Abstract
Two novel actinobacteria, strain PSKA28T and PSKA54T were isolated from soil sample of Kashmir-Himalaya, India (latitude 34°-01′ N; longitude 74°-47′ E; altitude 5328 ft). Polyphasic-taxonomic analysis revealed that these strains belong to the genus Streptomyces. The 16S rRNA gene-sequence similarity of these strain were highest (98.6%) with that of the Streptomyces torulosus NRRLB-3889T. They showed 92.1% gyrB gene-sequence similarity but 92.9 and 94.6% rpoB gene-sequence similarity, respectively, with Streptomyces torulosus NRRLB-3889T. The sequence similarities were significantly lower than the recommended threshold value for novel taxonomic position and the 16S rRNA sequence-based phylogenetic analysis indicated that these two isolates are in distinct clade. Phylogenomic analysis with their genome sequences, conferred by Type Strain Genome Server separated them from rest of the Streptomyces type strains. The cell wall contained ll-diaminopimelic acid and the whole-cell hydrolysate contained glucose and ribose. Major fatty acid methyl esters were 15:0 anteiso, 16:0 iso and 17:0 anteiso. Average nucleotide identity, average amino acid identity and digital DNA–DNA hybridization (dDDH) values as well as evolutionary distance based on multilocus sequence analysis, between closely related type strains and either of the strain PSKA28T or PSKA54T, were considerably lower than the recommended threshold value (< 70% dDDH or < 95–96% ANI/AAI or > 0.007 MLSA distance). Therefore, these isolates represent a novel Streptomyces species, for which we proposed the name Streptomyces himalayensis sp. nov. Genotypic and phenotypic analyses clearly split these strains into two closely related sub-clusters. Based on this, two novel subspecies Streptomyces himalayensis subsp. himalayensis subsp. nov. and Streptomyces himalayensis subsp. aureolus subsp. nov. are proposed, with type strains JCM33755T (= MTCC12933T, MCC4145T) and JCM33759T (= MTCC12938, MCC4180), respectively.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- BA:
-
Bennett’s agar
- ISP:
-
International Streptomyces Project
- GGDC:
-
Genome-to-genome distance calculator
- MLSA:
-
Multilocus sequence analysis
- dDDH:
-
Digital DNA–DNA hybridization
- ANI:
-
Average nucleotide identity
- AAI:
-
Average amino acid identity
- TYGS:
-
Type strain genome server
- NRPS:
-
Non-ribosomal polypeptide synthetases
- PKS:
-
Polyketide synthase
References
Adékambi T, Drancourt M, Raoult D (2009) The rpoB gene as a tool for clinical microbiologists. Trends Microbiol 17:37–45. https://doi.org/10.1016/j.tim.2008.09.008
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P et al (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43. https://doi.org/10.1128/MMBR.00019-15
Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26. https://doi.org/10.1038/ja.2005.1
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, Costa MSD 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. https://doi.org/10.1099/ijsem.0.002516
Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–668. www.jstor.org/stable/2459725
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
Fitch WM (1971) Towards defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:400–416. https://www.jstor.org/stable/2412116
Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216. https://doi.org/10.1146/annurev.mi.37.100183.001201
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. https://doi.org/10.1099/ijs.0.64483-0
Guo Y, Zheng W, Rong X, Huang Y (2008) A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 58:149–159. https://doi.org/10.1099/ijs.0.65224-0
Jia F, Liu C, Zhao J, Zhang Y, Li L, Zhou S, Shen Y et al (2015) Streptomyces vulcanius sp. nov., a novel actinomycete isolated from volcanic sediment. Anton van Leeuwenhoek 107:15–21. https://doi.org/10.1007/s10482-014-0299-9
Kämpfer P, Kroppenstedt RM (1996) Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 42:989–1005. https://doi.org/10.1139/m96-128
Kim KO, Shin KS, Kim MN, Shin KS, Labeda DP et al (2012) Reassessment of the status of Streptomyces setonii and reclassification of Streptomyces fimicarius as a later synonym of Streptomyces setonii and Streptomyces albovinaceus as a later synonym of Streptomyces globisporus based on combined 16S rRNA/gyrB gene sequence analysis. Int J Syst Evol Microbiol 62:2978. https://doi.org/10.1099/ijs.0.040287-0
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 rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Kimura M (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge
Kirby BM, Everest GJ, Meyers PR (2010) Phylogenetic analysis of the genus Kribbella based on the gyrB gene: proposal of a gyrB sequence threshold for species delineation in the genus Kribbella. Anton van Leeuwenhoek 97:131–142. https://doi.org/10.1007/s10482-009-9393-9
