1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 71, Issue 9

sp. nov., a thermophilic, nitrogen-fixing fermentative bacterium isolated from a terrestrial hot spring in Japan No Access

Abstract

A novel nitrogen-fixing fermentative bacterium, designated as YA01, was isolated from Nakabusa hot springs in Japan. The short-rod cells of strain YA01 were Gram-positive and non-sporulating. Phylogenetic trees of the 16S rRNA gene sequence and concatenated sequences of 40 single-copy ribosomal genes revealed that strain YA01 belonged to the genus and was closely related to 108, DSM 6725 and 2002. The 16S rRNA gene sequence of strain YA01 shares less than 98.1 % identity to the known species. The G+C content of the genomic DNA was 34.8 mol%. Strain YA01 shares low genome-wide average nucleotide identity (90.31–91.10 %), average amino acid identity (91.45–92.10 %) and <70 % digital DNA–DNA hybridization value (41.8–44.2 %) with the three related species of the genus . Strain YA01 grew at 50–78 °C (optimum, 70 °C) and at pH 5.0–9.5 (optimum, pH 6.5). Strain YA01 mainly produced acetate by consuming (+)-glucose as a carbon source. The main cellular fatty acids were iso-C (35.7 %), C (33.3 %), DMA (6.6 %) and iso-C (5.9 %). Based on its distinct phylogenetic position, biochemical and physiological characteristics, and the major cellular fatty acids, strain YA01 is considered to represent a novel species of the genus for which the name sp. nov. is proposed (type strain YA01=DSM 112098=JCM 34253).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Caldicellulosiruptor , fermentation , hot spring and nitrogen fixation
Funding
This study was supported by the:
  • Japan Society for Bioscience, Biotechnology, and Agrochemistry (Award JSBBA Innovative Research Program Award)
    • Principle Award Recipient: HarutaShin
© 2021 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005014
2021-09-20
2024-04-18
Loading full text...

Full text loading...

