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Title: Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia

Journal Article · · Biology Direct
 [1];  [2];  [3];  [4];  [1];  [5];  [5];  [5];  [2];  [2];  [2];  [2];  [2];  [6];  [6];  [6];  [6];  [7];  [5];  [5] more »;  [8] « less
  1. University of Hawaii, Honolulu, HI (United States)
  2. National Institutes of Health (NIH), Bethesda, MD (United States)
  3. Univ. of Hawaii, Honolulu, HI (United States); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
  4. University of Hawaii, Honolulu, HI (United States)\; Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
  5. Nankai University, Tianjin (China)
  6. Wairakei Research Centre, Taupo (New Zealand)
  7. Wairakei Research Centre, Taupo (New Zealand); University of Calgary, AB (Canada)
  8. University of Hawaii, Honolulu, HI (United States);
+ Show Author Affiliations

The phylum Verrucomicrobia is a widespread but poorly characterized bacterial clade. Although cultivation-independent approaches detect representatives of this phylum in a wide range of environments, including soils, seawater, hot springs and human gastrointestinal tract, only few have been isolated in pure culture. We have recently reported cultivation and initial characterization of an extremely acidophilic methanotrophic member of the Verrucomicrobia, strain V4, isolated from the Hell's Gate geothermal area in New Zealand. Similar organisms were independently isolated from geothermal systems in Italy and Russia. We report the complete genome sequence of strain V4, the first one from a representative of the Verrucomicrobia. Isolate V4, initially named "Methylokorus infernorum" (and recently renamed Methylacidiphilum infernorum) is an autotrophic bacterium with a streamlined genome of ~2.3 Mbp that encodes simple signal transduction pathways and has a limited potential for regulation of gene expression. Central metabolism of M. infernorum was reconstructed almost completely and revealed highly interconnected pathways of autotrophic central metabolism and modifications of C1-utilization pathways compared to other known methylotrophs. The M. infernorum genome does not encode tubulin, which was previously discovered in bacteria of the genus Prosthecobacter, or close homologs of any other signature eukaryotic proteins. Phylogenetic analysis of ribosomal proteins and RNA polymerase subunits unequivocally supports grouping Planctomycetes, Verrucomicrobia and Chlamydiae into a single clade, the PVC superphylum, despite dramatically different gene content in members of these three groups. Comparative-genomic analysis suggests that evolution of the M. infernorum lineage involved extensive horizontal gene exchange with a variety of bacteria. The genome of M. infernorum shows apparent adaptations for existence under extremely acidic conditions including a major upward shift in the isoelectric points of proteins. Conclusion: The results of genome analysis of M. infernorum support the monophyly of the PVC superphylum. M. infernorum possesses a streamlined genome but seems to have acquired numerous genes including those for enzymes of methylotrophic pathways via horizontal gene transfer, in particular, from Proteobacteria.

Research Organization:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Department of Defense (DoD); University of Hawaii; National Institutes of Health (NIH)
Grant/Contract Number:
AC52-06NA25396; W81XWH0520013
OSTI ID:
1626625
Journal Information:
Biology Direct, Vol. 3, Issue 1; ISSN 1745-6150
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

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Prokaryotic Hydrocarbon Degraders book January 2018
Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications journal November 2011
The PVC superphylum: exceptions to the bacterial definition? journal August 2013
Editing of the gut microbiota reduces carcinogenesis in mouse models of colitis-associated colorectal cancer journal July 2019
The Methanol Dehydrogenase Gene, mxaF, as a Functional and Phylogenetic Marker for Proteobacterial Methanotrophs in Natural Environments journal February 2013
Diversity of thermophiles in a Malaysian hot spring determined using 16S rRNA and shotgun metagenome sequencing journal March 2015
Planctomycetes and eukaryotes: A case of analogy not homology: Insights & Perspectives journal August 2011
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker journal December 2015
Transitional forms between the three domains of life and evolutionary implications journal September 2011
Methanotrophs and copper journal July 2010
Modularity of methylotrophy, revisited: Modularity of methylotrophy, revisited journal March 2011
Nitrogen fixation by the verrucomicrobial methanotroph ‘Methylacidiphilum fumariolicum’ SolV journal April 2010
The Ecology of Acidophilic Microorganisms in the Corroding Concrete Sewer Environment journal April 2017
Genome Analysis of Planctomycetes Inhabiting Blades of the Red Alga Porphyra umbilicalis journal March 2016
Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph journal August 2019
Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions: Methane, microbes and models journal May 2013
Mixotrophy drives niche expansion of verrucomicrobial methanotrophs journal August 2017
Metabolic engineering of methanotrophs and its application to production of chemicals and biofuels from methane: Biofuel energy consumption-Economic growth relationship: An empirical investigation of Brazil journal August 2016
Next generation taxonomy: integrating traditional species description with the holobiont concept and genomic approaches - The in-depth characterization of a novel Euplotes species as a case study posted_content January 2019
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Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice‐covered Lakes journal July 2018
Tissue-Associated Bacterial Alterations in Rectal Carcinoma Patients Revealed by 16S rRNA Community Profiling journal December 2016
Transcriptome analysis in whole blood reveals increased microbial diversity in schizophrenia journal May 2018
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The 1st EMBO workshop on PVC bacteria—Planctomycetes–Verrucomicrobia–Chlamydiae superphylum: Exceptions to the bacterial definition? journal September 2013
Methylacidiphilum fumariolicum SolV, a thermoacidophilic ‘Knallgas’ methanotroph with both an oxygen-sensitive and -insensitive hydrogenase journal December 2016
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Thermophilic methanotrophs: in hot pursuit journal August 2019
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Composition of bacterial and archaeal communities in the rumen of dromedary camel using cDNA-amplicon sequencing journal August 2019
Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae journal July 2019
Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface journal December 2019
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High Throughput Sequencing to Detect Differences in Methanotrophic Methylococcaceae and Methylocystaceae in Surface Peat, Forest Soil, and Sphagnum Moss in Cranesville Swamp Preserve, West Virginia, USA journal April 2015

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
horizontal gene transfer
methanol dehydrogenase
phyletic pattern
glycerate kinase
bacterial clade