
journal, October 2001
- Legendre, Pierre; Gallagher, Eugene D.
- Oecologia, Vol. 129, Issue 2
H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils
journal, January 2001
- Dong, Z.; Layzell, D. B.
- Plant and Soil, Vol. 229, Issue 1, p. 1-12
Tropospheric H2 budget and the response of its soil uptake under the changing environment
journal, March 2009
- Constant, Philippe; Poissant, Laurier; Villemur, Richard
- Science of The Total Environment, Vol. 407, Issue 6
Climbing Nitrogenase: Toward a Mechanism of Enzymatic Nitrogen Fixation
journal, May 2009
- Hoffman, Brian M.; Dean, Dennis R.; Seefeldt, Lance C.
- Accounts of Chemical Research, Vol. 42, Issue 5
Microelectrode Measurements of Hydrogen Concentrations and Gradients in Legume Nodules
journal, January 1991
- Witty, J. F.
- Journal of Experimental Botany, Vol. 42, Issue 6
FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011
- Magoc, T.; Salzberg, S. L.
- Bioinformatics, Vol. 27, Issue 21
The Growth and Survival of Mycobacterium smegmatis Is Enhanced by Co-Metabolism of Atmospheric H2
journal, July 2014
- Greening, Chris; Villas-Bôas, Silas G.; Robson, Jennifer R.
- PLoS ONE, Vol. 9, Issue 7
Primer and platform effects on 16S rRNA tag sequencing
journal, August 2015
- Tremblay, Julien; Singh, Kanwar; Fern, Alison
- Frontiers in Microbiology, Vol. 6
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Three different [NiFe] hydrogenases confer metabolic flexibility in the obligate aerobe M ycobacterium smegmatis : The [NiFe]-hydrogenases of
journal, November 2013
- Berney, Michael; Greening, Chris; Hards, Kiel
- Environmental Microbiology, Vol. 16, Issue 1
The tropospheric cycle of H 2 : a critical review
journal, January 2009
- Ehhalt, D. H.; Rohrer, F.
- Tellus B: Chemical and Physical Meteorology, Vol. 61, Issue 3
Effect of hydrogen on soil bacterial community structure in two soils as determined by terminal restriction fragment length polymorphism
journal, January 2009
- Zhang, Ye; He, Xiang; Dong, Zhongmin
- Plant and Soil, Vol. 320, Issue 1-2
Occurrence, Classification, and Biological Function of Hydrogenases: An Overview
journal, October 2007
- Vignais, Paulette M.; Billoud, Bernard
- Chemical Reviews, Vol. 107, Issue 10, p. 4206-4272
Detection of a Reproducible, Single-Member Shift in Soil Bacterial Communities Exposed to Low Levels of Hydrogen
journal, January 2010
- Osborne, C. A.; Peoples, M. B.; Janssen, P. H.
- Applied and Environmental Microbiology, Vol. 76, Issue 5
Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2
journal, June 2008
- Constant, Philippe; Poissant, Laurier; Villemur, Richard
- The ISME Journal, Vol. 2, Issue 10
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009
- Robinson, M. D.; McCarthy, D. J.; Smyth, G. K.
- Bioinformatics, Vol. 26, Issue 1
Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase
journal, March 2010
- Constant, Philippe; Chowdhury, Soumitra Paul; Pratscher, Jennifer
- Environmental Microbiology, Vol. 12, Issue 3
Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation
journal, January 2012
- McCarthy, Davis J.; Chen, Yunshun; Smyth, Gordon K.
- Nucleic Acids Research, Vol. 40, Issue 10
Directions for Making Mechanical Analyses of Soils by the Hydrometer Method
journal, January 1936
- Bouyoucos, George John
- Soil Science, Vol. 42, Issue 3
Soil carbon content and relative abundance of high affinity H2-oxidizing bacteria predict atmospheric H2 soil uptake activity better than soil microbial community composition
journal, June 2015
- Khdhiri, Mondher; Hesse, Laura; Popa, Maria Elena
- Soil Biology and Biochemistry, Vol. 85
Atmospheric Hydrogen Scavenging: from Enzymes to Ecosystems
journal, December 2014
- Greening, Chris; Constant, Philippe; Hards, Kiel
- Applied and Environmental Microbiology, Vol. 81, Issue 4
Microbial activity and bacterial composition of H2-treated soils with net CO2 fixation
journal, October 2005
- Stein, Susanne; Selesi, Draženka; Schilling, Rolf
- Soil Biology and Biochemistry, Vol. 37, Issue 10
Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage
journal, November 2008
- Clarke, K. Robert; Somerfield, Paul J.; Gorley, Raymond N.
