Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Streptomyces pacificus sp. nov., a novel spongiicolazolicin-producing actinomycete isolated from a coastal sediment

The Journal of Antibiotics volume 76, pages 93–100 (2023)Cite this article

Subjects

Abstract

A polyphasic approach was used to determine the taxonomic position of a marine actinomycete, designated isolate CWH03T, which we previously reported to produce new linear azole-containing peptides spongiicolazolicins A and B. Strain CWH03T is mesophilic, neutrophilic, and halotolerant streptomycete that forms spiral spore chains on aerial mycelium. Comparative 16S rRNA gene sequencing showed that CWH03T was most closely related to Streptomyces tirandamycinicus HNM0039T (99.7%), Streptomyces spongiicola HNM0071T (99.4%), ‘Streptomyces marianii’ ICN19T (99.1%) and Streptomyces wuyuanensis CGMCC4.7042T (99.0%). The phylogenetic tree prepared using the 16S rRNA gene, as well as the phylogenomic tree using the genome BLAST distance phylogeny method and 81 core housekeeping genes, respectively, showed that the closest relative of strain CWH03T was S. spongiicola HNM0071T. The average nucleotide identity and digital DNA-DNA hybridization values between strains CWH03T and S. spongiicola HNM0071T were 91.46% and 44.2%, respectively, which were below the thresholds of 96% and 70% for prokaryotic conspecific assignation. The G+C content of the genomic DNA of strain CWH03T was 72.3%. Whole-cell hydrolysates of strain CWH03T contained LL-diaminopimelic acid. The predominant menaquinone was MK-9(H8) (88.3%), and the major fatty acids were iso-C16:0 (28.4%), anteiso-C15:0 (15.0%) and iso-C15:0 (12.9%). The major phospholipids were diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and an unidentified phospholipid. Based on data obtained from phenotypic, phylogenetic, genomic, and chemotaxonomic analyses, strain CWH03T represents a novel species of the genus Streptomyces, for which the proposed name is Streptomyces pacificus sp. nov. The type strain is CWH03T ( = NBRC 114659T = TBRC 15780T).

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Schatz A, Bugle E, Waksman SA. Streptomycin, a substance exhibiting antibiotic activity against Gram-positive and Gram-negative bacteria. Proc Soc Exp Biol Med. 1944;55:66–9.

    Article  CAS  Google Scholar 

  2. Bérdy J. Bioactive microbial metabolites. J Antibiot. 2005;58:1–26.

    Article  Google Scholar 

  3. Zhang J, Hassan HA, Abdelmohsen UR, Zahran EM. A glossary for chemical approaches towards unlocking the trove of metabolic treasures in actinomycetes. Molecules 2022;27:142.

    Article  CAS  Google Scholar 

  4. Bhattarai K, Bastola R, Baral B. Antibiotic drug discovery: Challenges and perspectives in the light of emerging antibiotic resistance. Adv Genet. 2020;105:229–92.

    Article  CAS  Google Scholar 

  5. Ramesh S, Mathivanan N. Screening of marine actinomycetes isolated from the Bay of Bengal, India for antimicrobial activity and industrial enzymes. World J Microbiol Biotechnol. 2009;25:2103–11.

    Article  CAS  Google Scholar 

  6. Subramani R, Aalbersberg W. Marine actinomycetes: An ongoing source of novel bioactive metabolites. Microbiol Res. 2012;167:571–80.

    Article  CAS  Google Scholar 

  7. Jose PA, Maharshi A, Jha B. Actinobacteria in natural products research: Progress and prospects. Microbiol Res. 2021;246:1–14.

    Article  Google Scholar 

  8. Safaei N, et al. Angucycline-like aromatic polyketide from a novel Streptomyces species reveals freshwater snail Physa acuta as underexplored reservoir for antibiotic-producing actinomycetes. Antibiotics (Basel). 2020;10:22.

    Article  Google Scholar 

  9. Iniyan AM, et al. Streptomyces marianii sp. nov., a novel marine actinomycete from southern coast of India. J Antibiot. 2021;74:59–69.

    Article  CAS  Google Scholar 

  10. Zhao XQ, et al. Streptomyces xinghaiensis sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol. 2009;59:2870–4.

    Article  CAS  Google Scholar 

  11. Mangamuri U, Vijayalakshmi M, Ganduri VSRK, Rajulapati SB, Poda S. Extracellular L-Asparaginase from Streptomyces labedae VSM-6: Isolation, Production and Optimization of Culture Conditions Using RSM. Pharmacogn J. 2017;9:932–41.

