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. 2020 Jul 29;35(3):ME20074. doi: 10.1264/jsme2.ME20074

TEMPURA: Database of Growth TEMPeratures of Usual and RAre Prokaryotes

Yu Sato 1,*, Kenji Okano 1, Hiroyuki Kimura 2,3, Kohsuke Honda 1
PMCID: PMC7511790  PMID: 32727974

Abstract

Growth temperature is one of the most representative biological parameters for characterizing living organisms. Prokaryotes have been isolated from various temperature environments and show wide diversity in their growth temperatures. We herein constructed a database of growth TEMPeratures of Usual and RAre prokaryotes (TEMPURA, http://togodb.org/db/tempura), which contains the minimum, optimum, and maximum growth temperatures of 8,639 prokaryotic strains. Growth temperature information is linked with taxonomy IDs, phylogenies, and genomic information. TEMPURA provides useful information to researchers working on biotechnological applications of extremophiles and their biomolecules as well as those performing fundamental studies on the physiological diversity of prokaryotes.

Keywords: growth temperature, database, prokaryote, genome, 16S ribosomal RNA

Living organisms adapt to changes in various environmental parameters, such as temperature, pH, pressure, and nutrient availability, in their natural habitats. Prokaryotes are often found in various extreme environments, ranging from arctic lakes (below 0°C) to deep-sea hydrothermal vents (higher than 100°C), and show wider diversity in their growth temperatures than eukaryotes (Tschitschko et al., 2018; Dick, 2019). The growth temperatures of prokaryotes are important information not only for fundamental studies (e.g., those on the mechanisms of temperature adaptation by living organisms and the exploration of limits of the biosphere), but also bioprospecting studies on commercially valuable thermotoleant enzymes and antifreeze proteins. However, the majority of studies have focused on a limited number of model extremophiles due to the time-consuming process of a literature search for rare thermophiles and psychrophiles (Haki and Rakshit, 2003).

Therefore, a comprehensive database of prokaryotic growth temperatures represents a promising tool for overcoming these limitations and facilitating both fundamental and biotechnological studies in relevant fields. A database summarizing the optimum growth temperatures of 1,072 prokaryotes has already been developed (Huang et al., 2004), but is currently inaccessible (Modarres et al., 2018). Although the optimum growth temperatures of 8,093 prokaryotes have been utilized to investigate the relationships between their growth temperatures and genome sequences, these data have not been published as a database (Sauer et al., 2015, 2019). Therefore, we herein newly constructed a database of growth TEMPeratures of Usual and RAre prokaryotes (TEMPURA), which includes the minimum, optimum, and maximum growth temperatures of 8,639 prokaryotic strains. We also performed a correlation analysis between growths temperature and guanine-plus-cytosine (G+C) contents in prokaryotic DNA using data deposited in TEMPURA.

To construct the database, we manually collected the minimum (Tmin), optimum (Topt), and maximum (Tmax) growth temperatures of 8,639 strains (archaea, 549; bacteria, 8,090). Each strain deposited in TEMPURA has a direct link to the corresponding web page in the NCBI Taxonomy database (Sayers et al., 2009, 2019). Tmin, Topt, and Tmax of the strain was obtained from the oldest relevant study cited on the web page. When there was no relevant study in the Taxonomy database, the online version of Bergey’s Manual (https://onlinelibrary.wiley.com/doi/book/10.1002/9781118960608) was employed as a source of strain information. Strains without this set of growth temperature information were removed. When an optimum growth temperature was shown as a range, the average value was employed. Additionally, the lowest (Topt_low) and highest (Topt_high) values in the range were shown in TEMPURA. Based on growth temperatures, we divided strains into four groups as described previously (Madigan et al., 2003; Moyer and Morita, 2007): psychrophiles and psychrotrophic microorganisms (Topt<20°C), mesophiles (20≤Topt<45°C), thermophiles (45≤Topt<80°C), and hyperthermophiles (80°C≤Topt).

