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Title: The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes

Journal Article · · PLoS ONE
 [1];  [1];  [1];  [1];  [1];  [2];  [3];  [2];  [1];  [1]
  1. Univ. of Washington, Seattle, WA (United States)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

We describe five novel Methylophilaceae ecotypes from a single ecological niche in Lake Washington, USA, and compare them to three previously described ecotypes, in terms of their phenotype and genome sequence divergence. Two of the ecotypes appear to represent novel genera within the Methylophilaceae. Genome-based metabolic reconstruction highlights metabolic versatility of Methylophilaceae with respect to methylotrophy and nitrogen metabolism, different ecotypes possessing different combinations of primary substrate oxidation systems (MxaFI-type methanol dehydrogenase versus XoxF-type methanol dehydrogenase; methylamine dehydrogenase versus N-methylglutamate pathway) and different potentials for denitrification (assimilatory versus respiratory nitrate reduction). By comparing pairs of closely related genomes, we uncover that site-specific recombination is the main means of genomic evolution and strain divergence, including lateral transfers of genes from both closely- and distantly related taxa. The new ecotypes and the new genomes contribute significantly to our understanding of the extent of genomic and metabolic diversity among organisms of the same family inhabiting the same ecological niche. These organisms also provide novel experimental models for studying the complexity and the function of the microbial communities active in methylotrophy.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231; SC0010556; MCB-0950183
OSTI ID:
1619062
Journal Information:
PLoS ONE, Vol. 9, Issue 7; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 45 works
Citation information provided by
Web of Science

References (44)

Bacterial Species and Speciation journal August 2001
Methylophilaceae link methanol oxidation to denitrification in freshwater lake sediment as suggested by stable isotope probing and pure culture analysis: Denitrification with methanol by Methylophilaceae journal July 2009
Genome of Methylobacillus flagellatus, Molecular Basis for Obligate Methylotrophy, and Polyphyletic Origin of Methylotrophy journal April 2007
Molecular structure and gene analysis of Ce3+-induced methanol dehydrogenase of Bradyrhizobium sp. MAFF211645 journal June 2011
A metagenomic insight into freshwater methane-utilizing communities and evidence for cooperation between the Methylococcaceae and the Methylophilaceae journal January 2013
Comparative transcriptomics in three Methylophilaceae species uncover different strategies for environmental adaptation journal January 2013
Gradients in microbial methanol uptake: productive coastal upwelling waters to oligotrophic gyres in the Atlantic Ocean journal November 2012
High-resolution metagenomics targets specific functional types in complex microbial communities journal August 2008
Towards a Genome-Based Taxonomy for Prokaryotes journal September 2005
Expressed Genome of Methylobacillus flagellatus as Defined through Comprehensive Proteomics and New Insights into Methylotrophy journal July 2010
Aerobic Methylotrophic Prokaryotes book January 2013
High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences journal March 2013
Insights into Denitrification in Methylotenera mobilis from Denitrification Pathway and Methanol Metabolism Mutants journal March 2013
Identification of Novel Methane-, Ethane-, and Propane-Oxidizing Bacteria at Marine Hydrocarbon Seeps by Stable Isotope Probing journal July 2010
Methyloversatilis universalis gen. nov., sp. nov., a novel taxon within the Betaproteobacteria represented by three methylotrophic isolates journal November 2006
Modularity of methylotrophy, revisited: Modularity of methylotrophy, revisited journal March 2011
Utility of Environmental Primers Targeting Ancient Enzymes: Methylotroph Detection in Lake Washington journal October 2004
FASconCAT: Convenient handling of data matrices journal September 2010
A Catalytic Role of XoxF1 as La3+-Dependent Methanol Dehydrogenase in Methylobacterium extorquens Strain AM1 journal November 2012
Molecular structure of La3+-induced methanol dehydrogenase-like protein in Methylobacterium radiotolerans journal May 2011
Improved conversion of methanol to single-cell protein by Methylophilus methylotrophus journal October 1980
Methylotenera mobilis gen. nov., sp. nov., an obligately methylamine-utilizing bacterium within the family Methylophilaceae journal December 2006
IMG: the integrated microbial genomes database and comparative analysis system journal December 2011
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy journal April 2011
Genomes of Three Methylotrophs from a Single Niche Reveal the Genetic and Metabolic Divergence of the Methylophilaceae journal May 2011
Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation journal August 2003
The small genome of an abundant coastal ocean methylotroph journal July 2008
Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters journal March 2013
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes journal September 2003
Analysis of two formaldehyde oxidation pathways in Methylobacillus flagellatus KT, a ribulose monophosphate cycle methylotroph journal January 2000
The Fast Changing Landscape of Sequencing Technologies and Their Impact on Microbial Genome Assemblies and Annotation journal December 2012
Synergistic metabolism of a broad range of C1 compounds in the marine methylotrophic bacterium HTCC2181: C1 metabolism in the marine isolate HTCC2181 journal October 2011
Rare earth metals are essential for methanotrophic life in volcanic mudpots: Rare earth metals essential for methanotrophic life journal September 2013
Genome sequence of strain HIMB624, a cultured representative from the OM43 clade of marine Betaproteobacteria journal March 2012
Novel methylotrophic isolates from lake sediment, description of Methylotenera versatilis sp. nov. and emended description of the genus Methylotenera journal February 2011
Methylobacterium Genome Sequences: A Reference Blueprint to Investigate Microbial Metabolism of C1 Compounds from Natural and Industrial Sources journal May 2009
Analysis of Gene Islands Involved in Methanopterin-Linked C1 Transfer Reactions Reveals New Functions and Provides Evolutionary Insights journal June 2005
Methylobacterium Genome Sequences: A Reference Blueprint to Investigate Microbial Metabolism of C1 Compounds from Natural and Industrial Sources text January 2009
Methylotrophy in a Lake: from Metagenomics to Single-Organism Physiology journal May 2011
Bacterial Populations Active in Metabolism of C1 Compounds in the Sediment of Lake Washington, a Freshwater Lake journal November 2005
Complete Genome Sequence of the Bacterium Methylovorus sp. Strain MP688, a High-Level Producer of Pyrroloquinolone Quinone journal December 2010
An Integrated Proteomics/Transcriptomics Approach Points to Oxygen as the Main Electron Sink for Methanol Metabolism in Methylotenera mobilis journal July 2011
Updating Prokaryotic Taxonomy journal September 2005