- Journal of Experimental Marine Biology and Ecology, Vol. 366, Issue 1-2
Hydrogen fertilization of soils - is this a benefit of legumes in rotation?
journal, November 2003
- Dong, Z.; Wu, L.; Kettlewell, B.
- Plant, Cell and Environment, Vol. 26, Issue 11
Soils contain two different activities for oxidation of hydrogen
journal, January 1990
- Schuler, Sibylle; Conrad, Ralf
- FEMS Microbiology Letters, Vol. 73, Issue 1
Distinct soil microbial diversity under long-term organic and conventional farming
journal, October 2014
- Hartmann, Martin; Frey, Beat; Mayer, Jochen
- The ISME Journal, Vol. 9, Issue 5
Consumption of atmospheric hydrogen during the life cycle of soil-dwelling actinobacteria: Uptake of H
journal, November 2013
- Meredith, Laura K.; Rao, Deepa; Bosak, Tanja
- Environmental Microbiology Reports, Vol. 6, Issue 3
The inability of hydrogen bacteria to utilize atmospheric hydrogen is due to threshold and affinity for hydrogen
journal, May 1983
- Conrad, Ralf; Aragno, Michel; Seiler, Wolfgang
- FEMS Microbiology Letters, Vol. 18, Issue 3
Unique Flexibility in Energy Metabolism Allows Mycobacteria to Combat Starvation and Hypoxia
journal, January 2010
- Berney, Michael; Cook, Gregory M.
- PLoS ONE, Vol. 5, Issue 1
Hydrogen Inhibition of Nitrogen Reduction by Nitrogenase in Isolated Soybean Nodule Bacteroids
journal, October 1989
- Rasche, Madeline E.; Arp, Daniel J.
- Plant Physiology, Vol. 91, Issue 2
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO).
journal, January 1996
- Conrad, R.
- Microbiological reviews, Vol. 60, Issue 4
Using QIIME to Analyze 16S rRNA Gene Sequences from Microbial Communities
journal, December 2011
- Kuczynski, Justin; Stombaugh, Jesse; Walters, William Anton
- Current Protocols in Bioinformatics, Vol. 36, Issue 1
Breathing air to save energy - new insights into the ecophysiological role of high-affinity [NiFe]-hydrogenase in Streptomyces avermitilis
journal, November 2015
- Liot, Quentin; Constant, Philippe
- MicrobiologyOpen, Vol. 5, Issue 1
Demonstration of two different H2-oxidizing activities in soil using an H2 consumption and a tritium exchange assay
journal, February 1994
- H�ring, Veronika; Conrad, Ralf
- Biology and Fertility of Soils, Vol. 17, Issue 2
Ecologically meaningful transformations for ordination of species data
journal, October 2001
- Legendre, Pierre; Gallagher, Eugene D.
- Oecologia, Vol. 129, Issue 2
Effect of hydrogen on soil bacterial community structure in two soils as determined by terminal restriction fragment length polymorphism
journal, January 2009
- Zhang, Ye; He, Xiang; Dong, Zhongmin
- Plant and Soil, Vol. 320, Issue 1-2
Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage
journal, November 2008
- Clarke, K. Robert; Somerfield, Paul J.; Gorley, Raymond N.
- Journal of Experimental Marine Biology and Ecology, Vol. 366, Issue 1-2
Tropospheric H2 budget and the response of its soil uptake under the changing environment
journal, March 2009
- Constant, Philippe; Poissant, Laurier; Villemur, Richard
- Science of The Total Environment, Vol. 407, Issue 6
Microbial activity and bacterial composition of H2-treated soils with net CO2 fixation
journal, October 2005
- Stein, Susanne; Selesi, Draženka; Schilling, Rolf
- Soil Biology and Biochemistry, Vol. 37, Issue 10
Co-localization of atmospheric H2 oxidation activity and high affinity H2-oxidizing bacteria in non-axenic soil and sterile soil amended with Streptomyces sp. PCB7
journal, September 2011
- Constant, Philippe; Chowdhury, Soumitra Paul; Hesse, Laura
- Soil Biology and Biochemistry, Vol. 43, Issue 9
Climbing Nitrogenase: Toward a Mechanism of Enzymatic Nitrogen Fixation
journal, May 2009
- Hoffman, Brian M.; Dean, Dennis R.; Seefeldt, Lance C.
- Accounts of Chemical Research, Vol. 42, Issue 5
Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2
journal, June 2008
- Constant, Philippe; Poissant, Laurier; Villemur, Richard
- The ISME Journal, Vol. 2, Issue 10
Distinct soil microbial diversity under long-term organic and conventional farming
journal, October 2014
- Hartmann, Martin; Frey, Beat; Mayer, Jochen
- The ISME Journal, Vol. 9, Issue 5
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival
journal, September 2015
- Greening, Chris; Biswas, Ambarish; Carere, Carlo R.
