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Title: H2-saturation of high affinity H2-oxidizing bacteria alters the ecological niche of soil microorganisms unevenly among taxonomic groups

Journal Article · · PeerJ
DOI:https://doi.org/10.7717/peerj.1782· OSTI ID:1378719
 [1];  [2];  [3];  [1]
  1. INRS-Institut Armand-Frappier, Laval, Quebec (Canada)
  2. Biomonitoring National Research Council Canada, Montreal, Quebec (Canada)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1378719
Journal Information:
PeerJ, Vol. 4, Issue 3; ISSN 2167-8359
Publisher:
PeerJ Inc.Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 24 works
Citation information provided by
Web of Science

References (56)

UCHIME improves sensitivity and speed of chimera detection journal June 2011
Plant growth promoting H<sub>2</sub>-oxidizing bacteria as seed inoculants for cereal crops journal January 2012
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB journal July 2006
Breathing air to save energy - new insights into the ecophysiological role of high-affinity [NiFe]-hydrogenase in  Streptomyces avermitilis journal November 2015
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
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences journal August 2013
A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases journal March 2014
Gas Exchange of Legume Nodules and the Regulation of Nitrogenase Activity journal June 1993
Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2 journal July 2011
WGCNA: an R package for weighted correlation network analysis journal December 2008
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival journal September 2015
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy journal June 2007
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
Ecologically meaningful transformations for ordination of species data journal October 2001
H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils journal January 2001
Tropospheric H2 budget and the response of its soil uptake under the changing environment journal March 2009
Climbing Nitrogenase: Toward a Mechanism of Enzymatic Nitrogen Fixation journal May 2009
Microelectrode Measurements of Hydrogen Concentrations and Gradients in Legume Nodules journal January 1991
FLASH: fast length adjustment of short reads to improve genome assemblies journal September 2011
The Growth and Survival of Mycobacterium smegmatis Is Enhanced by Co-Metabolism of Atmospheric H2 journal July 2014
Primer and platform effects on 16S rRNA tag sequencing journal August 2015
Search and clustering orders of magnitude faster than BLAST journal August 2010
Three different [NiFe] hydrogenases confer metabolic flexibility in the obligate aerobe M ycobacterium smegmatis : The [NiFe]-hydrogenases of journal November 2013
The tropospheric cycle of H 2 : a critical review journal January 2009
Effect of hydrogen on soil bacterial community structure in two soils as determined by terminal restriction fragment length polymorphism journal January 2009
Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview journal October 2007
Detection of a Reproducible, Single-Member Shift in Soil Bacterial Communities Exposed to Low Levels of Hydrogen journal January 2010
Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2 journal June 2008
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase journal March 2010
Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation journal January 2012
Directions for Making Mechanical Analyses of Soils by the Hydrometer Method journal January 1936
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
Atmospheric Hydrogen Scavenging: from Enzymes to Ecosystems journal December 2014
Microbial activity and bacterial composition of H2-treated soils with net CO2 fixation journal October 2005
Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage journal November 2008
Hydrogen fertilization of soils - is this a benefit of legumes in rotation? journal November 2003
Soils contain two different activities for oxidation of hydrogen journal January 1990
Distinct soil microbial diversity under long-term organic and conventional farming journal October 2014
Consumption of atmospheric hydrogen during the life cycle of soil-dwelling actinobacteria: Uptake of H journal November 2013
The inability of hydrogen bacteria to utilize atmospheric hydrogen is due to threshold and affinity for hydrogen journal May 1983
Unique Flexibility in Energy Metabolism Allows Mycobacteria to Combat Starvation and Hypoxia journal January 2010
Hydrogen Inhibition of Nitrogen Reduction by Nitrogenase in Isolated Soybean Nodule Bacteroids journal October 1989
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). journal January 1996
Using QIIME to Analyze 16S rRNA Gene Sequences from Microbial Communities journal December 2011
Demonstration of two different H2-oxidizing activities in soil using an H2 consumption and a tritium exchange assay journal February 1994
Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide journal March 2019
Horizontal gene transfer enables programmable gene stability in synthetic microbiota journal September 2022
Antibody-mediated inhibition of GDF15–GFRAL activity reverses cancer cachexia in mice journal July 2020
Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain journal January 2020
Environmental factors shape the epiphytic bacterial communities of Gracilariopsis lemaneiformis journal April 2021
Novel, Oxygen-Insensitive Group 5 [NiFe]-Hydrogenase in Ralstonia eutropha journal June 2013
Conservation in Soil of H2 Liberated from N2 Fixation by Hup- Nodules journal January 1983
Mixotrophic Growth of Hydrogenomonas eutropha journal January 1969
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). journal January 1996
Primer and platform effects on 16S rRNA tag sequencing text January 2015