Skip to main content
Log in

Natronorubrum halophilum sp. nov. isolated from two inland salt lakes

  • Microbial Systematics and Evolutionary Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Two halophilic archaeal strains, SHR37T and NEN6, were isolated from salt lakes located in the Tibet and Xinjiang regions of China. The two strains were found to form a single cluster (99.9% and 99.3% similarity, respectively) separating them from the six current members of Natronorubrum (94.7–96.9% and 86.1–90.8% similarity, respectively) on the basis of the 16S rRNA and rpoB′ gene sequence similarities and phylogenetic analysis. Diverse phenotypic characteristics differentiate strains SHR37T and NEN6 from current Natronorubrum members. Their polar lipids are C20C20 and C20C25glycerol diether derivatives of PG, PGP-Me, and a major gycolipid chromatographically identical to disulfated mannosyl glucosyl diether (S2-DGD). Four minor unidentified gycolipids are also present. The OrthoANI and in silico DDH values of the two strains were 97.3% and 76.1%, respectively, which were much higher than the threshold values proposed as a species boundary (ANI 95–96% and in silico DDH 70%), which revealed that the two strains represent one species; the two values (ANI 79.0–81.9% and in silico DDH 23.5–25.7%) of the strains examined in this study and the current members of Natronorubrum are much lower than the recommended threshold values, suggesting that strains SHR37T and NEN6 represent a genomically different species of Natronorubrum. These results showed that strains SHR37T (= CGMCC 1.15233T = JCM 30845T) and NEN6 (= CGMCC 1.17161) represent a novel species of Natronorubrum, for which the name Natronorubrum halophilum sp. nov. is proposed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldon, T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics25, 1972–1973.

    Article  Google Scholar 

  • Chun, J., Oren, A., Ventosa, A., Christensen, H., Arahal, D.R., da Costa, M.S., Rooney, A.P., Yi, H., Xu, X.W., De Meyer, S., et al. 2018. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int. J. Syst. Evol. Microbiol.68, 461–466.

    Article  CAS  Google Scholar 

  • Cui, H.L., Gao, X., Yang, X., and Xu, X.W. 2010. Halorussus rarus gen. nov., sp. nov., a new member of the family Halobacteriaceae isolated from a marine solar saltern. Extremophiles14, 493–499.

    Article  CAS  Google Scholar 

  • Cui, H.L., Tohty, D., Feng, J., Zhou, P.J., and Liu, S.J. 2006. Natronorubrum aibiense sp. nov., an extremely halophilic archaeon isolated from Aibi salt lake in Xin-Jiang, China, and emended description of the genus Natronorubrum. Int. J. Syst. Evol. Microbiol.56, 1515–1517.

    Article  CAS  Google Scholar 

  • Cui, H.L., Tohty, D., Liu, L.C., Liu, S.J., Oren, A., and Zhou, P.J. 2007. Natronorubrum sulfidifaciens sp. nov., an extremely haloalkaliphilic archaeon isolated from Aiding salt lake in Xin-Jiang, China. Int. J. Syst. Evol. Microbiol.57, 738–740.

    Article  CAS  Google Scholar 

  • Cui, H.L., Zhou, P.J., Oren, A., and Liu, S.J. 2009. Intraspecific polymorphism of 16S rRNA genes in two halophilic archaeal genera, Haloarcula and Halomicrobium. Extremophiles13, 31–37.

    Article  CAS  Google Scholar 

  • Delcher, A.L., Bratke, K.A., Powers, E.C., and Salzberg, S.L. 2007. Identifying bacterial genes and endosymbiont DNA with glimmer. Bioinformatics23, 673–679.

    Article  CAS  Google Scholar 

  • Felsenstein, J. 1981. Evolutionary trees from DNA sequences: A maximum likelihood approach. J. Mol. Evol.17, 368–376.

    Article  CAS  Google Scholar 

  • Fitch, W.M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool.20, 406–416.

