Abstract
A Gram-strain-negative, rod-shaped, aerobic bacterium, designated strain TRM 85114T, was isolated from the Jincaotan wetland in the Pamir Plateau of China. This strain grew optimally at 30 °C and pH 6.0 in the presence of 3% (w/v) NaCl. Phylogenetic analysis of 16S rRNA gene sequences revealed that strain TRM 85114T was affiliated with the genus Halomonas, and shared high sequence similarity with Halomonas korlensis XK1T (97.3%) and Halomonas tibetensis pyc13T (96.4%). Strain TRM 85114T contained C16:0 and C19:0 cyclo ω8c as primary cellular fatty acids, Q-9 as predominate respiratory quinone, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, phospholipids of unknown structure containing glucosamine, unidentified aminophospholipids, unidentified lipids and three unidentified phospholipids as the major polar lipids. The complete genome of TRM 85114T comprised 3,902 putative genes with a total of 4,126,476 bp and a G + C content of 61.6%. The average nucleotide identity and digital DNA–DNA hybridization values between strain TRM 85114T and related type Halomonas strains of H. korlensis XK1T, H. tibetensis pyc13T, Chromohalobacter salexigens DSM 6768T, and Halomonas urumqiensis BZ-SZ-XJ27T were 75.4–88.9% and 22.9–39.2%, respectively. Based on phenotypic, chemotaxonomic, and molecular features, strain TRM 85114T represents a novel species of the genus Halomonas, for which the name is proposed as Halomonas jincaotanensis sp. nov.. The type strain is TRM 85114T (CCTCC AB 2021006T = LMG 32311T). The amount of 1-naphthylamine degradation by strain TRM 85114T reached up to 32.0 mg/L in 14 days.
Similar content being viewed by others
References
Al Farraj DA, Hadibarata T, Yuniarto A, Alkufeidy RM, Alshammari MK, Syafiuddin A (2020) Exploring the potential of halotolerant bacteria for biodegradation of polycyclic aromatic hydrocarbon. Bioprocess Biosyst Eng 43:2305–2314. https://doi.org/10.1007/s00449-020-02415-4
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Arahal DR, Vreeland RH, Litchfield CD, Mormile MR, Tindall BJ, Oren A, Bejar V, Quesada E, Ventosa A (2007) Recommended minimal standards for describing new taxa of the family Halomonadaceae. Int J Syst Evol Microbiol 57:2436–2446. https://doi.org/10.1099/ijs.0.65430-0
Athalye M, Noble WC, Minnikin DE (1985) Analysis of cellular fatty acids by gas chromatography as a tool in the identification of medically important coryneform bacteria. J Appl Bacteriol 58:507–512. https://doi.org/10.1111/j.1365-2672.1985.tb01491.x
Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973. https://doi.org/10.1093/bioinformatics/btp348
Collins MD, Jones D (1981) Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol Rev 45:316–354. https://doi.org/10.1128/mr.45.2.316-354.1981
Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230. https://doi.org/10.1099/00221287-100-2-221
Czelusniak J, Goodman M, Moncrief ND, Kehoe SM (1990) Maximum parsimony approach to construction of evolutionary trees from aligned homologous sequences. Methods Enzymol 183:601–615. https://doi.org/10.1016/0076-6879(90)83039-c
de la Haba RR, Marquez MC, Papke RT, Ventosa A (2012) Multilocus sequence analysis of the family Halomonadaceae. Int J Syst Evol Microbiol 62:520–538. https://doi.org/10.1099/ijs.0.032938-0
Dou G, He W, Liu H, Ma Y (2015) Halomonas heilongjiangensis sp. nov., a novel moderately halophilic bacterium isolated from saline and alkaline soil. Antonie Van Leeuwenhoek 108:403–413. https://doi.org/10.1007/s10482-015-0493-4
Du H, Zhao Y, Wu F, Ouyang P, Chen J, Jiang X, Ye J, Chen GQ (2020) Engineering Halomonas bluephagenesis for L-Threonine production. Metab Eng 60:119–127. https://doi.org/10.1016/j.ymben.2020.04.004
Dyall-Smith M (2015) The Halohandbook. http://www.haloarchaea.com/resources/halohandbook/
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:238. https://doi.org/10.1186/s13059-019-1832-y
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol Int J Org Evol 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Govarthanan M, Khalifa AY, Kamala-Kannan S, Srinivasan P, Selvankumar T, Selvam K, Kim W (2020) Significance of allochthonous brackish water Halomonas sp. on biodegradation of low and high molecular weight polycyclic aromatic hydrocarbons. Chemosphere 243:125389. https://doi.org/10.1016/j.chemosphere.2019.125389
