skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Natural Selection in Synthetic Communities Highlights the Roles of Methylococcaceae and Methylophilaceae and Suggests Differential Roles for Alternative Methanol Dehydrogenases in Methane Consumption

Journal Article · · Frontiers in Microbiology

We describe experiments that follow species dynamics and gene expression patterns in synthetic bacterial communities including species that compete for the single carbon substrate supplied, methane, and species unable to consume methane, which could only succeed through cooperative interactions. We demonstrate that these communities mostly select for two functional guilds, methanotrophs of the family Methylococcaceae and non-methanotrophic methylotrophs of the family Methylophilaceae, these taxonomic guilds outcompeting all other species included in the synthetic mix. The metatranscriptomics analysis uncovered that in both Methylococcaceae and Methylophilaceae, some of the most highly transcribed genes were the ones encoding methanol dehydrogenases (MDH). Remarkably, expression of alternative MDH genes (mxaFI versus xoxF), previously shown to be subjects to the rare Earth element switch, was found to depend on environmental conditions such as nitrogen source and methane and O2 partial pressures, and also to be species-specific. Along with the xoxF genes, genes encoding divergent cytochromes were highly expressed in both Methylophilaceae and Methylococcaceae, suggesting their function in methanol metabolism, likely encoding proteins serving as electron acceptors from XoxF enzymes. The research presented tested a synthetic community model that is much simplified compared to natural communities consuming methane, but more complex than the previously utilized two-species model. The performance of this model identifies prominent species for future synthetic ecology experiments and highlights both advantages of this approach and the challenges that it presents.

Research Organization:
Univ. of Washington, Seattle, WA (United States); Univ. of California, Oakland, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0016224; AC02-05CH11231
OSTI ID:
1510491
Journal Information:
Frontiers in Microbiology, Vol. 8; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 32 works
Citation information provided by
Web of Science

References (60)