TEMPURA was constructed on TogoDB (http://togodb.org), an online database that is freely accessed. It contains species names, taxonomy IDs, lineages (superkingdom, phylum, class, order, family, and genus), and genomic information (G+C content and genome size) in addition to growth temperatures. The lineage and genomic data of the isolated strains were obtained from the NCBI Taxonomy database and NCBI Genome database, respectively (Sayers et al., 2009, 2019).

TEMPURA also includes information on various extremophiles: 209 psychrophiles and psychrotrophic microorganisms (3 archaea and 206 bacteria), 7,574 mesophiles (327 archaea and 7,247 bacteria), 731 thermophiles (104 archaea and 627 bacteria), and 125 hyperthermophiles (115 archaea and 10 bacteria). Among them, Methanopyrus kandleri strain 116 showed the highest Tmax of 122°C (Takai et al., 2008), whereas “Geogemma barossii” strain 121 and Pyrolobus fumarii strain 1A showed the highest Topt of 106°C (Blöchl et al., 1997; Kashefi and Lovley, 2003). These archaea were all isolated from deep-sea hydrothermal vents, which are one of the hottest places on Earth’s surface. On the other hand, the lowest Tmin of –20°C was observed for Planococcus faecalis strain AJ003, a bacterium isolated from the stools of Antarctic penguins (Kim et al., 2015), and the lowest Topt was 2°C (or lower) for Moritella profunda strain 2674, a moderate-piezophilic bacterium isolated from Atlantic sediments (Xu et al., 2003). Therefore, the strains that showed the highest Tmax or lowest Tmin were not necessarily the same as those with the highest or lowest Topt. TEMPURA also revealed the existence of rare strains growing in a wide temperature range. The largest difference between Tmin and Tmax was 60°C in Kosmotoga olearia strain TBF 19.5.1 (20 and 80°C), Bacillus beveridgei strain MLTeJB (5 and 65°C), and Streptomyces thermoautotrophicus strain UBT1 (10 and 70°C), which were isolated from a high-temperature oil field (DiPippo et al., 2009), a highly alkaline and hypersaline lake (Baesman et al., 2009), and the covering soil of a burning charcoal pile (Gadkari et al., 1990), respectively. The large temperature gradient in an oil reservoir, diurnal temperature variations in a salt lake, and rapid heating by burning may had led to the adaptation of these strains to a wide range of temperatures.

TEMPURA is also useful for correlation analyses between growth temperatures and genomic information. In the present study, we performed correlation analyses between growth temperatures and G+C contents, which are related to the structural strengths of DNA and RNA or genome sizes as major nucleotide information (Fig. 1). No correlations were observed between the G+C content of a genomic sequence and Tmin, Topt, or Tmax (R=–0.291 to –‍0.032) (Fig. 1a). On the other hand, strong positive correlations were found between the G+C contents of 16S ribosomal RNAs and growth temperatures in archaea (R=0.842 to 0.880) (Fig. 1b). Similar results were obtained in bacteria (R=0.378 to 0.404); however, correlation coefficients and symmetry in data distribution were lower than those in archaea. Higher coefficients (R=0.455 to 0.505) were observed when only thermophilic bacteria were subjected to the correlation analysis (Fig. S1), suggesting that a high G+C content, and thus, the structural strength of ribosomal RNAs are of importance for the thermal adaptation of prokaryotes, particularly at high temperatures. This result is consistent with previous findings showing higher G+C contents in the ribosomal RNAs of thermophiles and hyperthermophiles than in those of psychrophiles, psychrotrophic microorganisms, and mesophiles (Galtier and Lobry, 1997; Khachane et al., 2005; Kimura et al., 2006; Wang et al., 2006; Kimura et al., 2007, 2010, 2013). Data symmetry in thermophilic bacteria also appeared to be higher than that in the others (Fig. S1), which may be due to the presumably higher accuracy in the procedure to investigate the growth temperatures of these bacteria. The proportion of thermophilic and hyperthermophilic strains was significantly lower in bacteria (8.0%) than in archaea (40.1%). This may have resulted in the lower correlation coefficient in bacteria than in archaea. We also found that genome sizes showed a moderately negative correlation with growth temperatures in both archaea (R=–0.592 to –0.579) and bacteria (R=–0.378 to –0.313) (Fig. 1c). These results demonstrated that genomic DNA is slightly shorter in thermophiles and hyperthermophiles than in psychrophiles, psychrotrophic microorganisms, and mesophiles, which is consistent with previous findings (Sabath et al., 2013). As described above, TEMPURA will be useful for obtaining and utilizing growth temperatures, which will accelerate fundamental and applicable studies in various fields.