    Article  CAS  Google Scholar 

  12. Huang X, Zhou S, Huang D, Chen J, Zhu W. Streptomyces spongiicola sp. nov., an actinomycete derived from marine sponge. Int J Syst Evol Microbiol. 2015;66:738–43.

    Article  Google Scholar 

  13. Li L, Wang J, Zhou YJ, Lin HW, Lu YH. (2019). Streptomyces reniochalinae sp. nov. and Streptomyces diacarni sp. nov., from marine sponges. Int J Syst Evol Microbiol. 2019;69:99–104.

    Article  CAS  Google Scholar 

  14. Huang X, et al. Streptomyces tirandamycinicus sp. nov., a novel marine sponge-derived actinobacterium with antibacterial potential against Streptococcus agalactiae. Front Microbiol. 2019;10:1–11.

    Article  Google Scholar 

  15. Braña AF, et al. Desertomycin G, a new antibiotic with activity against Mycobacterium tuberculosis and human breast tumor cell lines produced by Streptomyces althioticus MSM3, isolated from the Cantabrian Sea Intertidal macroalgae Ulva sp. Mar Drugs. 2019;17:114.

    Article  Google Scholar 

  16. Zhang S, et al. Antimicrobial tunicamycin derivatives from the deep sea-derived Streptomyces xinghaiensis SCSIO S15077. Nat Prod Res. 2020;34:1499–1504.

    Article  CAS  Google Scholar 

  17. Ishida K, et al. New dihydronaphthothiophene derivatives by the biological transformation of seriniquinone using marine-derived actinomycete Streptomyces albogriseolus OM27-12. J Antibiot. 2021;75:9–15.

    Article  Google Scholar 

  18. Suzuki M, et al. Isolation and structure determination of new linear azole-containing peptides spongiicolazolicins A and B from Streptomyces sp. CWH03. Appl Microbiol Biotechnol. 2021;105:93–104.

    Article  CAS  Google Scholar 

  19. Goris J, et al. DNA-DNA hybridization values and their relationship to whole- genome sequence similarities. Int J Syst Evol Microbiol. 2007;57:81–91.

    Article  CAS  Google Scholar 

  20. Shirling EB, Gottlibe D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol. 1966;16:313–40.

    Article  Google Scholar 

  21. Tamura T, Hatano K. Phylogenetic analysis of the genus Actinoplanes and transfer of Actinoplanes minutisporangius Ruan et al. 1986 and ‘Actinoplanes aurantiacus’ to Cryptosporangium minutisporangium comb. nov. and Cryptosporangium aurantiacum sp. nov. Int J Syst Evol Microbiol. 2001;51:2119–25.

    Article  CAS  Google Scholar 

  22. Yoon SH, et al. Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67:1613–7.

    Article  CAS  Google Scholar 

  23. Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.

    CAS  Google Scholar 

  24. Takahashi K, Nei M. Efficiencies of fast algorithms of phylogenetic inference under the criteria of maximum parsimony, minimum evolution, and maximum likelihood when a large number of sequences are used. Mol Biol Evol. 2000;17:1251–8.

    Article  CAS  Google Scholar 

  25. Felsenstein J. Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol. 1981;17:368–76.

    Article  CAS  Google Scholar 

  26. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2021;35:1547–9.

    Article  Google Scholar 

  27. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 1985;39:783–91.

    Article  Google Scholar 

  28. Tanizawa Y, Fujisawa T, Arita M, Nakamura Y. DFAST: A flexible prokaryotic genome annotation pipeline for faster genome publication. Methods Mol Biol. 2019;1962:215–26.

    Article  CAS  Google Scholar 

  29. Kim J, Na SI, Kim D, Chun J. UBCG2: Up-to-date bacterial core genes and pipeline for phylogenomic analysis. J Microbiol. 2021;59:609–15.

    Article  CAS  Google Scholar 

  30. 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.

    Article  Google Scholar 

  31. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek. 2017;110:1281–6.

    Article  CAS  Google Scholar 

  32. 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:D801–7.

    Article  CAS  Google Scholar 

  33. Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol. 1983;29:319–22.

    Article  CAS  Google Scholar 

  34. Tamura T, Ishida Y, Suzuki KI. Descriptions of Actinoplanes ianthinogenes nom. rev. and Actinoplanes octamycinicus corrig. comb. nov., nom. rev. Int J Syst Evol Microbiol. 2011;61:2916–21.

