Skip to main content
Log in

Streptomyces telluris sp. nov., a promising terrestrial actinobacterium with antioxidative potentials

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

An actinomycete strain, AA8T, which produced a long straight chain of spores (verticillati type), was isolated from the rhizosphere soil of Mangifera indica in Bangkok, Thailand. A polyphasic taxonomic study was carried out to establish the taxonomic position of the strain. Strain AA8T formed a tight taxonomic position in the 16S rRNA gene tree with Streptomyces roseifaciens MBT76T. In contrast, the genome-based taxonomic analysis showed that strain AA8T shared low average nucleotide identity-BLAST (94.1%), the digital DNA–DNA hybridization (58.2%), and the average amino acid identity (93.6%) values with S. roseifaciens MBT76T. Moreover, a combination of physiological and biochemical properties indicated that strain AA8T was distinguished from all Streptomyces species with effectively published names. Strain AA8T, therefore, represents a novel species of Streptomyces, and the name Streptomyces telluris is proposed for the strain. The type strain is AA8T (= TBRC 8483T = NBRC 113461T). The chemical investigation led to the isolation of nine known compounds (compounds 19). Among these compounds, compound 7 (3,4-dihydroxybenzaldehyde) possesses strong antioxidant activity equal to ascorbic acid, a powerful antioxidative agent.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All the data generated in this study have been included in this published article and its supplementary information files. The 16S rRNA gene and the whole-genome sequences of strain AA8T have been deposited in the GenBank databases with the accession numbers LC377949 and JANIID000000000, respectively.

Abbreviations

AAI:

Average amino acid identity

ANIb:

Average nucleotide identity-BLAST

DAP:

Diaminopimelic acid

dDDH:

Digital DNA–DNA hybridization

GBDP:

Genome blast distance phylogeny

GGDC:

Genome-to-Genome Distance Calculator

GL:

Glycolipid

HPLC:

High-performance liquid chromatography

ISCC-NBS:

Inter-Society Color Council-the National Bureau of Standards

ISP:

International Streptomyces Project

Ls:

Unidentified lipids

MK:

Menaquinone

ML:

Maximum-likelihood

PE:

Phosphatidylethanolamine

NPG:

Ninhydrin-positive lipid

PI:

Phosphatidylinositol

PLs:

Unidentified phospholipids

NJ:

Neighbor-joining

TLC:

Thin-layer chromatography

TYGS:

Type strain genome server

References

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

    Article  Google Scholar 

  • Ali MA, Punniyamurthy T (2010) Palladium-catalyzed one-pot conversion of aldehydes to amides. Adv Synth Catal 352:288–292

    Article  CAS  Google Scholar 

  • Arai T (1975) Culture media for actinomycetes. The Society for Actinomycetes, Tokyo

    Google Scholar 

  • Arumugam M, Mitra A, Jaisankar P et al (2010) Isolation of an unusual metabolite 2-allyloxyphenol from a marine actinobacterium, its biological activities and applications. Appl Microbiol Biotechnol 86:109–117

    Article  CAS  PubMed  Google Scholar 

  • Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blin K, Shaw S, Kloosterman AM et al (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brand-Williams W, Cuvelier ME, Berset C (1995) Useofafree radical method to evaluate antioxidant activity. Leben Wissens Technol 28:25–30

    Article  CAS  Google Scholar 

  • Chang TS, Tseng M, Ding HY, Tai (2008) Isolation and characterization of Streptomyces hiroshimensis strain TI-C3 with anti-tyrosinase activity. J Cosmet Sci 59:33–40

    CAS  PubMed  Google Scholar 

  • Cheng C, Othman EM, Reimer A et al (2016) Ageloline A, new antioxidant and antichlamydial quinolone from the marine sponge-derived bacterium Streptomyces sp. SBT345. Tetrahedron Lett 57:2786–2789

    Article  CAS  Google Scholar 

  • Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2,4-diaminobutyric acid. J Appl Bacteriol 48:459–470

    Article  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 

  • Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–667

    Article  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 

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

    Article  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 

  • Furutani Y, Naganawa H, Takeuchi T, Umezawa H (1977) Isolation and structure of new isocoumarins. Agric Biol Chem 41:1179–1183