- The ISME Journal, Vol. 10, Issue 3
Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide
journal, March 2019
- Islam, Zahra F.; Cordero, Paul R. F.; Feng, Joanna
- The ISME Journal, Vol. 13, Issue 7
Horizontal gene transfer enables programmable gene stability in synthetic microbiota
journal, September 2022
- Wang, Teng; Weiss, Andrea; Aqeel, Ammara
- Nature Chemical Biology, Vol. 18, Issue 11
Antibody-mediated inhibition of GDF15–GFRAL activity reverses cancer cachexia in mice
journal, July 2020
- Suriben, Rowena; Chen, Michael; Higbee, Jared
- Nature Medicine, Vol. 26, Issue 8
Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain
journal, January 2020
- Raldúa, Demetrio; Casado, Marta; Prats, Eva
- Scientific Reports, Vol. 10, Issue 1
Environmental factors shape the epiphytic bacterial communities of Gracilariopsis lemaneiformis
journal, April 2021
- Pei, Pengbing; Aslam, Muhammad; Du, Hong
- Scientific Reports, Vol. 11, Issue 1
Hydrogen fertilization of soils - is this a benefit of legumes in rotation?
journal, November 2003
- Dong, Z.; Wu, L.; Kettlewell, B.
- Plant, Cell and Environment, Vol. 26, Issue 11
A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases
journal, March 2014
- Greening, C.; Berney, M.; Hards, K.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 11
UCHIME improves sensitivity and speed of chimera detection
journal, June 2011
- Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C.
- Bioinformatics, Vol. 27, Issue 16
Microelectrode Measurements of Hydrogen Concentrations and Gradients in Legume Nodules
journal, January 1991
- Witty, J. F.
- Journal of Experimental Botany, Vol. 42, Issue 6
Hydrogen Inhibition of Nitrogen Reduction by Nitrogenase in Isolated Soybean Nodule Bacteroids
journal, October 1989
- Rasche, Madeline E.; Arp, Daniel J.
- Plant Physiology, Vol. 91, Issue 2
Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase
journal, March 2010
- Constant, Philippe; Chowdhury, Soumitra Paul; Pratscher, Jennifer
- Environmental Microbiology, Vol. 12, Issue 3
The inability of hydrogen bacteria to utilize atmospheric hydrogen is due to threshold and affinity for hydrogen
journal, May 1983
- Conrad, Ralf; Aragno, Michel; Seiler, Wolfgang
- FEMS Microbiology Letters, Vol. 18, Issue 3
Soils contain two different activities for oxidation of hydrogen
journal, January 1990
- Schuler, Sibylle; Conrad, Ralf
- FEMS Microbiology Letters, Vol. 73, Issue 1
Novel, Oxygen-Insensitive Group 5 [NiFe]-Hydrogenase in Ralstonia eutropha
journal, June 2013
- Schäfer, Caspar; Friedrich, Bärbel; Lenz, Oliver
- Applied and Environmental Microbiology, Vol. 79, Issue 17
Conservation in Soil of H2 Liberated from N2 Fixation by Hup- Nodules
journal, January 1983
- La Favre, J. S.; Focht, D. D.
- Applied and Environmental Microbiology, Vol. 46, Issue 2
Mixotrophic Growth of Hydrogenomonas eutropha
journal, January 1969
- Rittenberg, Sydney C.; Goodman, Nelson S.
- Journal of Bacteriology, Vol. 98, Issue 2
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO).
journal, January 1996
- Conrad, R.
- Microbiological reviews, Vol. 60, Issue 4
Gas Exchange of Legume Nodules and the Regulation of Nitrogenase Activity
journal, June 1993
- Hunt, S.; Layzell, D. B.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 44, Issue 1
Unique Flexibility in Energy Metabolism Allows Mycobacteria to Combat Starvation and Hypoxia
journal, January 2010
- Berney, Michael; Cook, Gregory M.
- PLoS ONE, Vol. 5, Issue 1
The Growth and Survival of Mycobacterium smegmatis Is Enhanced by Co-Metabolism of Atmospheric H2
journal, July 2014
- Greening, Chris; Villas-Bôas, Silas G.; Robson, Jennifer R.
- PLoS ONE, Vol. 9, Issue 7
Primer and platform effects on 16S rRNA tag sequencing
text, January 2015
- Alison, Fern,; Feng, Chen,; Julien, Tremblay,
- The University of North Carolina at Chapel Hill University Libraries