1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 73, Issue 6

sp. nov. and sp. nov., two novel halophilic actinobacteria isolated from halophytes No Access

Abstract

A polyphasic approach was used to describe two halophilic actinobacterial strains, designated LSu2-4 and RSe5-2, which were isolated from halophytes [ (L.) Dum. and (L.) L.] collected from Prachuap Khiri Khan province, Thailand. Comparative analysis of 16S rRNA gene sequences showed that strains LSu2-4 and RSe5-2 were assigned to the genus , with YIM 90109(99.2 and 99.2 % similarities, respectively) and DSM 44494(99.0 and 98.8 % similarities, respectively) being their closely related strains. Whereas the 16S rRNA gene sequence similarity between LSu2-4 and RSe5-2 was 99.4 %. Phylogenetic and phylogenomic analyses based on 16S rRNA gene and whole-genome sequences revealed that both strains clustered with YIM 90109 and DSM 44494. The average nucleotide identity (ANI) based on , ANI based on MUMmer and digital DNA–DNA hybridization (dDDH) relatedness values between the two strains and their closest type strains were below the threshold values for identifying a novel species. Morphological characteristics and chemotaxonomic features of both strains were typical for the genus by formed well-developed substrate mycelia and aerial mycelia which fragmented into rod-shaped spores. Whole-cell hydrolysates contained -diaminopimelic acid as the diagnostic diamino acid. The predominant menaquinones were variously hydrogenated with 10 isoprene units and contained phosphatidylcholine in their polar lipid profiles. Major fatty acids were iso-C and 10-methyl C. analysis predicted that the genomes of LSu2-4 and RSe5-2 contained genes associated with stress responses and biosynthetic gene clusters encoding diverse bioactive metabolites. Characterization based on chemotaxonomic, phenotypic, genotypic and phylogenetic evidence demonstrated that strains LSu2-4 and RSe5-2 represents two novel species of the genus , for which the names sp. nov. (type strain LSu2-4=TBRC 16415=NBRC 115855) and sp. nov. (type strain RSe5-2=TBRC 16416=NBRC 115856) are proposed.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): actinobacteria , halophytes , Nocardiopsis and polyphasic taxonomy
Funding
This study was supported by the:
  • Kasetsart University, Biodiversity Center Kasetsart University (Award Post-master research scholarship)
    • Principle Award Recipient: TanatornChantavorakit
  • Kasetsart University, Biodiversity Center Kasetsart University (Award Post-master research scholarship)
    • Principle Award Recipient: KannikaDuangmal
© 2023 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005948
2023-06-22
2024-05-03
Loading full text...

Full text loading...