    CAS  Google Scholar 

  • Gordon RE, Barnett DA, Handerhan JE, Pang CHN (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 24:54–63

    Article  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    Article  CAS  PubMed  Google Scholar 

  • Ishida T, Yoshimura H, Takekawa M et al (2021) Discovery, characterization and functional improvement of kumamonamide as a novel plant growth inhibitor that disturbs plant microtubules. Sci Rep 11:6077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh T, Kudo T, Parenti F, Seino A (1989) Amended description of the genus Kineosporia, based on chemotaxonomic and morphological studies. Int J Syst Bacteriol 39:168–173

    Article  Google Scholar 

  • Jaroszewski J, Stærk D, Holm-Møller SB et al (2005) Naravelia zeylanica: occurrence of primary benzamides in flowering plants. Nat Prod Res 19:291–294

    Article  CAS  PubMed  Google Scholar 

  • Kämpfer P (2012) Genus Streptomyces. the actinobacteria. In: Goodfellow M et al (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp 1455–1767

    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

    Google Scholar 

  • Kim WG, Kim JP, Kim CJ, Lee KH, Yoo ID (1996) Benzastatins A, B, C, and D: new free radical scavengers from Streptomyces nitrosporeus 30643. I. Taxonomy, fermentation, isolation, physico-chemical properties and biological activities. J Antibiot 49:20–25

    Article  CAS  Google Scholar 

  • Kim WG, Ryoo IJ, Park JS, Yoo ID (2001) Benzastatins H and I, new benzastatin derivatives with neuronal cell protecting activity from Streptomyces nitrosporeus. J Antibiot 54:513–516

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kolehmainen ET, Laihia KP, Hyötyläinen JMI, Kauppinen RT (1995) 1H, 13C and 17O NMR spectral study of chlorinated 3,4-dihydroxybenzaldehydes (protocatechualdehydes). Spectrochim Acta A Mol Biomol Spectrosc 51:419–427

    Article  Google Scholar 

  • Komagata K, Suzuki KI (1987) Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 19:161–207

    Article  CAS  Google Scholar 

  • Konstantinidis KT, Rosselló-Móra R, Amann R (2017) Uncultivated microbes in need of their own taxonomy. ISME J 11:2399–2406

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lechevalier MP, De Bièvre C, Lechevalier HA (1977) Chemotaxonomy of aerobic actinomycetes: phospholipid composition. Biochem Syst Ecol 5:249–260

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Li XF, Kim DS et al (2003) Indolyl alkaloid derivatives, Nb-acetyltryptamine and oxaline from a marine-derived fungus. Arch Pharm Res 26:21–23

    Article  PubMed  Google Scholar 

  • Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high throughput platform for state- of-the-art genome-based taxonomy. Nat Commun 10:2182–2192

    Article  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff PJ, Alexander FA, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60–73

    Article  Google Scholar 

  • Minnikin DE, O’Donnell AG, Goodfellow M et al (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241

    Article  CAS  Google Scholar 

  • Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70:5607–5612

    Article  PubMed  PubMed Central  Google Scholar 

  • Phongsopitanun W, Thawai C, Suwanborirux K et al (2014) Streptomyces chumphonensis sp. nov., isolated from marine sediments. Int J Syst Evol Microbiol 64:2605–2610

    Article  CAS  PubMed  Google Scholar 

  • Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302

    Article  CAS  PubMed  Google Scholar 

  • Quinn GA, Banat AM, Abdelhameed AM, Banat IM (2020) Streptomyces from traditional medicine: sources of new innovations in antibiotic discovery. J Med Microbiol 69:1040–1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106:19126–19131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) J SpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinfor 32:929–931

    Article  CAS  Google Scholar 

  • Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe Mag 9:111–118

    Article  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. MIDI technical note 101. MIDI Inc., Newark, pp 1–7

    Google Scholar 

  • Schultz AW, Oh DC, Carney JR (2008) Biosynthesis and structures of cyclomarins and cyclomarazines, prenylated cyclic peptides of marine actinobacterial origin. J Am Chem Soc 130:4507–4516

    Article  CAS  PubMed  Google Scholar 

  • Ser HL, Tan LTH, Palanisamy UD et al (2016) Streptomyces antioxidans sp. Nov., a novel mangrove soil actinobacterium with antioxidative and neuroprotective potentials. Front Microbiol 7:899