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger data sets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lefort V, Desper R, Gascuel O (2015) FastME 2.0: A comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800. https://doi.org/10.1093/molbev/msv150
Lyons AJ, Pridham TG (1971) Streptomyces torulosus sp. nov., an unusual knobby-spored taxon. Appl Microbiol 22:190–193
Maiti PK, Mandal S (2019) Majority of actinobacterial strains isolated from Kashmir Himalaya soil are rich source of antimicrobials and industrially important biomolecules. Adv Microbiol 9:220–238. https://doi.org/10.4236/aim.2019.93016
Maiti PK, Mandal S (2020) Lentzea indica sp. nov., a novel actinobacteria isolated from Indian Himalayan-soil. Anton van Leeuwenhoek. https://doi.org/10.1007/s10482-020-01449-8
Maiti PK, Das S, Sahoo P, Mandal S (2020) Streptomyces sp. SM01 isolated from Indian soil produces a novel antibiotic picolinamycin effective against multi drug resistant bacterial strains. Sci Rep 10:10092. https://doi.org/10.1038/s41598-020-66984-w
Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218. https://doi.org/10.1016/S0022-2836(61)80047-8
Mayfield CI, Williams ST, Ruddick SM, Hatfield HL (1972) Studies on the ecology of actinomycetes in soil. IV. Observations on the form and growth of Streptomycetes in soil. Soil Biol Biochem 4:79–91. https://doi.org/10.1016/0038-0717(72)90045-4
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:2182. https://doi.org/10.1038/s41467-019-10210-3
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
Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al (2014) Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genom Sci 10:2
Mohammadipanah F, Wink J (2016) Actinobacteria from arid and desert habitats: diversity and biological activity. Front Microbiol 6:1541. https://doi.org/10.3389/fmicb.2015.01541
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131. https://doi.org/10.1073/pnas.0906412106
Rodriguez LMR, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. Peer J Preprints 4:e1900v1
Rong X, Huang Y (2010) Taxonomic evaluation of the Streptomyces griseus clade using multilocus sequence analysis and DNA:DNA hybridisation with proposal to combine 29 species and three subspecies as 11 genomic species. Int J Syst Evol Microbiol 60:696–703. https://doi.org/10.1099/ijs.0.012419-0
Rong X, Huang Y (2012) Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Syst Appl Microbiol 35:7–18. https://doi.org/10.1016/j.syapm.2011.10.004
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
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101. MIDI Inc., Newark, DE, USA
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340. https://doi.org/10.1099/00207713-16-3-313
Sripreechasak P, Phongsopitanun W, Tamura T, Tanasupawat S (2017) Streptomyces krungchingensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 67:50–54. https://doi.org/10.1099/ijsem.0.001570
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Bio Evol 9:678–687
Thompson CC, Thompson FL, Vandemeulebroecke K, Hoste B, Dawyndt P et al (2004) Use of recA as an alternative phylogenetic marker in the family Vibrionaceae. Int J Syst Evol Microbiol 54:919–924. https://doi.org/10.1099/ijs.0.02963-0
Thumar JT, Dhulia K, Singh SP (2010) Isolation and partial purification of an antimicrobial agent from halotolerant alkaliphilic Streptomyces aburaviensis strain Kut-8. World J Microbiol Biotechnol 26:2081–2087. https://doi.org/10.1007/s11274-010-0394-7
Tiwari K, Gupta RK (2012) Rare actinomycetes: a potential store house for novel antibiotics. Crit Rev Biotechnol 32:108–132. https://doi.org/10.3109/07388551.2011.562482
Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464. https://doi.org/10.1099/00207713-37-4-463
Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA et al (1983) Numerical classification of Streptomyces and related genera. Microbiol 129:1743–1813. https://doi.org/10.1099/00221287-129-6-1743
Yoon SH, Ha SM, Kwon S, Lim J, KimY, et al (2017) Introducing EzBio-Cloud: 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
Acknowledgements
We are grateful to SERB (DST), Govt of India, for financial support (grant No.: SB/YS/LS-154/2013 dated 05.12.2013) which has been partially used for this research.
Author information
Authors and Affiliations
Contributions
PKM performed the experiments. PKM and SM conceptualized the idea, designed the experiments, analyzed the data, and wrote the manuscript. SM helps in fund acquisition, reviewed, and edited the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no conflict of interest.
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
Maiti, P.K., Mandal, S. Streptomyces himalayensis sp. nov. including Streptomyces himalayensis subsp. himalayensis subsp. nov. and Streptomyces himalayensis subsp. aureolus subsp. nov. isolated from Western Himalaya. Arch Microbiol 203, 2325–2334 (2021). https://doi.org/10.1007/s00203-021-02232-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-021-02232-7