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

Abstract

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 andmore » 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.« less

Authors:
 [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);
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
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)
OSTI Identifier:
1626625
Grant/Contract Number:  
AC52-06NA25396; W81XWH0520013
Resource Type:
Accepted Manuscript
Journal Name:
Biology Direct
Additional Journal Information:
Journal Volume: 3; Journal Issue: 1; Journal ID: ISSN 1745-6150
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; horizontal gene transfer; methanol dehydrogenase; phyletic pattern; glycerate kinase; bacterial clade

Citation Formats

Hou, Shaobin, Makarova, Kira S., Saw, Jimmy HW, Senin, Pavel, Ly, Benjamin V., Zhou, Zhemin, Ren, Yan, Wang, Jianmei, Galperin, Michael Y., Omelchenko, Marina V., Wolf, Yuri I., Yutin, Natalya, Koonin, Eugene V., Stott, Matthew B., Mountain, Bruce W., Crowe, Michelle A., Smirnova, Angela V., Dunfield, Peter F., Feng, Lu, Wang, Lei, and Alam, Maqsudul. Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. United States: N. p., 2008. Web. doi:10.1186/1745-6150-3-26.
Hou, Shaobin, Makarova, Kira S., Saw, Jimmy HW, Senin, Pavel, Ly, Benjamin V., Zhou, Zhemin, Ren, Yan, Wang, Jianmei, Galperin, Michael Y., Omelchenko, Marina V., Wolf, Yuri I., Yutin, Natalya, Koonin, Eugene V., Stott, Matthew B., Mountain, Bruce W., Crowe, Michelle A., Smirnova, Angela V., Dunfield, Peter F., Feng, Lu, Wang, Lei, & Alam, Maqsudul. Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. United States. https://doi.org/10.1186/1745-6150-3-26
Hou, Shaobin, Makarova, Kira S., Saw, Jimmy HW, Senin, Pavel, Ly, Benjamin V., Zhou, Zhemin, Ren, Yan, Wang, Jianmei, Galperin, Michael Y., Omelchenko, Marina V., Wolf, Yuri I., Yutin, Natalya, Koonin, Eugene V., Stott, Matthew B., Mountain, Bruce W., Crowe, Michelle A., Smirnova, Angela V., Dunfield, Peter F., Feng, Lu, Wang, Lei, and Alam, Maqsudul. Tue . "Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia". United States. https://doi.org/10.1186/1745-6150-3-26. https://www.osti.gov/servlets/purl/1626625.
@article{osti_1626625,
title = {Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia},
author = {Hou, Shaobin and Makarova, Kira S. and Saw, Jimmy HW and Senin, Pavel and Ly, Benjamin V. and Zhou, Zhemin and Ren, Yan and Wang, Jianmei and Galperin, Michael Y. and Omelchenko, Marina V. and Wolf, Yuri I. and Yutin, Natalya and Koonin, Eugene V. and Stott, Matthew B. and Mountain, Bruce W. and Crowe, Michelle A. and Smirnova, Angela V. and Dunfield, Peter F. and Feng, Lu and Wang, Lei and Alam, Maqsudul},
abstractNote = {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.},
doi = {10.1186/1745-6150-3-26},
journal = {Biology Direct},
number = 1,
volume = 3,
place = {United States},
year = {Tue Jul 01 00:00:00 EDT 2008},
month = {Tue Jul 01 00:00:00 EDT 2008}
}

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Methylobacterium Genome Sequences: A Reference Blueprint to Investigate Microbial Metabolism of C1 Compounds from Natural and Industrial Sources
journal, May 2009


Distribution and diversity of V errucomicrobia methanotrophs in geothermal and acidic environments: Diversity of verrucomicrobial methanotrophs
journal, April 2014

  • Sharp, Christine E.; Smirnova, Angela V.; Graham, Jaime M.
  • Environmental Microbiology, Vol. 16, Issue 6
  • DOI: 10.1111/1462-2920.12454

Methanotrophic symbioses in marine invertebrates: Methanotrophic symbioses in marine invertebrates
journal, October 2009


The use of direct-fed microbials for mitigation of ruminant methane emissions: a review
journal, January 2014


Thermophilic methanotrophs: in hot pursuit
journal, August 2019

  • Houghton, Karen M.; Carere, Carlo R.; Stott, Matthew B.
  • FEMS Microbiology Ecology, Vol. 95, Issue 9
  • DOI: 10.1093/femsec/fiz125

Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic
journal, March 2009


Composition of bacterial and archaeal communities in the rumen of dromedary camel using cDNA-amplicon sequencing
journal, August 2019

  • Rabee, Alaa E.; Forster, Robert J.; Elekwachi, Chijioke O.
  • International Microbiology, Vol. 23, Issue 2
  • DOI: 10.1007/s10123-019-00093-1

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


PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference
journal, May 2014

  • Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim
  • Applied Microbiology and Biotechnology, Vol. 98, Issue 14
  • DOI: 10.1007/s00253-014-5766-8

Architecture and active site of particulate methane monooxygenase
journal, June 2012

  • Culpepper, Megen A.; Rosenzweig, Amy C.
  • Critical Reviews in Biochemistry and Molecular Biology, Vol. 47, Issue 6
  • DOI: 10.3109/10409238.2012.697865

Rare earth metals are essential for methanotrophic life in volcanic mudpots: Rare earth metals essential for methanotrophic life
journal, September 2013

  • Pol, Arjan; Barends, Thomas R. M.; Dietl, Andreas
  • Environmental Microbiology, Vol. 16, Issue 1
  • DOI: 10.1111/1462-2920.12249

Hell's Gate globin I: An acid and thermostable bacterial hemoglobin resembling mammalian neuroglobin
journal, September 2011