Fig. 1.

Fig. 1.

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Correlations between genomic features and growth temperatures in archaeal ([A], red circle and red line) and bacterial strains ([B], blue circle and blue line). Each graph shows the correlation between (a) the G+C content of a complete genome, (b) the G+C content of 16S rRNA, and (c) the genome size with each growth temperature (Tmin, Topt, and Tmax). Correlations were examined using Pearson’s correlation coefficients (R values).

Citation

Sato, Y., Okano, K., Kimura, H., and Honda, K. (2020) TEMPURA: Database of Growth TEMPeratures of Usual and RAre Prokaryotes. Microbes Environ 35: ME20074.

https://doi.org/10.1264/jsme2.ME20074

Supplementary Material

Supplementary Material (337.8KB, pdf)

Acknowledgements

This work was partly supported by the JST-MIRAI program (Grant Number JPMJMI17EK) and also by a Grant-in-Aid for JSPS Fellows (grant number 20J00010).

References

  1. Baesman S.M., Stolz J.F., Kulp T.R., and Oremland R.S. (2009) Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California, that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles 13: 695–705. [DOI] [PubMed] [Google Scholar]
  2. Blöchl E., Rachel R., Burggraf S., Hafenbradl D., Jannasch H.W., and Stetter K.O. (1997) Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113°C. Extremophiles 1: 14–21. [DOI] [PubMed] [Google Scholar]
  3. Dick G.J. (2019) The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat Rev Microbiol 17: 271–283. [DOI] [PubMed] [Google Scholar]
  4. DiPippo J.L., Nesbø C.L., Dahle H., Doolittle W.F., Birkland N.K., and Noll K.M. (2009) Kosmotoga olearia gen. nov., sp. nov., a thermophilic, anaerobic heterotroph isolated from an oil production fluid. Int J Syst Evol Microbiol 59: 2991–3000. [DOI] [PubMed] [Google Scholar]
  5. Gadkari D., Schricker K., Acker G., Kroppenstedt R.M., and Meyer O. (1990) Streptomyces thermoautotrophicus sp. nov., a thermophilic CO- and H2-oxidizing obligate chemolithoautotroph. Appl Environ Microbiol 56: 3727–3734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Galtier N., and Lobry J.R. (1997) Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol 44: 632–636. [DOI] [PubMed] [Google Scholar]
  7. Haki G.D., and Rakshit S.K. (2003) Developments in industrially important thermostable enzymes: a review. Bioresour Technol 89: 17–34. [DOI] [PubMed] [Google Scholar]
  8. Huang S.L., Wu L.C., Liang H.K., Pan K.T., Horng J.T., and Ko M.T. (2004) PGTdb: a database providing growth temperatures of prokaryotes. Bioinformatics 20: 276–278. [DOI] [PubMed] [Google Scholar]
  9. Kashefi K., and Lovley D.R. (2003) Extending the upper temperature limit for life. Science 301: 934. [DOI] [PubMed] [Google Scholar]
  10. Khachane A.N., Timmis K.N., and dos Santos V.A.P.M. (2005) Uracil content of 16S rRNA of thermophilic and psychrophilic prokaryotes correlates inversely with their optimal growth temperatures. Nucleic Acids Res 33: 4016–4022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kim J.H., Kang H.J., Yu B.J., Kim S.C., and Lee P.C. (2015) Planococcus faecalis sp. nov., a carotenoid-producing species isolated from stools of antarctic penguins. Int J Syst Evol Microbiol 65: 3373–3378. [DOI] [PubMed] [Google Scholar]