Hu J, Shao D, Chen C, Sheng G, Ren X, Wang X (2011) Removal of 1-naphthylamine from aqueous solution by multiwall carbon nanotubes/iron oxides/cyclodextrin composite. J Hazard Mater 185:463–471. https://doi.org/10.1016/j.jhazmat.2010.09.055
Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11:119. https://doi.org/10.1186/1471-2105-11-119
Jackman SD, Vandervalk BP, Mohamadi H, Chu J, Yeo S, Hammond SA, Jahesh G, Khan H, Coombe L, Warren RL, Birol I (2017) ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter. Genome Res 27:768–777. https://doi.org/10.1101/gr.214346.116
Jiang XR, Yin J, Chen XB, Chen GQ (2018) Halomonas and pathway engineering for bioplastics production. Methods Enzymol 608:309–328. https://doi.org/10.1016/bs.mie.2018.04.008
Jiang XR, Yan X, Yu LP, Liu XY, Chen GQ (2021) Hyperproduction of 3-hydroxypropionate by Halomonas bluephagenesis. Nat Commun 12:1513. https://doi.org/10.1038/s41467-021-21632-3
Kazemi E, Tarhriz V, Amoozegar MA, Hejazi MS (2021) Halomonas azerbaijanica sp. nov., a halophilic bacterium isolated from Urmia Lake after the 2015 drought. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.004578
Kim M, Oh HS, Park SC, 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. https://doi.org/10.1099/ijs.0.059774-0
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/bf01731581
Koh HW, Rani S, Kim SJ, Moon E, Nam SW, Rhee SK, Park SJ (2017) Halomonas aestuarii sp. nov., a moderately halophilic bacterium isolated from a tidal flat. Int J Syst Evol Microbiol 67:4298–4303. https://doi.org/10.1099/ijsem.0.001824
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lee I, Ouk Kim Y, Park SC, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. https://doi.org/10.1099/ijsem.0.000760
Li HB, Zhang LP, Chen SF (2008) Halomonas korlensis sp. nov., a moderately halophilic, denitrifying bacterium isolated from saline and alkaline soil. Int J Syst Evol Microbiol 58:2582–2588. https://doi.org/10.1099/ijs.0.65711-0
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964. https://doi.org/10.1093/nar/25.5.955
Lu HB, Xing P, Zhai L, Phurbu D, Tang Q, Wu QL (2018) Halomonas tibetensis sp. nov., isolated from saline lakes on Tibetan Plateau. J Microbiol 56:493–499. https://doi.org/10.1007/s12275-018-8076-5
Mata JA, Martinez-Canovas J, Quesada E, Bejar V (2002) A detailed phenotypic characterisation of the type strains of Halomonas species. Syst Appl Microbiol 25:360–375. https://doi.org/10.1078/0723-2020-00122
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60. https://doi.org/10.1186/1471-2105-14-60
Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933–2935. https://doi.org/10.1093/bioinformatics/btt509
Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J, Finn RD (2015) Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 43:D130-137. https://doi.org/10.1093/nar/gku1063
Nguyen HT, Nielsen JL, Nielsen PH (2012) 'Candidatus Halomonas phosphatis’, a novel polyphosphate-accumulating organism in full-scale enhanced biological phosphorus removal plants. Environ Microbiol 14:2826–2837. https://doi.org/10.1111/j.1462-2920.2012.02826.x
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. https://doi.org/10.1101/gr.186072.114
Parsons JG, Patton S (1967) Two-dimensional thin-layer chromatography of polar lipids from milk and mammary tissue. J Lipid Res 8:696–698. https://doi.org/10.1016/S0022-2275(20)38896-9
Poli A, Nicolaus B, Denizci AA, Yavuzturk B, Kazan D (2013) Halomonas smyrnensis sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 63:10–18. https://doi.org/10.1099/ijs.0.037036-0
Premnath N, Mohanrasu K, Guru Raj Rao R, Dinesh GH, Prakash GS, Ananthi V, Ponnuchamy K, Muthusamy G, Arun A (2021) A crucial review on polycyclic aromatic Hydrocarbons - Environmental occurrence and strategies for microbial degradation. Chemosphere 280:130608. https://doi.org/10.1016/j.chemosphere.2021.130608