    Article  PubMed  PubMed Central  Google Scholar 

  • Seyoum A, Asres K, El-Fiky FK (2006) Structure-radical scavenging activity relationships of flavonoids. Phytochemistry 67:2058–2070

    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 

  • Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Supong K, Suriyachadkun C, Pittayakhajonwut P, Suwanborirux K, Thawai C (2013) Micromonospora spongicola sp. nov., an actinomycete isolated from a marine sponge in the Gulf of Thailand. J Antibiot 66:505–509

    Article  CAS  Google Scholar 

  • Supong K, Thawai C, Supothina S et al (2016) Antimicrobial and anti-oxidant activities of quinoline alkaloids from Pseudomonas aeruginosa BCC76810. Phytochem Lett 17:100–106

    Article  CAS  Google Scholar 

  • Tamaoka J (1994) Determination of DNA base composition. In: Goodfellow M, O’Donnell AG (eds) Chemical methods on prokaryotic systematics. Wiley, Chichester, pp 463–470

    Google Scholar 

  • Tan LTH, Chan KG, Khan TM et al (2017) Streptomyces sp MUM212 as a source of antioxidants with radical scavenging and metal chelating properties. Front Pharmacol 8:276

    Article  PubMed  PubMed Central  Google Scholar 

  • Thawai C, Rungjindamai N, Klanbut K, Tanasupawat S (2017) Nocardia xestospongiae sp. nov., isolated from a marine sponge in the Andaman Sea. Int J Syst Evol Microbiol 67:1451–1456

    Article  CAS  PubMed  Google Scholar 

  • Tietz JI, Schwalen CJ, Patel PS et al (2017) A new genome-mining tool redefines the lasso peptide biosynthetic landscape. Nat Chem Biol 13:470–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Aart LT, Nouioui I, Kloosterman A et al (2019) Polyphasic classification of the gifted natural product producer Streptomyces roseifaciens sp. nov. Int J Syst Evol Microbiol 69:899–908

    Article  PubMed  Google Scholar 

  • Williams ST, Cross T (1971) Chapter XI actinomycetes. In: Booth C et al (eds) Methods in microbiology. Academic Press, London, pp 295–334

    Google Scholar 

  • Yang D, Fu HA (2010) Simple and practical copper-catalyzed approach to substituted phenols from aryl halides by using water as the solvent. Chemistry 16:2366–2370

    Article  CAS  PubMed  Google Scholar 

  • Yoon SH, Ha SM, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zdero C, Jakupovic J, Bohlmann F (1990) Diterpenes and other constituents from Pteronia species. Phytochemistry 29:1231–1245

    Article  CAS  Google Scholar 

  • Zinad DS, Shaaban KA, Abdalla MA et al (2011) Bioactive isocoumarins from a terrestrial Streptomyces sp. ANK302. Nat Prod Commun 6:1934578X1100600111

    Google Scholar 

Download references

Acknowledgements

We thank the Actinobacterial Research Unit (ARU), School of Science, King Mongkut’s Institute of Technology Ladkrabang, for laboratory support.

Funding

The authors gratefully acknowledge the funding support from the National Science, Research and Innovation Fund (NSRF) (Grant number: RE-KRIS/FF65/23) to CT.

Author information

Authors and Affiliations

Authors

Contributions

OT: formal analysis, methodology, resources, writing original draft preparation. TD and ST: chemotaxonomic analyses and biological activity assay. PP and CI: chemotaxonomic analyses, and manuscript editing. CS: data curation, and resources. ST and Y-WH: manuscript editing. CT: conceptualization, data curation, funding acquisition, project administration, resources, validation, and manuscript editing. All authors have read and approved the final version of the manuscript.

Corresponding author

Correspondence to Chitti Thawai.

Ethics declarations

Conflict of interest

The authors declare that they do not have any conflicts of interest.

Additional information

Communicated by Wen-Jun Li.

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 2682 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thayanuwadtanawong, O., Duangupama, T., Bunbamrung, N. et al. Streptomyces telluris sp. nov., a promising terrestrial actinobacterium with antioxidative potentials. Arch Microbiol 205, 247 (2023). https://doi.org/10.1007/s00203-023-03585-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-023-03585-x

Keywords

Navigation