Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum

Dongying Wu, Jason Raymond, Martin Wu, Sourav Chatterji, Qinghu Ren, Joel E. Graham, Donald Ashley Bryant, Frank Robb, Albert Colman, Luke J. Tallon, Jonathan H. Badger, Ramana Madupu, Naomi L. Ward, Jonathan A. Eisen

Research output: Contribution to journalArticle

67 Citations (Scopus)

Abstract

In order to enrich the phylogenetic diversity represented in the available sequenced bacterial genomes and as part of an "Assembling the Tree of Life" project, we determined the genome sequence of Thermomicrobium roseum DSM 5159. T. roseum DSM 5159 is a red-pigmented, rod-shaped, Gram-negative extreme thermophile isolated from a hot spring that possesses both an atypical cell wall composition and an unusual cell membrane that is composed entirely of long-chain 1,2-diols. Its genome is composed of two circular DNA elements, one of 2,006,217 bp (referred to as the chromosome) and one of 919,596 bp (referred to as the megaplasmid). Strikingly, though few standard housekeeping genes are found on the megaplasmid, it does encode a complete system for chemotaxis including both chemosensory components and an entire flagellar apparatus. This is the first known example of a complete flagellar system being encoded on a plasmid and suggests a straightforward means for lateral transfer of flagellum-based motility. Phylogenomic analyses support the recent rRNA-based analyses that led to T. roseum being removed from the phylum Thermomicrobia and assigned to the phylum Chloroflexi. Because T. roseum is a deep-branching member of this phylum, analysis of its genome provides insights into the evolution of the Chloroflexi. In addition, even though this species is not photosynthetic, analysis of the genome provides some insight into the origins of photosynthesis in the Chloroflexi. Metabolic pathway reconstructions and experimental studies revealed new aspects of the biology of this species. For example, we present evidence that T. roseum oxidizes CO aerobically, making it the first thermophile known to do so. In addition, we propose that glycosylation of its carotenoids plays a crucial role in the adaptation of the cell membrane to this bacterium's thermophilic lifestyle. Analyses of published metagenomic sequences from two hot springs similar to the one from which this strain was isolated, show that close relatives of T. roseum DSM 5159 are present but have some key differences from the strain sequenced.

Original languageEnglish (US)
Article numbere4207
JournalPloS one
Volume4
Issue number1
DOIs
StatePublished - Jan 16 2009

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Thermomicrobium roseum
thermophilic microorganisms
Chloroflexi
Carbon Monoxide
Genes
Genome
Hot Springs
genome
Hot springs
plasmids
hot springs
Cell Membrane
Cell membranes
Bacterial Genomes
Circular DNA
Metagenomics
cell membranes
Flagella
Essential Genes
Photosynthesis

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Wu, D., Raymond, J., Wu, M., Chatterji, S., Ren, Q., Graham, J. E., ... Eisen, J. A. (2009). Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum. PloS one, 4(1), [e4207]. https://doi.org/10.1371/journal.pone.0004207
Wu, Dongying ; Raymond, Jason ; Wu, Martin ; Chatterji, Sourav ; Ren, Qinghu ; Graham, Joel E. ; Bryant, Donald Ashley ; Robb, Frank ; Colman, Albert ; Tallon, Luke J. ; Badger, Jonathan H. ; Madupu, Ramana ; Ward, Naomi L. ; Eisen, Jonathan A. / Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum. In: PloS one. 2009 ; Vol. 4, No. 1.
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author = "Dongying Wu and Jason Raymond and Martin Wu and Sourav Chatterji and Qinghu Ren and Graham, {Joel E.} and Bryant, {Donald Ashley} and Frank Robb and Albert Colman and Tallon, {Luke J.} and Badger, {Jonathan H.} and Ramana Madupu and Ward, {Naomi L.} and Eisen, {Jonathan A.}",
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Wu, D, Raymond, J, Wu, M, Chatterji, S, Ren, Q, Graham, JE, Bryant, DA, Robb, F, Colman, A, Tallon, LJ, Badger, JH, Madupu, R, Ward, NL & Eisen, JA 2009, 'Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum', PloS one, vol. 4, no. 1, e4207. https://doi.org/10.1371/journal.pone.0004207

Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum. / Wu, Dongying; Raymond, Jason; Wu, Martin; Chatterji, Sourav; Ren, Qinghu; Graham, Joel E.; Bryant, Donald Ashley; Robb, Frank; Colman, Albert; Tallon, Luke J.; Badger, Jonathan H.; Madupu, Ramana; Ward, Naomi L.; Eisen, Jonathan A.

In: PloS one, Vol. 4, No. 1, e4207, 16.01.2009.

Research output: Contribution to journalArticle

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AU - Wu, Martin

AU - Chatterji, Sourav

AU - Ren, Qinghu

AU - Graham, Joel E.

AU - Bryant, Donald Ashley

AU - Robb, Frank

AU - Colman, Albert

AU - Tallon, Luke J.

AU - Badger, Jonathan H.

AU - Madupu, Ramana

AU - Ward, Naomi L.

AU - Eisen, Jonathan A.

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N2 - In order to enrich the phylogenetic diversity represented in the available sequenced bacterial genomes and as part of an "Assembling the Tree of Life" project, we determined the genome sequence of Thermomicrobium roseum DSM 5159. T. roseum DSM 5159 is a red-pigmented, rod-shaped, Gram-negative extreme thermophile isolated from a hot spring that possesses both an atypical cell wall composition and an unusual cell membrane that is composed entirely of long-chain 1,2-diols. Its genome is composed of two circular DNA elements, one of 2,006,217 bp (referred to as the chromosome) and one of 919,596 bp (referred to as the megaplasmid). Strikingly, though few standard housekeeping genes are found on the megaplasmid, it does encode a complete system for chemotaxis including both chemosensory components and an entire flagellar apparatus. This is the first known example of a complete flagellar system being encoded on a plasmid and suggests a straightforward means for lateral transfer of flagellum-based motility. Phylogenomic analyses support the recent rRNA-based analyses that led to T. roseum being removed from the phylum Thermomicrobia and assigned to the phylum Chloroflexi. Because T. roseum is a deep-branching member of this phylum, analysis of its genome provides insights into the evolution of the Chloroflexi. In addition, even though this species is not photosynthetic, analysis of the genome provides some insight into the origins of photosynthesis in the Chloroflexi. Metabolic pathway reconstructions and experimental studies revealed new aspects of the biology of this species. For example, we present evidence that T. roseum oxidizes CO aerobically, making it the first thermophile known to do so. In addition, we propose that glycosylation of its carotenoids plays a crucial role in the adaptation of the cell membrane to this bacterium's thermophilic lifestyle. Analyses of published metagenomic sequences from two hot springs similar to the one from which this strain was isolated, show that close relatives of T. roseum DSM 5159 are present but have some key differences from the strain sequenced.

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