    Article  Google Scholar 

  • Gonzalez, C., Gutierrez, C., and Ramirez, C. 1978. Halobacterium vallismortis sp. nov. an amylolytic and carbohydrate-metabolizing, extremely halophilic bacterium. Can. J. Microbiol.24, 710–715.

    Article  CAS  Google Scholar 

  • Goris, J., Konstantinidis, K.T., Klappenbach, J.A., Coenye, T., Vandamme, P., and Tiedje, J.M. 2007. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol.57, 81–91.

    Article  CAS  Google Scholar 

  • Gupta, R.S., Naushad, S., and Baker, S. 2015. Phylogenomic analyses and molecular signatures for the class Halobacteria and its two major clades: a proposal for division of the class Halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov., containing the novel families Haloferacaceae fam. nov. and Natrialbaceae fam. nov. Int. J. Syst. Evol. Microbiol.65, 1050–1069.

    Article  CAS  Google Scholar 

  • Gupta, R.S., Naushad, S., Fabros, R., and Adeolu, M. 2016. A phylogenomic reappraisal of family-level divisions within the class Halobacteria: proposal to divide the order Halobacteriales into the families Halobacteriaceae, Haloarculaceae fam. nov., and Halococcaceae fam. nov., and the order Haloferacales into the families, Haloferacaceae and Halorubraceae fam nov. Antonie van Leeuwenhoek109, 565–587.

    Article  Google Scholar 

  • Gutiérrez, M.C., Castillo, A.M., Corral, P., Minegishi, H., and Ventosa, A. 2010. Natronorubrum sediminis sp. nov., an archaeon isolated from a saline lake. Int. J. Syst. Evol. Microbiol.60, 1802–1806.

    Article  Google Scholar 

  • Gutiérrez, M.C., Castillo, A.M., Kamekura, M., and Ventosa, A. 2008. Haloterrigena salina sp. nov., an extremely halophilic archaeon isolated from a salt lake. Int. J. Syst. Evol. Microbiol.58, 2880–2884.

    Article  Google Scholar 

  • Gutiérrez, C. and González, C. 1972. Method for simultaneous detection of proteinase and esterase activities in extremely halophilic bacteria. Appl. Microbiol.24, 516–517.

    Article  Google Scholar 

  • Holding, A.J. and Collee, J.G. 1971. Routine biochemical tests. In Norris, J.R. and Ribbons, D.W. (eds.), Methods in Microbiology, vol. 6, pp. 1–32. Academic Press, Inc., London, UK.

    Google Scholar 

  • Katoh, K. and Standley, D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and — usability. Mol. Biol. Evol.30, 772–780.

    Article  CAS  Google Scholar 

  • Kim, M., Oh, H.S., Park, S.C., and Chun, J. 2014. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol.64, 346–351.

    Article  CAS  Google Scholar 

  • Lagesen, K., Hallin, P., Rødland, E.A., Stærfeldt, H.H., Rognes, T., and Ussery, D.W. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res.35, 3100–3108.

    Article  CAS  Google Scholar 

  • Li, L., Stoeckert, C.J.Jr, and Roos, D.S. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res.13, 2178–2189.

    Article  CAS  Google Scholar 

  • Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., He, G., Chen, Y., Pan, Q., Liu, Y., et al. 2012. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Giga-Science1, 18.

    Article  Google Scholar 

  • McDade, J.J. and Weaver, R.H. 1959. Rapid methods for the detection of gelatin hydrolysis. J. Bacteriol.77, 60–64.

    Article  CAS  Google Scholar 

  • Meier-Kolthoff, J.P., Auch, A.F., Klenk, H.P., and Göker M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics14, 60.

    Article  Google Scholar 

  • Minegishi, H., Kamekura, M., Itoh, T., Echigo, A., Usami, R., and Hashimoto, T. 2010. Further refinement of the phylogeny of the Halobacteriaceae based on the full-length RNA polymerase subunit B′ (rpoB′) gene. Int. J. Syst. Evol. Microbiol.60, 2398–2408.