Qu L, Lai Q, Zhu F, Hong X, Zhang J, Shao Z, Sun X (2011) Halomonas daqiaonensis sp. nov., a moderately halophilic, denitrifying bacterium isolated from a littoral saltern. Int J Syst Evol Microbiol 61:1612–1616. https://doi.org/10.1099/ijs.0.026344-0
Ramezani M, Pourmohyadini M, Nikou MM, Makzum S, Schumann P, Clermont D, Criscuolo A, Amoozegar MA, Kampfer P, Sproer C (2020) Halomonas lysinitropha sp. nov., a novel halophilic bacterium isolated from a hypersaline wetland. Int J Syst Evol Microbiol 70:6098–6105. https://doi.org/10.1099/ijsem.0.004504
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Tuma S, Izaguirre JK, Bondar M, Marques MM, Fernandes P, da Fonseca MMR, Cesario MT (2020) Upgrading end-of-line residues of the red seaweed Gelidium sesquipedale to polyhydroxyalkanoates using Halomonas boliviensis. Biotechnol Rep (amst) 27:e00491. https://doi.org/10.1016/j.btre.2020.e00491
Vreeland R, Litchfield C, Martin E, Elliot E (1980) Halomonas elongata, a new genus and species of extremely salttolerant bacteria. Int J Syst Evol Microbiol 30:485–495. https://doi.org/10.1099/00207713-30-2-485
Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Truper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 37:463–464. https://doi.org/10.1099/00207713-37-4-463
Williamson A, De Santi C, Altermark B, Karlsen C, Hjerde E (2016) Complete genome sequence of Halomonas sp. R5–57. Stand Genom Sci 11:62. https://doi.org/10.1186/s40793-016-0192-4
Xu L, Xu XW, Meng FX, Huo YY, Oren A, Yang JY, Wang CS (2013) Halomonas zincidurans sp. nov., a heavy-metal-tolerant bacterium isolated from the deep-sea environment. Int J Syst Evol Microbiol 63:4230–4236. https://doi.org/10.1099/ijs.0.051656-0
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yu LP, Wu FQ, Chen GQ (2019) Next-generation industrial biotechnology-transforming the current industrial biotechnology into competitive processes. Biotechnol J 14:e1800437. https://doi.org/10.1002/biot.201800437
Zhang S, Pan J, Lu W, Yan Y, Wang H, Wiegel J, Zhao B (2016) Halomonas urumqiensis sp. nov., a moderately halophilic bacterium isolated from a saline-alkaline lake. Int J Syst Evol Microbiol 66:1962–1969. https://doi.org/10.1099/ijsem.0.000975
Zhong ZP, Liu Y, Wang F, Zhou YG, Liu HC, Liu ZP (2016) Lacimicrobium alkaliphilum gen. nov., sp. nov., a member of the family Alteromonadaceae isolated from a salt lake. Int J Syst Evol Microbiol 66:422–429. https://doi.org/10.1099/ijsem.0.000735
Acknowledgements
This study was supported by the National Natural Science Foundation of China (31900007), Bingtuan Science and Technology Program (2018BC008), the Microbial Resources Utilization Innovation Team in Key Field of Xin Jiang Production and Construction Corps (2017CB014), and the principal fund (TDHNLH201604).
Funding
This study was supported by the National Natural Science Foundation of China (31900007), Bingtuan Science and Technology Program (2018BC008), the Microbial Resources Utilization Innovation Team in Key Field of Xin Jiang Production and Construction Corps (2017CB014), and the principal fund (TDHNLH201604).
Author information
Authors and Affiliations
Contributions
XB performed the experiments, analyzed the data, and drafted the manuscript. ZL conducted the degradation test of 1-naphthylamine. ZX, CW, and MR critically revised the manuscript. LZ contributed to the creation. All authors read and approved the manuscript. We thank HC and PX for finding and providing Halomonas tibetensis pyc13T.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare no conflict of interest.
Ethical approval
No specific ethical or institutional permission was required for sampling, and our experimental studies did not involve endangered or protected species.
Additional information
Communicated by Erko Stackebrandt.
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
About this article
Cite this article
Bu, X., Xia, Z., Liu, Z. et al. Halomonas jincaotanensis sp. nov., isolated from the Pamir Plateau degrading polycyclic aromatic hydrocarbon. Arch Microbiol 204, 398 (2022). https://doi.org/10.1007/s00203-022-03008-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03008-3