Abstract
Six novel halophilic archaeal strains of XZYJT10T, XZYJ18T, XZYJT40T, XZYJT49T, YCN54T and LT46T were isolated from a solar saltern in Tibet, a salt lake in Shanxi, and a saline soil in Xinjiang, China. Sequence similarities of 16S rRNA and rpoB′ genes among strains XZYJT10T, XZYJ18T, XZYJT40T, XZYJT49T, YCN54T, LT46T and current members of Halorussus were 90.6–97.8% and 87.8–96.4%, respectively. The average nucleotide identity and in silico DNA-DNA hybridization values among these six strains and current Halorussus members were in the range of 76.5–87.5% and 21.0–33.8%, respectively. These values were all below the species boundary threshold values. The phylogenomic tree based on 122 conserved archaeal protein marker genes revealed that the six novel strains formed individual distinct branches and clustered tightly with Halorussus members. Several phenotypic characteristics distinguished the six strains from current Halorussus members. Polar lipid analysis showed that the six novel strains contained phosphatidylglycerol, phosphatidylglycerol phosphate methyl ester, phosphatidylglycerol sulfate and two to three glycolipids. Phenotypic, chemotaxonomic and phylogenetic properties showed that the six strains represented six novel species within the genus Halorussus, for which the names Halorussus vallis sp. nov., Halorussus aquaticus sp. nov., Halorussus gelatinilyticus sp. nov., Halorussus limi sp. nov., Halorussus salilacus sp. nov., and Halorussus salinisoli sp. nov. are proposed.
Similar content being viewed by others
References
Chaumeil PA, Mussig AJ, Hugenholtz P et al (2019) GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36(6):1925–1927. https://doi.org/10.1093/bioinformatics/btz848
Chek MF, Hiroe A, Hakoshima T et al (2019) PHA synthase (PhaC): interpreting the functions of bioplastic-producing enzyme from a structural perspective. Appl Microbiol Biotechnol 103(3):1131–1141. https://doi.org/10.1007/s00253-018-9538-8
Cui HL, Dyall-Smith ML (2021) Cultivation of halophilic archaea (class Halobacteria ) from thalassohaline and athalassohaline environments. Mar Life Sci Technol 3:243–251. https://doi.org/10.1007/s42995-020-00087-3
Cui HL, Zhou PJ, Oren A et al (2008) Intraspecific polymorphism of 16S rRNA genes in two halophilic archaeal genera, Haloarcula and Halomicrobium. Extremophiles 13:31–37. https://doi.org/10.1007/s00792-008-0194-2
Cui HL, Gao X, Yang X et al (2010) Halorussus rarus gen. nov., sp. nov., a new member of the family Halobacteriaceae isolated from a marine solar saltern. Extremophiles 14:493–499. https://doi.org/10.1007/s00792-010-0329-0
Ding Y, Han D, Cui HL (2020) Halorussus halophilus sp. nov., a novel halophilic archaeon isolated from a marine solar saltern. Curr Microbiol 77(7):1321–1327. https://doi.org/10.1007/s00284-020-01921-8
Donovan HP, Maria C, David WW et al (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36(10):996–1004. https://doi.org/10.1038/nbt.4229
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17(6):368–376. https://doi.org/10.1007/BF01734359
Fernandez-Castillo R, Rodriguez-Valera F, Gonzalez-Ramos J et al (1986) Accumulation of poly (β-hydroxybutyrate) by halobacteria. Appl Environ Microbiol 51(1):214–216. https://doi.org/10.1128/aem.51.1.214-216.1986
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20(4):406–416. https://doi.org/10.2307/2412116
Han D, Cui HL (2020) Halostella pelagica sp. nov. and Halostella litorea sp. nov., isolated from salted brown alga Laminaria. Int J Syst Evol Microbiol 70(3):1969–1976. https://doi.org/10.1099/ijsem.0.004003
Han D, Cui HL (2022) Halorussus halobius sp. nov., Halorussus marinus sp. nov. and Halorussus pelagicus sp. nov., isolated from salted brown alga Laminaria. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.005313