  12. Kimura H., Sugihara M., Kato K., and Hanada S. (2006) Selective phylogenetic analysis targeted at 16S rRNA genes of thermophiles and hyperthermophiles in deep-subsurface geothermal environments. Appl Environ Microbiol 72: 21–27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kimura H., Ishibashi J., Masuda H., Kato K., and Hanada S. (2007) Selective phylogenetic analysis targeting 16S rRNA genes of hyperthermophilic archaea in the deep-subsurface hot biosphere. Appl Environ Microbiol 73: 2110–2117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kimura H., Mori K., Tashiro T., Kato K., Yamanaka T., Ishibashi J., et al. (2010) Culture-independent estimation of optimal and maximum growth temperatures of archaea in subsurface habitats based on the G+C content in 16S rRNA gene sequences. Geomicrobiol J 27: 114–122. [Google Scholar]
  15. Kimura H., Mori K., Yamanaka T., and Ishibashi J. (2013) Growth temperatures of archaeal communities can be estimated from the guanine-plus-cytosine contents of 16S rRNA gene fragments. Environ Microbiol Rep 5: 468–474. [DOI] [PubMed] [Google Scholar]
  16. Madigan, M.T., Martinko, J.M., and Parker, J. (2003) Brock Biology of Microorganisms, 10th edn. London: Prentice Hall. [Google Scholar]
  17. Modarres H.P., Mofrad M.R., and Sanati-Nezhad A. (2018) ProtDataTherm: A database for thermostability analysis and engineering of proteins. PLoS One 13: e0191222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Moyer, C.L., and Morita, R.Y. (2007) Psychrophiles and psychrotrophs. In Encyclopedia of Life Sciences. New York, NY: John Wiley & Sons, pp. 1–6. [Google Scholar]
  19. Sabath N., Ferrada E., Barve A., and Wagner A. (2013) Growth temperature and genome size in bacteria are negatively correlated, suggesting genomic streamlining during thermal adaptation. Genome Biol Evol 5: 966–977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sauer D.B., Karpowich N.K., Song J.M., and Wang D.N. (2015) Rapid bioinformatic identification of thermostabilizing mutations. Biophys J 109: 1420–1428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sauer D.B., Wang D.N., and Valencia A. (2019) Predicting the optimal growth temperatures of prokaryotes using only genome derived features. Bioinformatics 35: 3224–3231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sayers E.W., Barrett T., Benson D.A., Bryant S.H., Canese K., Chetvernin., V., et al. (2009) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 37: D5–D15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sayers E.W., Agarwala R., Bolton E.E., Brister J.R., Canese K., Clark K., et al. (2019) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 8: D23–D28 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Takai K., Nakamura K., Toki T., Tsunogai U., Miyazaki M., Miyazaki J., et al. (2008) Cell proliferation at 122°C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc Natl Acad Sci U S A 105: 10949–10954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tschitschko B., Erdmann S., DeMaere M.Z., Roux S., Panwar P., Allen M.A., et al. (2018) Genomic variation and biogeography of Antarctic haloarchaea. Microbiome 6: 113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wang H.C., Susko E., and Roger A.J. (2006) On the correlation between genomic G+C content and optimal growth temperature in prokaryotes: Data quality and confounding factors. Biochem Biophys Res Commun 342: 681–684. [DOI] [PubMed] [Google Scholar]
  27. Xu Y., Nogi Y., Kato C., Liang Z., Rüger H.J., De Kegel D., et al. (2003) Moritella profunda sp. nov. and Moritella abyssi sp. nov., two psychropiezophilic organisms isolated from deep Atlantic sediments. Int J Syst Evol Microbiol 53: 533–538. [DOI] [PubMed] [Google Scholar]

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Supplementary Material (337.8KB, pdf)

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