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.

  • Article
  • Published:

Plant growth-promoting and antimicrobial chloropyrroles from a rare actinomycete of the genus Catellatospora

Abstract

Two new chloropyrroles, designated catellatopyrroles A (1) and B (2), along with 2-(2′-hydroxybenzoyl)pyrrole (3), were isolated from a culture extract of an actinomycete of the genus Catellatospora. The structures of 13 were elucidated through interpretation of NMR and MS data. Compounds 1 and 2 are the first chloropyrroles substituted by an aliphatic acyl group at the 5-position. Compounds 13 promoted root elongation of germinated lettuce seeds at 1–10 μM. While all compounds inhibited the growth of Gram-positive bacteria, activity against Gram-negative bacterium Rhizobium radiobacter and yeasts Candida albicans and Saccharomyces cerevisiae was varied. Compounds 1 and 2 were moderately cytotoxic against P388 cells.

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

Access options

Buy this article

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Dashti Y, Grkovic T, Abdelmohsen UR, Hentschel U, Quinn RJ. Actinomycete metabolome induction/suppression with N-acetylglucosamine. J Nat Prod. 2017;80:828–36.

    Article  CAS  PubMed  Google Scholar 

  2. Kontou EE, et al. Discovery and characterization of epemicins A and B, new 30-membered macrolides from Kutzneria sp. CA-103260. ACS Chem Biol. 2021;16:1456–68.

    Article  CAS  PubMed  Google Scholar 

  3. Son S, et al. Catenulisporolides, glycosylated triene macrolides from the chemically underexploited actinomycete Catenulispora species. Org Lett. 2018;20:7234–8.

    Article  CAS  PubMed  Google Scholar 

  4. Saito S, Indo K, Oku N, Komaki H, Kawasaki M, Igarashi Y. Unsaturated fatty acids and a prenylated tryptophan derivative from a rare actinomycete of the genus Couchioplanes. Beilstein J Org Chem. 2021;17:2939–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Saito S, et al. A cyclopeptide and three oligomycin-class polyketides produced by an underexplored actinomycete of the genus Pseudosporangium. Beilstein J Org Chem. 2020;16:1100–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Saito S, Oku N, Igarashi Y. Mycetoindole, an N-acyl dehydrotryptophan with plant growth inhibitory activity from an actinomycete of the genus Actinomycetospora. J Antibiot. 2022;75:44–7.

    Article  CAS  Google Scholar 

  7. Asano K, Kawamoto I. Catellatospora, a new genus of the actinomycetales. Int J Syst Bacteriol. 1986;36:512–7.

    Article  Google Scholar 

  8. Meier-Kolthoff JP, Sardà Carbasse J, 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  PubMed  Google Scholar 

  9. AntiSMASH. The AntiSMASH project. https://antismash.secondarymetabolites.org. Accessed 2021-12-27.

  10. Kurabachew M, et al. Lipiarmycin targets RNA polymerase and has good activity against multidrug-resistant strains of Mycobacterium tuberculosis. J Antimicrob Chemother. 2008;62:713–9.

    Article  CAS  PubMed  Google Scholar 

  11. Liu C, et al. Catellatolactams A–C, plant growth-promoting ansamacrolactams from a rare actinomycete of the genus Catellatospora. J Nat Prod. 2022;85:1993–9.

    Article  CAS  PubMed  Google Scholar 

  12. Petruso S, Bonanno S, Caronna S, Ciofalo M, Maggio B, Schillaci D. Oxidative halogenation of substituted pyrroles with Cu (II). Part IV. Bromination of 2‐(2′‐hydroxybenzoyl) pyrrole. A new synthesis of bioactive analogs of monodeoxypyoluteorin. J Heterocycl Chem. 1994;31:941–5.

    Article  Google Scholar 

  13. Kikuchi H, et al. Revised structure and synthesis of celastramycin A, a potent innate immune suppressor. Org Lett. 2009;11:1693–5.

    Article  CAS  PubMed  Google Scholar 

  14. Durán-Sampedro G, et al. Chlorinated BODIPYs: surprisingly efficient and highly photostable laser dyes. Eur J Org Chem. 2012;32:6335–50.

    Article  Google Scholar 

  15. Takahashi N, (ed.). Shokubutsu-kagaku-chosetsu-jikkenho (Experimental protocols for chemical regulation of plants). Tokyo: The Japanese Society for Chemical Regulation of Plants; 1989. p. 140–1 (in Japanese).

  16. Ahmed FR, Toube TP. Incorporation of carbon-14 in the biosynthesis of the macrolide antibiotic, IL-F28249-.ALPHA. J Antibiot. 1993;46:888–91.

    Article  Google Scholar 

  17. Yamagishi Y, Shindo K, Kawai H. Rumbrin, a new cytoprotective substance produced by Auxarthron umbrinum. II. Physico-chemical properties and structure determination. J Antibiot. 1993;46:888–91.

    Article  CAS  Google Scholar 

  18. Hosoe T, Fukushima K, Takizawa K, Miyaji M, Kawai K. Three pyrrolyloctatetraenyl-α-pyrones from Auxarthron conjugatum. Phytochemistry. 1999;52:459–63.

    Article  CAS  Google Scholar 

  19. Clark BR, Capon RJ, Lacey E, Tennant S, Gill JH. Polyenylpyrroles and polyenylfurans from an Australian isolate of the soil ascomycete Gymnoascus reessii. Org Lett. 2006;8:701–4.