References

  1. Yuan F, Xu Y, Leng B, Wang B. Beneficial effects of salt on halophyte growth: morphology, cells, and genes. Open Life Sci 2019; 14:191–200 [View Article] [PubMed]
     [Google Scholar]
  2. Qin S, Feng W-W, Zhang Y-J, Wang T-T, Xiong Y-W et al. Diversity of bacterial microbiota of coastal halophyte Limonium sinense and amelioration of salinity stress damage by symbiotic plant growth-promoting actinobacterium Glutamicibacter halophytocola KLBMP 5180. Appl Environ Microbiol 2018; 84:e01533-18 [View Article] [PubMed]
     [Google Scholar]
  3. Qin S, Feng W-W, Wang T-T, Ding P, Xing K et al. Plant growth-promoting effect and genomic analysis of the beneficial endophyte Streptomyces sp. KLBMP 5084 isolated from halophyte Limonium sinense. Plant Soil 2017; 416:117–132 [View Article]
     [Google Scholar]
  4. Gao L, Huang Y, Liu Y, Mohamed OAA, Fan X et al. Bacterial community structure and potential microbial coexistence mechanism associated with three halophytes adapting to the extremely hypersaline environment. Microorganisms 2022; 10:1124 [View Article] [PubMed]
     [Google Scholar]
  5. Meyer J. Nocardiopsis, a new genus of the order Actinomycetales. Int J Syst Evol Microbiol 1976; 26:487–493 [View Article]
     [Google Scholar]
  6. Tang S-K, Li W-J, Dong W, Zhang Y-G, Xu L-H et al. Studies of the biological characteristics of some halophilic and halotolerant actinomycetes isolated from saline and alkaline soils. Actinomycetologica 2003; 17:6–10 [View Article]
     [Google Scholar]
  7. He S-T, Zhi X-Y, Jiang H, Yang L-L, Wu J-Y et al. Biogeography of Nocardiopsis strains from hypersaline environments of Yunnan and Xinjiang Provinces, western China. Sci Rep 2015; 5:13323 [View Article] [PubMed]
     [Google Scholar]
  8. Ibrahim AH, Desoukey SY, Fouad MA, Kamel MS, Gulder TAM et al. Natural product potential of the genus Nocardiopsis. Mar Drugs 2018; 16:147 [View Article] [PubMed]
     [Google Scholar]
  9. Muangham S, Suksaard P, Mingma R, Matsumoto A, Takahashi Y et al. Nocardiopsis sediminis sp. nov., isolated from mangrove sediment. Int J Syst Evol Microbiol 2016; 66:3835–3840 [View Article] [PubMed]
     [Google Scholar]
  10. Li F, Xie Q, Zhou S, Kong F, Xu Y et al. Nocardiopsis coralli sp. nov. a novel actinobacterium isolated from the coral Galaxea astreata. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
     [Google Scholar]
  11. Chen Y-G, Zhang Y-Q, Tang S-K, Liu Z-X, Xu L-H et al. Nocardiopsis terrae sp. nov., a halophilic actinomycete isolated from saline soil. Antonie van Leeuwenhoek 2010; 98:31–38 [View Article] [PubMed]
     [Google Scholar]
  12. Yang R, Zhang L-P, Guo L-G, Shi N, Lu Z et al. Nocardiopsis valliformis sp. nov., an alkaliphilic actinomycete isolated from alkali lake soil in China. Int J Syst Evol Microbiol 2008; 58:1542–1546 [View Article] [PubMed]
     [Google Scholar]
  13. Al-Zarban SS, Abbas I, Al-Musallam AA, Steiner U, Stackebrandt E et al. Nocardiopsis halotolerans sp. nov., isolated from salt marsh soil in Kuwait. Int J Syst Evol Microbiol 2002; 52:525–529 [View Article] [PubMed]
     [Google Scholar]
  14. Zhang Y-G, Liu Q, Wang H-F, Park D-J, Guo J-W et al. Nocardiopsis ansamitocini sp. nov., a new producer of ansamitocin P-3 of the genus Nocardiopsis. Int J Syst Evol Microbiol 2016; 66:230–235 [View Article] [PubMed]
     [Google Scholar]
  15. Asem MD, Salam N, Idris H, Zhang X-T, Bull AT et al. Nocardiopsis deserti sp. nov., isolated from a high altitude Atacama Desert soil. Int J Syst Evol Microbiol 2020; 70:3210–3218 [View Article] [PubMed]
     [Google Scholar]
  16. Bennur T, Kumar AR, Zinjarde S, Javdekar V. Nocardiopsis species: Incidence, ecological roles and adaptations. Microbiol Res 2015; 174:33–47 [View Article] [PubMed]
     [Google Scholar]
  17. Lechevalier MP, Lechevalier H. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 1970; 20:435–443 [View Article]
     [Google Scholar]
  18. Chantavorakit T, Suksaard P, Matsumoto A, Duangmal K. Amycolatopsis suaedae sp. nov., an endophytic actinomycete isolated from Suaeda maritima roots. Int J Syst Evol Microbiol 2019; 69:2591–2596 [View Article] [PubMed]
     [Google Scholar]
  19. KÜSter E, Williams ST. Selection of media for isolation of streptomycetes. Nature 1964; 202:928–929 [View Article] [PubMed]
     [Google Scholar]
  20. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  21. Lee I, Chalita M, Ha S-M, Na S-I, Yoon S-H et al. ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 2017; 67:2053–2057 [View Article] [PubMed]
     [Google Scholar]
  22. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
     [Google Scholar]
  23. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
     [Google Scholar]
  24. Tarlachkov S, Starodumova I. Taxondc: calculating the similarity value of the 16S rRNA gene sequences of prokaryotes or ITS regions of fungi. J Bioinf Genom 2017; 3:1–4
     [Google Scholar]
  25. Mingma R, Pathom-aree W, Trakulnaleamsai S, Thamchaipenet A, Duangmal K. Isolation of rhizospheric and roots endophytic actinomycetes from Leguminosae plant and their activities to inhibit soybean pathogen, Xanthomonas campestris pv. glycine. World J Microbiol Biotechnol 2014; 30:271–280 [View Article] [PubMed]
