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. 2020 Aug 13;9(33):e00608-20. doi: 10.1128/MRA.00608-20

Draft Genome Sequence of Thermanaeromonas sp. Strain C210, Isolated in the Presence of Carbon Monoxide

Masao Inoue a, Ayumi Tanimura a, Yuto Fukuyama a, Suguru Okunishi b, Hiroto Maeda b, Takashi Yoshida a, Yoshihiko Sako a,
Editor: Frank J Stewartc
PMCID: PMC7427185  PMID: 32817147

The genus Thermanaeromonas comprises two species of thermophilic, strictly anaerobic, spore-forming bacteria. Here, we report the draft genome sequence of Thermanaeromonas sp. strain C210, which was first isolated in the presence of carbon monoxide. The genome sequence provides insight into carbon monoxide-dependent metabolism for members of the genus Thermanaeromonas.

ABSTRACT

The genus Thermanaeromonas comprises two species of thermophilic, strictly anaerobic, spore-forming bacteria. Here, we report the draft genome sequence of Thermanaeromonas sp. strain C210, which was first isolated in the presence of carbon monoxide. The genome sequence provides insight into carbon monoxide-dependent metabolism for members of the genus Thermanaeromonas.

ANNOUNCEMENT

The genus Thermanaeromonas is a member of the family Thermoanaerobacteraceae, class Clostridia, phylum Firmicutes. In this genus, two species, T. toyohensis and T. burensis, are described as thermophilic, strictly anaerobic, spore-forming, thiosulfate-reducing bacteria (1, 2); however, genomic information is available only for T. toyohensis strain ToBET (GenBank accession number LT838272). Here, we report the draft genome sequence of Thermanaeromonas sp. strain C210, which was first isolated from marine sediment in the presence of carbon monoxide (CO).

The sediment was collected from Yamagawa Bay, Ata Caldera, in Kagoshima Prefecture, Japan (31°12′43″N, 130°38′18″E; depth, 10 to 11 cm; elevation, −46 m). Strain C210 was enriched, isolated, and cultivated for genome sequencing at 65°C under 100 % CO gas in hypotonic artificial seawater (hASW) medium, as described previously (3).

Genomic DNA extraction, library preparation, sequencing, and genome assembly were carried out as described previously (4, 5). Genomic DNA was extracted using the DNeasy blood and tissue kit (Qiagen, Hilden, Germany); then, a DNA library was prepared using the Nextera mate pair library preparation kit (Illumina, San Diego, CA). Sequencing was performed on the Illumina MiSeq instrument with the MiSeq reagent kit v.3 (600 cycles), which generated 4,827,688 paired-end reads. Quality trimming and adapter removal were performed using Trimmomatic v.0.3.6 (ILLUMINACLIP:2:30:10 LEADING:3 TRAILING:3 SLIDINGWINDOW:4:15 MINLEN:30) (6). Mate pair reads were selected and junction adapters were trimmed using NxTrim v.0.4.1 (7). De novo genome assembly was performed with SPAdes v.3.13.0 with the option “--hqmp” (8), using the filtered 2,314,613 mate pair reads. The assembled scaffolds were quality controlled using BWA v.0.7.17 (9), SAMtools v.0.1.19 (10), and NxRepair v.0.13 (11). Annotation was performed with the DFAST server v.1.0.2 (12). Genomic comparison was performed using OAT v.0.93.1 (13), GGDC v.2.1 (14), and BLAST (15). Default parameters were used for all software unless otherwise noted.

The draft genome was assembled into 19 scaffolds with an N50 value of 658,646 bp, an average coverage of 278×, a total length of 2,676,999 bp, and an average G+C content of 57.1%. The numbers of predicted protein-coding genes, rRNAs, and tRNAs were 2,618, 6, and 48, respectively. The average nucleotide identity and digital DNA-DNA hybridization to T. toyohensis ToBET were 71.4% and 24.0%, respectively. The sequence identities of the 16S rRNA genes to T. toyohensis ToBET and T. burensis IA106T were 92.7% and 98.7 to 98.8%, respectively. These results suggest that strain C210 is a member of the genus Thermanaeromonas.

We identified three genes encoding anaerobic CO dehydrogenase (CODH), one with a gene cluster for hydrogen-evolving hydrogenase (TAMC210_016640 to TAMC210_16840), another with a gene cluster for acetyl-coenzyme A (CoA) synthase (TAMC210_19150 to TAMC210_19280), and the last with genes for CooF and ferredoxin-NAD(P)H oxidoreductase (TAMC210_04640 to TAMC210_04620). The amino acid sequence identities of these three CODHs of strain C210 to their orthologs in T. toyohensis ToBET were >85%. These results were consistent with the fact that strain C210 was enriched in the presence of CO and with recent bioinformatics-based analyses showing that the genus Thermanaeromonas includes possible hydrogen-evolving, CO-oxidizing bacteria (1618).

Data availability.

This draft genome sequence was deposited in GenBank under accession number BLWF00000000.1. The raw reads were deposited in SRA under accession number DRA010181.

ACKNOWLEDGMENTS

This work was supported by JSPS KAKENHI grant number JP16H06381 (to Y.S.).