    Article  Google Scholar 

  • Najjari, A., Elshahed, M.S., Cherif, A., and Youssef, N.H. 2015. Patterns and determinants of halophilic Archaea (Class Halobacteria) diversity in Tunisian endorheic salt lakes and sebkhet systems. Appl. Environ. Microbiol.81, 4432–4441.

    Article  CAS  Google Scholar 

  • Nguyen, L.T., Schmidt, H.A., von Haeseler, A., and Minh, B.Q. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol.32, 268–274.

    Article  CAS  Google Scholar 

  • Oren, A., Ventosa, A., and Grant, W.D. 1997. Proposed minimal standards for description of new taxa in the order Halobacteriales. Int. J. Syst. Bacteriol.47, 233–238.

    Article  Google Scholar 

  • Overbeek, R., Olson, R., Pusch, G.D., Olsen, G.J., Davis, J.J., Disz, T., Edwards, R.A., Gerdes, S., Parrello, B., Shukla, M., et al. 2014. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res.42, D206–D214.

    Article  CAS  Google Scholar 

  • Pagaling, E., Wang, H., Venables, M., Wallace, A., Grant, W.D., Cowan, D.A., Jones, B.E., Ma, Y., Ventosa, A., and Heaphy, S. 2009. Microbial biogeography of six salt lakes in Inner Mongolia, China, and a salt lake in Argentina. Appl. Environ. Microbiol.75, 5750–5760.

    Article  CAS  Google Scholar 

  • Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P., and Tyson, G.W. 2015. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res.25, 1043–1055.

    Article  CAS  Google Scholar 

  • Richter, M. and Rosselló-Móra, R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA106, 19126–19131.

    Article  CAS  Google Scholar 

  • Ruiz-Romero, E., Valenzuela-Encinas, C., López-Ramírez, M.P., de los Angeles Coutiño-Coutiño, M., Marsch, R., and Dendooven, L. 2013. Natronorubrum texcoconense sp. nov., a haloalkaliphilic archaeon isolated from soil of the former lake Texcoco (Mexico). Arch. Microbiol.195, 145–151.

    Article  CAS  Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol.4, 406–425.

    CAS  PubMed  Google Scholar 

  • Siakotos, A.N. and Rouser, G. 1965. Analytical separation of nonlipid water soluble substances and gangliosides from other lipids by dextran gel column chromatography. J. Am. Oil Chem. Soc.42, 913–919.

    Article  CAS  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D.S., Filipski, A., and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol.30, 2725–2729.

    Article  CAS  Google Scholar 

  • Vaskovsky, V.E. and Kostetsky, E.Y. 1968. Modified spray for the detection of phospholipids on thin-layer chromatograms. J. Lipid Res.9, 396.

    CAS  PubMed  Google Scholar 

  • Walsh, D.A., Papke, R.T., and Doolittle, W.F. 2005. Archaeal diversity along a soil salinity gradient prone to disturbance. Environ. Microbiol.7, 1655–1666.

    Article  CAS  Google Scholar 

  • Xu, Y., Zhou, P., and Tian, X. 1999. Characterization of two novel haloalkaliphilic archaea Natronorubrum bangense gen. nov., sp. nov. and Natronorubrum tibetense gen. nov., sp. nov. Int. J. Syst. Bacteriol.49, 261–266.

    Article  CAS  Google Scholar 

  • Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. 2017. Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. Int. J. Syst. Evol. Microbiol.67, 1613–1617.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 31770005) and the National Science & Technology Infrastructure Program of China (No. 2017FY100302). The authors thank Dr. Mike Dyall-Smith (University of Melbourne) for many helpful suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heng-Lin Cui.

Additional information

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tao, CQ., Ding, Y., Zhao, YJ. et al. Natronorubrum halophilum sp. nov. isolated from two inland salt lakes. J Microbiol. 58, 105–112 (2020). https://doi.org/10.1007/s12275-020-9514-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-020-9514-8

Keywords

Navigation