     [Google Scholar]
  26. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
     [Google Scholar]
  27. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
     [Google Scholar]
  28. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 1971; 20:406–416 [View Article]
     [Google Scholar]
  29. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article]
     [Google Scholar]
  30. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
     [Google Scholar]
  31. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
     [Google Scholar]
  32. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
     [Google Scholar]
  33. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
     [Google Scholar]
  34. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
     [Google Scholar]
  35. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
     [Google Scholar]
  36. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  37. Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP et al. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 2021; 49:W29–W35 [View Article] [PubMed]
     [Google Scholar]
  38. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
     [Google Scholar]
  39. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
     [Google Scholar]
  40. Kaweewan I, Komaki H, Hemmi H, Kodani S. Isolation and structure determination of a new thiopeptide globimycin from Streptomyces globisporus subsp. globisporus based on genome mining. Tetrahedron Letters 2018; 59:409–414 [View Article]
     [Google Scholar]
  41. Hutchinson CR. Biosynthetic studies of daunorubicin and tetracenomycin C. Chem Rev 1997; 97:2525–2536 [View Article] [PubMed]
     [Google Scholar]
  42. Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F, Girard G, Yáñez-Guerra LA et al. The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biol Evol 2013; 5:1165–1175 [View Article] [PubMed]
     [Google Scholar]
  43. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
     [Google Scholar]
  44. Mundie D. The NBS/ISCC Color System Pittsburgh, PA: Polymath Systems; 1995
     [Google Scholar]
  45. Gordon RE, Barnett DA, Handerhan JE, Pang C-N. Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 1974; 24:54–63 [View Article]
     [Google Scholar]
  46. Williams ST, Goodfellow M, Alderson G, Wellington EM, Sneath PH et al. Numerical classification of Streptomyces and related genera. J Gen Microbiol 1983; 129:1743–1813 [View Article] [PubMed]
     [Google Scholar]
  47. Gordon RE, Mihm JM. A comparative study of some strains received as nocardiae. J Bacteriol 1957; 73:15–27 [View Article] [PubMed]
     [Google Scholar]
  48. Becker B, Lechevalier M, Lechevalier H. Chemical composition of cell-wall preparations from strains of various form-genera of aerobic actinomycetes. Appl Microbiol 1965; 13:236–243 [View Article] [PubMed]
     [Google Scholar]
  49. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article] [PubMed]
     [Google Scholar]
  50. Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 1983; 29:319–322 [View Article]
     [Google Scholar]
  51. Tomiyasu I. Mycolic acid composition and thermally adaptative changes in Nocardia asteroides. J Bacteriol 1982; 151:828–837 [View Article] [PubMed]
     [Google Scholar]
  52. Minnikin D, Patel P, Alshamaony L, Goodfellow M. Polar lipid composition in the classification of Nocardia and related bacteria. Int J Syst Bacteriol 1977; 27:104–117 [View Article]
     [Google Scholar]
  53. Collins MD, Pirouz T, Goodfellow M, Minnikin DE. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 1977; 100:221–230 [View Article] [PubMed]
     [Google Scholar]
  54. Wu C, Lu X, Qin M, Wang Y, Ruan J. Analysis of menaquinone compound in microbial cells by HPLC. Microbiology 1989; 16:176–178
     [Google Scholar]
  55. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. In Technical Note No. 101 vol 101 Newark, DE: MIDI, Inc; 2001 pp 1–7
     [Google Scholar]
  56. Lechevalier MP, De Bievre C, Lechevalier H. Chemotaxonomy of aerobic actinomycetes: phospholipid composition. Biochem Syst Ecol 1977; 5:249–260 [View Article]
     [Google Scholar]
  57. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
     [Google Scholar]
  58. Li W-J, Kroppenstedt RM, Wang D, Tang S-K, Lee J-C et al. Five novel species of the genus Nocardiopsis isolated from hypersaline soils and emended description of Nocardiopsis salina Li et al. 2004. Int J Syst Evol Microbiol 2006; 56:1089–1096 [View Article] [PubMed]
     [Google Scholar]
  59. Al-tai AM, Ruan J-S. Nocardiopsis halophila sp. nov., a new halophilic actinomycete isolated from soil. Int J Syst Evol Microbiol 1994; 44:474–478 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005948
Loading
Nocardiopsis suaedae sp. nov. and Nocardiopsis endophytica sp. nov., two novel halophilic actinobacteria isolated from halophytes
Int J Syst Evol Microbiol 73, 005948 (2023); https://doi.org/10.1099/ijsem.0.005948
/content/journal/ijsem/10.1099/ijsem.0.005948
/content/journal/ijsem/10.1099/ijsem.0.005948
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error