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

Shaobin Hou^*¹ , Kira S Makarova^*² , Jimmy HW Saw^*¹^,7^,8 , Pavel Senin¹^,8 , Benjamin V Ly¹ , Zhemin Zhou³ , Yan Ren³ , Jianmei Wang³ , Michael Y Galperin² , Marina V Omelchenko² , Yuri I Wolf² , Natalya Yutin² , Eugene V Koonin² , Matthew B Stott⁴ , Bruce W Mountain⁴ , Michelle A Crowe⁴ , Angela V Smirnova⁴ , Peter F Dunfield⁴^,5 , Lu Feng³ , Lei Wang³^,6 and Maqsudul Alam¹^,7

¹Advance Studies in Genomics, Proteomics and Bioinformatics, College of Natural Sciences, University of Hawaii, Keller Hall #319, Honolulu, Hawaii, 96822, USA

²National Center for Biotechnology Information, NLM, National Institutes of Health, Bethesda, Maryland, 20894, USA

³TEDA School of Biological Sciences and Biotechnology, Nankai University, Tianjin, 300457, PR China

⁴Institute of Geological and Nuclear Sciences, Wairakei Research Centre, Taupo, New Zealand

⁵Department of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, T2N 1N4, Canada

⁶Key Laboratory of Molecular Microbiology and Technology of the Ministry of Education, College of Life Sciences, Nankai University, Tianjin, 300071, PR China

⁷Department of Microbiology, University of Hawai'i, Snyder Hall, 2538 The Mall, Honolulu, Hawaii, 96822, USA

⁸B-6, Bioscience Division, MS M888, Los Alamos National Laboratory, Los Alamos, NM 87545, USA

author email corresponding author email* Contributed equally

Biology Direct 2008, 3:26doi:10.1186/1745-6150-3-26


Published:	1 July 2008

Abstract

Background

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.

Results

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.

Reviewers

This article was reviewed by John A. Fuerst, Ludmila Chistoserdova, and Radhey S. Gupta.