    Article  CAS  Google Scholar 

  35. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101. Newark, DE: MIDI, Inc.; 1990.

  36. Minnikin D, et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods. 1984;2:233–41.

    Article  CAS  Google Scholar 

  37. Hamada M, et al. Luteimicrobium album sp. nov., a novel actinobacterium isolated from a lichen collected in Japan, and emended description of the genus Luteimicrobium. J Antibiot. 2012;65:427–31.

    Article  CAS  Google Scholar 

  38. Yassin AF, Haggenei B, Budzikiewicz H, Schaal KP. Fatty acid and polar lipid composition of the genus Amycolatopsis: Application of fast atom bombardment-mass spectrometry to structure analysis of underivatized phospholipids. Int J Syst Bacteriol. 1933;43:414–20.

    Article  Google Scholar 

  39. Hayakawa M, Nonomura H. Humic acid-vitamin agar, a new medium for the selective isolation of soil actinomycetes. J Ferment Technol. 1987;65:501–9.

    Article  CAS  Google Scholar 

  40. Japan Color Standard Laboratory (Nihon Shikisai Kenkyusho). Guide to color standard. 1st ed. Tokyo: Japan Color Standard Co. (Nihon Shikisai Sha); 1954. p. 4–9.

  41. Gerharbt P, et al. Manual of methods for general bacteriology. In: Robert MS, Noel RK, editors. General characterization. 1st ed. Washington, DC: American Society for Microbiology; 1981. p. 409–44.

  42. Kiska DL, Hicks K, Pettit DJ. Identification of medically relevant Nocardia species with an abbreviated battery of tests. J Clin Microbiol. 2002;40:1346–51.

    Article  Google Scholar 

  43. Gordon RE, Barnett DA, Handerhan JE, Pang CHN. Nocardia coeliaca, Nocardia autotrophica, and the Nocardin Strain. Int J Syst Bacteriol. 1974;24:54–63.

    Article  Google Scholar 

  44. 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;68:461–6.

    Article  CAS  Google Scholar 

  45. Zhang X, Zhang J, Zheng J, Xin D, Xin Y, et al. Streptomyces wuyuanensis sp. nov., an actinomycete from soil. Int J Syst Evol Microbiol. 2013;63:2945–50.

    Article  CAS  Google Scholar 

  46. Iniyan AM, Sudarman E, Wink J, Kannan RR, Vincent SGP. Ala-geninthiocin, a new broad spectrum thiopeptide antibiotic, produced by a marine Streptomyces sp. ICN19. J Antibiot. 2019;72:99–105.

    Article  CAS  Google Scholar 

  47. Zhou S, Xiao K, Huang D, Wu W, Xu Y, et al. Complete genome sequence of Streptomyces spongiicola HNM0071T, a marine sponge-associated actinomycete producing staurosporine and echinomycin. Mar Genom. 2019;43:61–4.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by JSPS KAKENHI Grant Number 16K07229. We are grateful to Dr. Bernhard Schink for his support with nomenclature.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Faculty of Life and Environmental Sciences, University of Yamanashi, Takeda-4-4-37, Kofu, 400-8510, Japan

    Miku Takahashi, Shoya Shinohara, Youji Nakagawa, Susumu Kokubo, Masayuki Hayakawa & Hideki Yamamura

  2. Biological Resource Center, National Institute of Technology and Evaluation (NBRC), 2-5-8 Kazusakamatari, Kisarazu, Chiba, 292-0818, Japan

    Moriyuki Hamada & Tomohiko Tamura

  3. Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan

    Hideo Dohra & Shinya Kodani

  4. Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan

    Hideo Dohra & Shinya Kodani

  5. Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan

    Hideo Dohra

  6. Academic Institute, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan

    Shinya Kodani

  7. Yamanashi Prefectural University, Iida-5-11-1, Kofu, 400-0035, Japan

    Masayuki Hayakawa

Authors
  1. Miku Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shoya Shinohara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Moriyuki Hamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomohiko Tamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hideo Dohra
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shinya Kodani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Youji Nakagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Susumu Kokubo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Masayuki Hayakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hideki Yamamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hideki Yamamura.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

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

Verify currency and authenticity via CrossMark

Cite this article

Takahashi, M., Shinohara, S., Hamada, M. et al. Streptomyces pacificus sp. nov., a novel spongiicolazolicin-producing actinomycete isolated from a coastal sediment. J Antibiot 76, 93–100 (2023). https://doi.org/10.1038/s41429-022-00589-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41429-022-00589-5

Search

Advanced search

Quick links