References

  1. Blumer-Schuette SE, Lewis DL, Kelly RM. Phylogenetic, microbiological, and glycoside hydrolase diversities within the extremely thermophilic, plant biomass-degrading genus Caldicellulosiruptor. Appl Environ Microbiol 2010; 76:8084–8092 [View Article]
     [Google Scholar]
  2. Blumer-Schuette SE, Giannone RJ, Zurawski J, Ozdemir I, Ma Q et al. Caldicellulosiruptor core and pangenomes reveal determinants for noncellulosomal thermophilic deconstruction of plant biomass. J Bacteriol 2012; 194:4015–4028 [View Article]
     [Google Scholar]
  3. Brunecky R, Alahuhta M, Xu Q, Donohoe BS, Crowley MF et al. Revealing nature’s cellulase diversity: the digestion mechanism of Caldicellulosiruptor bescii CelA. Science 2013; 342:1513–1516 [View Article]
     [Google Scholar]
  4. Blumer-schuette SE. Insights into thermophilic plant biomass hydrolysis from Caldicellulosiruptor systems biology. Microorganisms 2020; 8: [View Article]
     [Google Scholar]
  5. Rainey FA, Donnison AM, Janssen PH, Saul D, Rodrigo A et al. Description of Caldicellulosiruptor saccharolyticus gen. nov., sp. nov: An obligately anaerobic, extremely thermophilic, cellulolytic bacterium. FEMS Microbiol Lett 1994; 120:263–266 [View Article]
     [Google Scholar]
  6. Mladenovska Z, Mathrani IM, Ahring BK. Isolation and characterization of Caldicellulosiruptor lactoaceticus sp. nov., an extremely thermophilic, cellulolytic, anaerobic bacterium. Arch Microbiol 1995; 163:223–230 [View Article]
     [Google Scholar]
  7. Huang C, Patel BK, Mah RA, Baresi L. Caldicellulosiruptor owensensis sp. nov., an anaerobic, extremely thermophilic, xylanolytic bacterium. Int J Syst Evol Microbiol 1998; 48:91–97 [View Article]
     [Google Scholar]
  8. Bredholt S, Sonne-Hansen J, Nielsen P, Mathrani IM, Ahring BK. Caldicellulosiruptor kristjanssonii sp. nov., a cellulolytic, extremely thermophilic, anaerobic bacterium. Int J Syst Evol Microbiol 1999; 49:991–996 [View Article]
     [Google Scholar]
  9. Onyenwoke RU, Lee Y-J, Dabrowski S, Ahring BK, Wiegel J. Reclassification of Thermoanaerobium acetigenum as Caldicellulosiruptor acetigenus comb. nov. and emendation of the genus description. Int J Syst Evol Microbiol 2006; 56:1391–1395 [View Article]
     [Google Scholar]
  10. Miroshnichenko ML, Kublanov IV, Kostrikina NA, Tourova TP, Kolganova TV et al. Caldicellulosiruptor kronotskyensis sp. nov. and Caldicellulosiruptor hydrothermalis sp. nov., two extremely thermophilic, cellulolytic, anaerobic bacteria from Kamchatka thermal springs. Int J Syst Evol Microbiol 2008; 58:1492–1496 [View Article]
     [Google Scholar]
  11. Yang SJ, Kataeva I, Wiegel J, Yin Y, Dam P et al. Classification of “Anaerocellum thermophilum” strain DSM 6725 as Caldicellulosiruptor bescii sp. nov. Int J Syst Evol Microbiol 2010; 60:2011–2015 [View Article]
     [Google Scholar]
  12. Bing W, Wang H, Zheng B, Zhang F, Zhu G et al. Caldicellulosiruptor changbaiensis sp. nov., a cellulolytic and hydrogen-producing bacterium from a hot spring. Int J Syst Evol Microbiol 2015; 65:293–297 [View Article]
     [Google Scholar]
  13. Blank CE, Cady SL, Pace NR. Microbial composition of near-boiling silica-depositing thermal springs throughout Yellowstone National Park. Appl Environ Microbiol 2002; 68:5123–5135 [View Article]
     [Google Scholar]
  14. Purcell D, Sompong U, Yim LC, Barraclough TG, Peerapornpisal Y et al. The effects of temperature, pH and sulphide on the community structure of hyperthermophilic streamers in hot springs of northern Thailand. FEMS Microbiol Ecol 2007; 60:456–466 [View Article]
     [Google Scholar]
  15. Tamazawa S, Takasaki K, Tamaki H, Kamagata Y, Hanada S. Metagenomic and biochemical characterizations of sulfur oxidation metabolism in uncultured large sausage-shaped bacterium in hot spring microbial mats. PLoS One 2012; 7:e49793 [View Article]
     [Google Scholar]
  16. Takacs-Vesbach C, Inskeep WP, Jay ZJ, Herrgard MJ, Rusch DB et al. Metagenome sequence analysis of filamentous microbial communities obtained from geochemically distinct geothermal channels reveals specialization of three Aquificales lineages. Front Microbiol 2013; 4:84 [View Article]
     [Google Scholar]
  17. Ogawa K, Maki Y. Cellulose as extracellular polysaccharide of hot spring sulfur-turf bacterial mat. Biosci Biotechnol Biochem 2003; 67:2652–2654 [View Article]
     [Google Scholar]
  18. Nakagawa T, Fukui M. Phylogenetic characterization of microbial mats and streamers from a Japanese alkaline hot spring with a thermal gradient. J Gen Appl Microbiol 2002; 48:211–222 [View Article]
     [Google Scholar]
  19. Nakagawa T, Fukui M. Molecular characterization of community structures and sulfur metabolism within microbial streamers in Japanese hot springs. Appl Environ Microbiol 2003; 69:7044–7057 [View Article]
     [Google Scholar]
  20. Kubo K, Knittel K, Amann R, Fukui M, Matsuura K. Sulfur-metabolizing bacterial populations in microbial mats of the Nakabusa hot spring, Japan. Syst Appl Microbiol 2011; 34:293–302 [View Article]
     [Google Scholar]
  21. Otaki H, Everroad RC, Matsuura K, Haruta S. Production and consumption of hydrogen in hot spring microbial mats dominated by a filamentous anoxygenic photosynthetic bacterium. Microbes Environ 2012; 27:293–299 [View Article]
     [Google Scholar]
  22. Everroad RC, Otaki H, Matsuura K, Haruta S. Diversification of bacterial community composition along a temperature gradient at a thermal spring. Microbes Environ 2012; 27:374–381 [View Article]
     [Google Scholar]
  23. Tamazawa S, Yamamoto K, Takasaki K, Mitani Y, Hanada S et al. In situ gene expression responsible for sulfide oxidation and CO2 fixation of an uncultured large sausage-shaped Aquificae bacterium in a sulfidic hot spring. Microbes Environ 2016; 31:194–198 [View Article]
     [Google Scholar]
  24. Nishihara A, Haruta S, McGlynn SE, Thiel V, Matsuura K. Nitrogen fixation in thermophilic chemosynthetic microbial communities depending on hydrogen, sulfate, and carbon dioxide. Microbes Environ 2018; 33:10–18 [View Article]
     [Google Scholar]
  25. Nishihara A, Thiel V, Matsuura K, McGlynn SE, Haruta S. Phylogenetic diversity of nitrogenase reductase genes and possible nitrogen-fixing bacteria in thermophilic chemosynthetic microbial communities in Nakabusa hot springs. Microbes Environ 2018; 33:357–365 [View Article]
     [Google Scholar]
  26. Chen Y, Nishihara A, Haruta S. Nitrogen-fixing ability and nitrogen fixation related genes of thermophilic fermentative bacteria in the genus Caldicellulosiruptor. Microbes Environ 2021; 36:ME21018 [View Article] [PubMed]
     [Google Scholar]
  27. Altschul SF, Madden TL, Schäffer AA, Zhang JH, Zhang Z et al. Gapped BLAST and PSI-BLAST:a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article]
     [Google Scholar]
  28. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article]
     [Google Scholar]
  29. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article]
     [Google Scholar]
  30. Phillippy AM, Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article]
     [Google Scholar]
  31. Seemann T. PROKKA: Rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  32. Katoh K, Misawa K, Kuma KI, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article]
     [Google Scholar]
  33. Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article]
     [Google Scholar]
  34. Lemoine F, Domelevo Entfellner J-B, Wilkinson E, Correia D, Dávila Felipe M et al. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 2018; 556:452–456 [View Article]
     [Google Scholar]
  35. Rodriguez-R L, Konstantinidis K. The Enveomics collection: A toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016; 4:e1900vl [View Article]
     [Google Scholar]
  36. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article]
     [Google Scholar]
  37. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, MIDI Technical Note 101. Newark, DE: MIDI Inc; 2001
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005014
Loading
Caldicellulosiruptor diazotrophicus sp. nov., a thermophilic, nitrogen-fixing fermentative bacterium isolated from a terrestrial hot spring in Japan
Int J Syst Evol Microbiol 71, 005014 (2021); https://doi.org/10.1099/ijsem.0.005014
/content/journal/ijsem/10.1099/ijsem.0.005014
/content/journal/ijsem/10.1099/ijsem.0.005014
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error