XoxF Acts as the Predominant Methanol Dehydrogenase in the Type I Methanotroph Methylomicrobium buryatense journal February 2016
Aim, Load, Fire: The Type VI Secretion System, a Bacterial Nanoweapon journal January 2016
UCHIME improves sensitivity and speed of chimera detection journal June 2011
Lanthanide Chemistry: From Coordination in Chemical Complexes Shaping Our Technology to Coordination in Enzymes Shaping Bacterial Metabolism journal September 2016
Microorganisms and climate change: terrestrial feedbacks and mitigation options journal October 2010
Climate change and the permafrost carbon feedback journal April 2015
A metagenomic insight into freshwater methane-utilizing communities and evidence for cooperation between the Methylococcaceae and the Methylophilaceae journal January 2013
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
Molecular weaponry: diverse effectors delivered by the Type VI secretion system: Type VI secretion system effectors journal November 2015
The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes journal July 2014
The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss journal March 2012
Functional and genomic diversity of methylotrophic Rhodocyclaceae: description of Methyloversatilis discipulorum sp. nov. journal July 2015
Microbial megacities fueled by methane oxidation in a mineral spring cave journal September 2017
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy journal June 2007
Methane production, oxidation and mitigation: A mechanistic understanding and comprehensive evaluation of influencing factors journal December 2016
Modularity of methylotrophy, revisited: Modularity of methylotrophy, revisited journal March 2011
Draft Genome Sequences of Gammaproteobacterial Methanotrophs Isolated from Lake Washington Sediment: TABLE 1  journal March 2015
A Catalytic Role of XoxF1 as La3+-Dependent Methanol Dehydrogenase in Methylobacterium extorquens Strain AM1 journal November 2012
Communal Metabolism of Methane and the Rare Earth Element Switch journal June 2017
Lanthanides: New life metals? journal June 2016
Highly efficient methane biocatalysis revealed in a methanotrophic bacterium journal December 2013
Stable Isotope Probing Analysis of the Diversity and Activity of Methanotrophic Bacteria in Soils from the Canadian High Arctic journal July 2010
The 1.6Å X-ray Structure of the Unusual c-type Cytochrome, Cytochrome cL, from the Methylotrophic Bacterium Methylobacterium extorquens journal March 2006
Rare earth metals are essential for methanotrophic life in volcanic mudpots: Rare earth metals essential for methanotrophic life journal September 2013
PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference journal May 2014
UPARSE: highly accurate OTU sequences from microbial amplicon reads journal August 2013
Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils journal March 2017
Denitrification with methane as external carbon source journal June 2007
High-resolution phylogenetic microbial community profiling journal February 2016
Multiphyletic origins of methylotrophy in A lphaproteobacteria , exemplified by comparative genomics of Lake Washington isolates : Genomics of alphaproteobacterial methylotrophs journal February 2015
The Trichodesmium consortium: conserved heterotrophic co-occurrence and genomic signatures of potential interactions journal April 2017
A mathematical model of aerobic methane oxidation coupled to denitrification journal May 2017
Molecular structure and gene analysis of Ce3+-induced methanol dehydrogenase of Bradyrhizobium sp. MAFF211645 journal June 2011
Copper and cerium-regulated gene expression in Methylosinus trichosporium OB3b journal October 2017
Methane-fed microbial microcosms show differential community dynamics and pinpoint taxa involved in communal response journal October 2014
Bacterial community structure across environmental gradients in permafrost thaw ponds: methanotroph-rich ecosystems journal March 2015
Happy together: microbial communities that hook up to swap electrons journal November 2016
Molecular Characterization of Methanotrophic Isolates from Freshwater Lake Sediment journal December 2000
High-resolution metagenomics targets specific functional types in complex microbial communities journal August 2008
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies journal October 2015
Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions journal December 2016
Draft Genome of Pseudomonas sp. Strain 11/12A, Isolated from Lake Washington Sediment journal February 2015
Uptake and effect of rare earth elements on gene expression in Methylosinus trichosporium OB3b journal May 2016
Biotic Interactions in Microbial Communities as Modulators of Biogeochemical Processes: Methanotrophy as a Model System journal August 2016
Stimulation of Methanotrophic Growth in Cocultures by Cobalamin Excreted by Rhizobia journal October 2011
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal March 2016
The quinoprotein dehydrogenases for methanol and glucose journal August 2004
Genomics of Methylotrophy in Gram-Positive Methylamine-Utilizing Bacteria journal March 2015
Lanthanide-Dependent Regulation of Methanol Oxidation Systems in Methylobacterium extorquens AM1 and Their Contribution to Methanol Growth journal February 2016
MxaY regulates the lanthanide-mediated methanol dehydrogenase switch in Methylomicrobium buryatense journal January 2016
Oxygen availability is a major factor in determining the composition of microbial communities involved in methane oxidation journal January 2015
A Synthetic Ecology Perspective: How Well Does Behavior of Model Organisms in the Laboratory Predict Microbial Activities in Natural Habitats? journal June 2016
Genomes of Three Methylotrophs from a Single Niche Reveal the Genetic and Metabolic Divergence of the Methylophilaceae journal May 2011
Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community journal July 2015
Draft Genome Sequences of Five New Strains of Methylophilaceae Isolated from Lake Washington Sediment: TABLE 1 journal February 2015
Aerobic Methylotrophic Prokaryotes book January 2013
Targeted A-to-G base editing of chloroplast DNA in plants journal December 2022
Characterization and phylogenetic analysis of the complete mitochondrial genome of the pathogenic fungus Ilyonectria destructans journal February 2022
The atomic resolution structure of methanol dehydrogenase from Methylobacterium extorquens journal December 2004
Draft Genome of Janthinobacterium sp. RA13 Isolated from Lake Washington Sediment journal February 2015

Cited By (10)

Rare earth element alcohol dehydrogenases widely occur among globally distributed, numerically abundant and environmentally important microbes journal April 2019
Communal metabolism by Methylococcaceae and Methylophilaceae is driving rapid aerobic methane oxidation in sediments of a shallow seep near Elba, Italy journal July 2019
New pieces to the lanthanide puzzle journal March 2019
Lanthanide-Dependent Methylotrophs of the Family Beijerinckiaceae : Physiological and Genomic Insights journal October 2019
Genomic Evidence for Simultaneous Optimization of Transcription and Translation through Codon Variants in the pmoCAB Operon of Type Ia Methanotrophs journal July 2019
A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in Methylobacter journal January 2020
Construction and Characterization of Synthetic Bacterial Community for Experimental Ecology and Evolution journal August 2018
Lanthanide-Dependent Methanol Dehydrogenases of XoxF4 and XoxF5 Clades Are Differentially Distributed Among Methylotrophic Bacteria and They Reveal Different Biochemical Properties journal June 2018
Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR journal November 2018
Synthetic Methane-Consuming Communities from a Natural Lake Sediment journal July 2019