We thank Tatsuki Oguro and Yusuke Ogami from Kyoto University and the crew of the vessel Nansei-Maru at Kagoshima University for providing technical assistance with the sampling of marine sediments. We also thank Yusuke Ogami and Taiki Hino from Kyoto University for their technical assistance in DNA sequencing. Part of the computational analysis was performed at the Super Computer System, Institute for Chemical Research, Kyoto University.

M.I., T.Y., and Y.S. designed the work and drafted the paper. S.O. and H.M. conducted the sampling of marine sediments. A.T. and Y.F. isolated and maintained the strain. M.I. performed the genome sequencing and data analysis. All authors edited and approved the paper.

We declare no conflicts of interest with regard to the contents of this article.

REFERENCES

  • 1.Mori K, Hanada S, Maruyama A, Marumo K. 2002. Thermanaeromonas toyohensis gen. nov., sp. nov., a novel thermophilic anaerobe isolated from a subterranean vein in the Toyoha Mines. Int J Syst Evol Microbiol 52:1675–1680. doi: 10.1099/00207713-52-5-1675. [DOI] [PubMed] [Google Scholar]
  • 2.Gam ZBA, Daumas S, Casalot L, Bartoli-Joseph M, Necib S, Linard Y, Labat M. 2016. Thermanaeromonas burensis sp. nov., a thermophilic anaerobe isolated from a subterranean clay environment. Int J Syst Evol Microbiol 66:445–449. doi: 10.1099/ijsem.0.000739. [DOI] [PubMed] [Google Scholar]
  • 3.Yoneda Y, Yoshida T, Yasuda H, Imada C, Sako Y. 2013. A thermophilic, hydrogenogenic and carboxydotrophic bacterium, Calderihabitans maritimus gen. nov., sp. nov., from a marine sediment core of an undersea caldera. Int J Syst Evol Microbiol 63:3602–3608. doi: 10.1099/ijs.0.050468-0. [DOI] [PubMed] [Google Scholar]
  • 4.Inoue M, Tanimura A, Ogami Y, Hino T, Okunishi S, Maeda H, Yoshida T, Sako Y. 2019. Draft genome sequence of Parageobacillus thermoglucosidasius strain TG4, a hydrogenogenic carboxydotrophic bacterium isolated from a marine sediment. Microbiol Resour Announc 8:e01666-18. doi: 10.1128/MRA.01666-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Fukuyama Y, Tanimura A, Inoue M, Omae K, Yoshida T, Sako Y. 2019. Draft genome sequences of two thermophilic Moorella sp. strains, isolated from an acidic hot spring in Japan. Microbiol Resour Announc 8:e00663-19. doi: 10.1128/MRA.00663-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi: 10.1093/bioinformatics/btu170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.O'Connell J, Schulz-Trieglaff O, Carlson E, Hims MM, Gormley NA, Cox AJ. 2015. NxTrim: optimized trimming of Illumina mate pair reads. Bioinformatics 31:2035–2037. doi: 10.1093/bioinformatics/btv057. [DOI] [PubMed] [Google Scholar]
  • 8.Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. doi: 10.1089/cmb.2012.0021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 1303.3S997 [q-bio.GN] https://arxiv.org/abs/1303.3997.
  • 10.Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup . 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079. doi: 10.1093/bioinformatics/btp352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Murphy RR, O'Connell J, Cox AJ, Schulz-Trieglaff O. 2015. NxRepair: error correction in de novo sequence assembly using Nextera mate pairs. PeerJ 3:e996. doi: 10.7717/peerj.996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Tanizawa Y, Fujisawa T, Nakamura Y. 2018. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34:1037–1039. doi: 10.1093/bioinformatics/btx713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Lee I, Kim YO, Park S-C, Chun J. 2016. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. doi: 10.1099/ijsem.0.000760. [DOI] [PubMed] [Google Scholar]
  • 14.Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. doi: 10.1186/1471-2105-14-60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi: 10.1186/1471-2105-10-421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Omae K, Fukuyama Y, Yasuda H, Mise K, Yoshida T, Sako Y. 2019. Diversity and distribution of thermophilic hydrogenogenic carboxydotrophs revealed by microbial community analysis in sediments from multiple hydrothermal environments in Japan. Arch Microbiol 201:969–982. doi: 10.1007/s00203-019-01661-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Inoue M, Nakamoto I, Omae K, Oguro T, Ogata H, Yoshida T, Sako Y. 2019. Structural and phylogenetic diversity of anaerobic carbon-monoxide dehydrogenases. Front Microbiol 9:3353. doi: 10.3389/fmicb.2018.03353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Sant'Anna FH, Lebedinsky AV, Sokolova TG, Robb FT, Gonzalez JM. 2015. Analysis of three genomes within the thermophilic bacterial species Caldanaerobacter subterraneus with a focus on carbon monoxide dehydrogenase evolution and hydrolase diversity. BMC Genomics 16:757. doi: 10.1186/s12864-015-1955-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

This draft genome sequence was deposited in GenBank under accession number BLWF00000000.1. The raw reads were deposited in SRA under accession number DRA010181.


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