Cited By (25)

Similar but Not the Same: First Kinetic and Structural Analyses of a Methanol Dehydrogenase Containing a Europium Ion in the Active Site journal April 2018
Genome Characteristics of Two Novel Type I Methanotrophs Enriched from North Sea Sediments Containing Exclusively a Lanthanide-Dependent XoxF5-Type Methanol Dehydrogenase journal July 2016
Methylotrophs in natural habitats: current insights through metagenomics journal June 2015
Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae journal July 2019
Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions journal December 2016
Multiphyletic origins of methylotrophy in A lphaproteobacteria , exemplified by comparative genomics of Lake Washington isolates : Genomics of alphaproteobacterial methylotrophs journal February 2015
XoxF encoding an alternative methanol dehydrogenase is widespread in coastal marine environments journal June 2015
Combining metagenomics with metaproteomics and stable isotope probing reveals metabolic pathways used by a naturally occurring marine methylotroph: Metagenomics, metaproteomics and methylotrophy journal July 2015
Isolation and genomic characterization of Novimethylophilus kurashikiensis gen. nov. sp. nov., a new lanthanide-dependent methylotrophic species of Methylophilaceae: Novimethylophilus kurashikiensis gen. nov. sp. nov. journal March 2018
Just add lanthanides journal May 2015
Wide Distribution of Genes for Tetrahydromethanopterin/Methanofuran-Linked C1 Transfer Reactions Argues for Their Presence in the Common Ancestor of Bacteria and Archaea journal September 2016
Lanthanide-Dependent Methanol Dehydrogenases of XoxF4 and XoxF5 Clades Are Differentially Distributed Among Methylotrophic Bacteria and They Reveal Different Biochemical Properties journal June 2018
Anaerobic methane oxidation is an important sink for methane in the ocean's largest oxygen minimum zone journal May 2019
Lanthanides: New life metals? journal June 2016
New Methyloceanibacter diversity from North Sea sediments includes methanotroph containing solely the soluble methane monooxygenase: New Methyloceanibacter Diversity from North Sea Sediments journal September 2016
Development of a Combined Aerobic–Anoxic and Methane Oxidation Bioreactor System Using Mixed Methanotrophs and Biogas for Wastewater Denitrification journal July 2019
Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae text January 2019
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone journal January 2016
Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae. text January 2019
Draft Genomes of Two Strains of Flavobacterium Isolated from Lake Washington Sediment journal February 2015
Synthetic Methane-Consuming Communities from a Natural Lake Sediment journal July 2019
A Synthetic Ecology Perspective: How Well Does Behavior of Model Organisms in the Laboratory Predict Microbial Activities in Natural Habitats? journal June 2016
Natural Selection in Synthetic Communities Highlights the Roles of Methylococcaceae and Methylophilaceae and Suggests Differential Roles for Alternative Methanol Dehydrogenases in Methane Consumption journal December 2017
Genomics of Methylotrophy in Gram-Positive Methylamine-Utilizing Bacteria journal March 2015
Oxygen availability is a major factor in determining the composition of microbial communities involved in methane oxidation journal January 2015

Figures / Tables (6)