Skip to main content
Log in

Brachybacterium halotolerans sp. nov., a halotolerant, endophytic actinomycete isolated from branch of Bruguiera gymnoirhiza

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

A novel, aerobic, moderately halophilic Gram-positive actinomycete, strain MASK1Z-5T was isolated from a surface-sterilized branch of Bruguiera gymnoirhiza in Shankou Mangrove Nature Reserve, Guangxi, China. The taxonomic position of the strain was investigated using a polyphasic approach. Strain MASK1Z-5T tolerated up to 20% (w/v) NaCl (optimum 0–7%), and grew at pH 5.0–12.0 (optimum pH 7.0–8.0), 20–37 °C (optimum 30 °C). Phylogenetic analysis based on 16S rRNA gene sequences revealed that strain MASK1Z-5T belonged to the genus Brachybacterium, and showed the highest 16S rRNA gene sequence similarity of 98.0% to B. endophyticum M1HQ-2T. The cell-wall peptidoglycan contained meso-diaminopimelic acid as diagnostic diamino acid. MK-7 was the predominant menaquinone. The polar lipids comprised diphosphatidylglycerol, phosphatidylglycerol, one unidentified glycolipid and three unidentified lipids. The major fatty acids were anteiso-C15:0, iso-C16:0 and anteiso-C17:0. The DNA G + C content was calculated to be 71.8 mol% based on the whole genome sequence. The estimated values of average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) based on whole genome sequences between strain MASK1Z-5T and B. endophyticum M1HQ-2T were 81.8% and 25.0%, respectively. The phenotypic, chemotaxonomic and genotypic properties clearly indicated that strain MASK1Z-5T represents a novel species within the genus Brachybacterium, for which the name Brachybacterium halotolerans sp. nov. is proposed. The type strain is MASK1Z-5T (= CGMCC1.18660T = JCM 34339T).

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.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability statements

All data generated or analysed during this study are included in this published article, its supplementary information files and GenBank/EMBL/DDBJ.

References

  • Alanjary M, Steinke K, Ziemert N (2019) AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucl Acids Res 47(1):276–282

    Article  Google Scholar 

  • Bai X, Xiong Y, Lu S, Jin D, Lai X, Yang J, Niu L, Hu S, Meng X, Pu J, Ye C, Xu J (2016) Streptococcus pantholopis sp. nov. isolated from faeces of the tibetan antelope (pantholops hodgsonii). Int J Syst Evol Microbiol 66:3281–3286

    Article  CAS  PubMed  Google Scholar 

  • Bremer E, Krämer R (2019) Responses of microorganisms to osmotic stress. Ann Rev Microbiol 73:313–334

    Article  CAS  Google Scholar 

  • Collins MD, Brown J, Jones D (1988) Brachybacterium faecium gen. nov. sp. nov. a coryneform bacterium from poultry deep litter. Int J Syst Evol Microbiol 38:45–48

    CAS  Google Scholar 

  • Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Gontia I, Kavita K, Schmid M, Hartmann A, Jha B (2011) Brachybacterium saurashtrense sp. nov. a halotolerant root-associated bacterium with plant growth-promoting potential. Int J Syst Evol Microbiol 61:2799–2804

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gunde-Cimerman N, Plemenitaš A, Oren A (2018) Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiol Rev 42(3):353–375

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Tuo L, Habden X, Zhang YQ, Liu JM, Jiang ZK, Liu SW, Dilbar T, Sun CH (2015) Allosalinactinospora lopnorensis gen. nov. sp. nov. a new member of the family nocardiopsaceae isolated from soil. Int J Syst Evol Microbiol 65:206–213

    Article  CAS  PubMed  Google Scholar 

  • Heyrman J, Balcaen A, De Vos P, Schumann P, Swings J (2002) Brachybacterium fresconis sp. nov. and Brachybacterium sacelli sp. nov. isolated from deteriorated parts of a medieval wall painting of the chapel of castle herberstein (austria). Int J Syst Evol Microbiol 52:1641–1646

    CAS  PubMed  Google Scholar 

  • Kelly KL (1964) Inter-Society Color Council-National Bureau of Standards Color name Charts illustrated with Centroid Colors. US Government Printing Office, Washington, DC

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequence. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA 7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Gao C, Zhu L, Yu L, Qin M, Yan DM (2016) Diversity and cytotoxic activity of endophytic bacteria isolated from Sonneratia apetala of Maowei Sea. Acta Microbiol Sin 56:689–697