Han D, Zhu L, Cui HL (2019) Halorussus litoreus sp. nov., isolated from the salted brown alga Laminaria. Int J Syst Evol Microbiol 69(3):767–772. https://doi.org/10.1099/ijsem.0.003233
Kalyaanamoorthy S, Minh BQ, Wong TKF et al (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285
Kanehisa M, Goto S, Kawashima S et al (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277-280. https://doi.org/10.1093/nar/gkh063
Kim M, Oh HS, Park SC et al (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. https://doi.org/10.1099/ijs.0.059774-0
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Lee I, Ouk KY, Park SC et al (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66(2):1100–1103. https://doi.org/10.1099/ijsem.0.000760
Lobasso S, Pérez-Davó A, Vitale R et al (2015) Deciphering archaeal glycolipids of an extremely halophilic archaeon of the genus Halobellus by MALDI-TOF/MS. Chem Phys Lipids 186:1–8. https://doi.org/10.1016/j.chemphyslip.2014.11.002
Luo R, Liu B, Xie Y et al (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1(1):18. https://doi.org/10.1186/2047-217X-1-18
Meier-Kolthoff JP, Auch AF, Klenk HP et al (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60–60. https://doi.org/10.1186/1471-2105-14-60
Minegishi H, Kamekura M, Itoh T et al (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. https://doi.org/10.1099/ijs.0.017160-0
Nguyen LT, Schmidt HA, von Haeseler A et al (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Oren A, Ventosa A, Grant WD (1997) Proposed minimal standards for description of new taxa in the order Halobacteriales. Int J Syst Evol Microbiol 47:233–238. https://doi.org/10.1099/00207713-47-1-233
Parks DH, Imelfort M, Skennerton CT et al (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25(7):1043–1055. https://doi.org/10.1101/gr.186072.114
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Wainø M, Tindall BJ, Ingvorsen K (2000) Halorhabdus utahensis gen. nov., sp. nov., an aerobic, extremely halophilic member of the archaea from great salt lake. Utah Int J Syst Evol Microbiol 50:183–190. https://doi.org/10.1099/00207713-50-1-183
Xu WD, Zhang WJ, Han D et al (2015) Halorussus ruber sp. nov., isolated from an inland salt lake of China. Arch Microbiol 197(1):91–95. https://doi.org/10.1007/s00203-014-1058-z
Xu JQ, Xu WM, Li Y et al (2016) Halorussus salinus sp. nov., isolated from a marine solar saltern. Arch Microbiol 198(10):957–961. https://doi.org/10.1007/s00203-016-1253-1
Xu L, Dong Z, Fang L et al (2019) OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 47(W1):W52–W58. https://doi.org/10.1093/nar/gkz333
Yoon SH, Ha SM, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67(5):1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yuan PP, Han D, Zhang WJ et al (2015) Halorussus amylolyticus sp. nov., isolated from an inland salt lake. Int J Syst Evol Microbiol 65(10):3734–3738. https://doi.org/10.1099/ijsem.0.000487
Acknowledgements
We are grateful to Prof. Yu-Guang Zhou (CGMCC) for kindly providing the reference strains used in this study.
Funding
This work was financially supported by the National Natural Science Foundation of China (No. 32070003), and the National Science and Technology Fundamental Resources Investigation Program of China (No. 2019FY100700).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Ethical statement
The article does not contain any studies related to human participants or animals.
Additional information
Communicated by Oren.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zheng, XW., Wu, ZP., Sun, YP. et al. Halorussus vallis sp. nov., Halorussus aquaticus sp. nov., Halorussus gelatinilyticus sp. nov., Halorussus limi sp. nov., Halorussus salilacus sp. nov., Halorussus salinisoli sp. nov.: six extremely halophilic archaea isolated from solar saltern, salt lake and saline soil. Extremophiles 26, 32 (2022). https://doi.org/10.1007/s00792-022-01280-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00792-022-01280-1