    Google Scholar 

  • Lim HJ, Lee EH, Yoon Y, Chua B, Son A (2016) Portable lysis apparatus for rapid single-step DNA extraction of Bacillus subtilis. J Appl Microbiol 120:379–387

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Xie QY, Shi W, Li L, An JY, Zhao YM, Hong K (2014) Brachybacterium huguangmaarense sp. nov. isolated from lake sediment. Int J Syst Evol Microbiol 64:1673–1678

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhai L, Yao S, Cao Y, Cao Y, Zhang X, Su J, Ge Y, Zhao R, Cheng C (2015) Brachybacterium hainanense sp. nov., isolated from noni (Morinda citrifolia L.) branch. Int J Syst Evol Microbiol 65:4196–4201

    Article  CAS  PubMed  Google Scholar 

  • Minnikin D, O’Donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241

    Article  CAS  Google Scholar 

  • Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42:206–214

    Article  Google Scholar 

  • Richter M, Rossellómóra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newslett 20:1–6

    Google Scholar 

  • Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert K, Ludwig W, Springer N, Kroppenstedt R, Accolas J, Fiedler F (1996) Two coryneform bacteria isolated from the surface of french gruyère and beaufort cheeses are new species of the genus Brachybacterium: Brachybacterium alimentarium sp. nov. and Brachybacterium tyrofermentans sp. nov. Int J Syst Bacteriol 46:81–87

    Article  CAS  PubMed  Google Scholar 

  • Shirling EB, Gottlieb D (1966) Methods for characterization of streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  • Tak EJ, Kim PS, Hyun DW, Kim HS, Lee JY, Kang W, Sung H, Shin NR, Kim MS, Whon TW, Bae JW (2018) Phenotypic and genomic properties of Brachybacterium vulturis sp. nov. and Brachybacterium avium sp. nov. Front Microbiol 9: 1809

  • Takeuchi M, Fang CX, Yokota A (1995) Taxonomic study of the genus Brachybacterium: proposal of Brachybacterium conglomeratum sp. nov., nom. rev., Brachybacterium paraconglomeratum sp. nov., and Brachybacterium rhamnosum sp. nov. Int J Syst Bacteriol 45:160–168

    Article  Google Scholar 

  • Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt K, Borodovsky M, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44(14):6614–6624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuo L, Dong YP, Habden X, Liu JM, Guo L, Liu XF, Chen L, Jiang ZK, Liu SW, Zhang YB, Zhang YQ, Sun CH (2015) Nocardioides deserti sp. nov. an actinobacterium isolated from desert soil. Int J Syst Evol Microbiol 65:1604–1610

    Article  CAS  PubMed  Google Scholar 

  • Tuo L, Yan XR, Li FN, Bao YX, Shi HC, Li HY, Sun CH (2018) Brachybacterium endophyticum sp. nov. a novel endophytic actinobacterium isolated from bark of scutellaria baicalensis georgi. Int J Syst Evol Microbiol 68:3563–3568

    Article  CAS  PubMed  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Truuper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Xu P, Li WJ, Tang SK, Zhang YQ, Chen GZ, Chen HH, Xu LH, Jiang CL (2005) Naxibacter alkalitolerans gen. nov. sp. nov. a novel member of the family 'oxalobacteraceae’ isolated from china. Int J Syst Evol Microbiol 55:1149–1153

    Article  CAS  PubMed  Google Scholar 

  • Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017a) Introducing ezbiocloud: a taxonomically united database of 16s rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017b) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was supported by the National Natural Sciences Foundation of China (NSFC, Grant No. 81960642) and Guizhou Provincial Science and Technology Foundation (No. Qian Ke He Jichu [2019]1347).

Author information

Authors and Affiliations

Authors

Contributions

Ming-Sheng Chen, Xiao-Rui Yan and Li Tuo collected plant samples, isolated strains and preliminary identification. Ming-Sheng Chen performed experiments and wrote the manuscript. Li Tuo and Fei-Na Li performed genome and chemotaxonomic analyses. Ming-Sheng Chen, Xiao-Rui Yan and Xiao-Hui Chen, performed initial physiological and morphological analyses of the strain. Li Tuo conceived and designed the experiments and approved the final manuscript.

Corresponding author

Correspondence to Li Tuo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

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.

Supplementary file1 (PDF 251 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, MS., Li, FN., Chen, XH. et al. Brachybacterium halotolerans sp. nov., a halotolerant, endophytic actinomycete isolated from branch of Bruguiera gymnoirhiza. Antonie van Leeuwenhoek 114, 875–884 (2021). https://doi.org/10.1007/s10482-021-01565-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-021-01565-z

Keywords

Navigation