    Article  CAS  PubMed  Google Scholar 

  20. Rudi A, et al. Phorbazoles A–D, novel chlorinated phenylpyrrolyloxazoles from the marine sponge Phorbas aff. clathrata. Tetrahedron Lett. 1994;35:2589–92.

    Article  CAS  Google Scholar 

  21. Laird DW, LaBarbera DV, Feng X, Bugni TS, Harper MK, Ireland CM. Halogenated cyclic peptides isolated from the sponge Corticium sp. J Nat Prod. 2007;70:741–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Nuzzo G, Ciavatta ML, Kiss R, Mathieu V, Leclercqz H, Manzo E, Villani G, Mollo E, Lefranc F, D’Souza L, Gavagnin M, Cimino G. Chemistry of the nudibranch Aldisa andersoni: structure and biological activity of phorbazole metabolites. Mar Drugs. 2012;10:1799–811.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Qiao Y, et al. Characterization of the biosynthetic gene cluster for the antibiotic armeniaspirols in Streptomyces armeniacus. J Nat Prod. 2019;82:318–23.

    Article  CAS  PubMed  Google Scholar 

  24. Schnegotzki R, et al. Total synthesis and biosynthesis of cyclodepsipeptide cochinmicin I. Org Lett. 2022;24:2344–8.

    Article  CAS  PubMed  Google Scholar 

  25. Heide L. The aminocoumarins: biosynthesis and biology. Nat Prod Rep. 2009;26:1241–50.

    Article  CAS  PubMed  Google Scholar 

  26. van Pée K-H, Ligon JM. Biosynthesis of pyrrolnitrin and other phenylpyrrole derivatives by bacteria (up to mid-1999). Nat Prod Rep. 2000;17:157–64.

    Article  PubMed  Google Scholar 

  27. Takeda R. Pseudomonas pigments. I. Pyoluteorin, a new chlorine-containing pigment produced by Pseudomonas aeruginosa. Hakko Kogaku Zasshi. 1958;36:281–6.

    CAS  Google Scholar 

  28. Howell CR. Suppression of Pythium ultimum-induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology. 1980;70:712–5.

    Article  CAS  Google Scholar 

  29. Takeda R. Structure of a new antibiotic, pyoluteorin. J Am Chem Soc. 1958;80:4749–50.

    Article  CAS  Google Scholar 

  30. Ezaki N, Koyama M, Shomura T, Tsuruoka T, Inouye S. Pyrrolomycins C, D and E, new members of pyrrolomycins. J Antibiot. 1983;36:1263–7.

    Article  CAS  Google Scholar 

  31. Koyama M, Ezaki N, Tsuruoka T, Inouye S. Structural studies on pyrrolomycins C, D and E. J Antibiot. 1983;36:1483–9.

    Article  CAS  Google Scholar 

  32. Hughes CC, Kauffman CA, Jensen PR, Fenical W. Structures, reactivities, and antibiotic properties of the marinopyrroles A–F. J Org Chem. 2010;75:3240–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Shindo K, Yamagishi Y, Kawai H. Thiazohalostatin, a new cytoprotective substance produced by Actinomadura. II. Physico-chemical properties and structure determination. J Antibiot. 1996;46:1638–42.

    Article  Google Scholar 

  34. Zhang Z, et al. Nomimicins B-D, new tetronate-class polyketides from a marine-derived actinomycete of the genus Actinomadura. Beilstein J Org Chem. 2021;17:2194–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lu S, Harunari E, Oku N, Igarashi Y, Trehangelin E. a bisacyl trehalose with plant growth promoting activity from a rare actinomycete Polymorphospora sp. RD064483. J Antibiot. 2022;75:296–300.

    Article  CAS  Google Scholar 

  36. Zhang Z, et al. Kumemicinones A–G, cytotoxic angucyclinones from a deep sea-derived actinomycete of the genus Actinomadura. J Nat Prod. 2022;85:1098–108.

    Article  CAS  PubMed  Google Scholar 

  37. Igarashi Y, et al. Nonthmicin, a polyether polyketide bearing a halogen-modified tetronate with neuroprotective and antiinvasive activity from Actinomadura sp. Org Lett. 2017;19:1406–9.

    Article  CAS  PubMed  Google Scholar 

  38. Yamamura H, Hayakawa M, Iimura Y. Application of sucrose-gradient centrifugation for selective isolation of Nocardia spp. from soil. J Appl Microbiol. 2003;95:677–85.

    Article  CAS  PubMed  Google Scholar 

  39. 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  PubMed  PubMed Central  Google Scholar 

  40. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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 

  42. Karim MRU, Harunari E, Oku N, Akasaka K, Igarashi Y, Bulbimidazoles A–C. antimicrobial and cytotoxic alkanoyl imidazoles from a marine gammaproteobacterium Microbulbifer species. J Nat Prod. 2020;83:1295–9.

    Article  PubMed  Google Scholar 

  43. Sharma AR, Zhou T, Harunari E, Oku N, Trianto A, Igarashi Y. Labrenzbactin from a coral-associated bacterium Labrenzia sp. J Antibiot. 2019;72:634–9.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Mr. Masaru Watanabe at Yamanashi University for SEM sample preparation. P388 cells were obtained from JCRB Cell Bank under an accession code JCRB0017 (Lot. 06252002). This work was supported by JSPS KAKENHI Grant Number 19K05848 to YI.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasuhiro Igarashi.

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 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

Liu, C., Yamamura, H., Hayakawa, M. et al. Plant growth-promoting and antimicrobial chloropyrroles from a rare actinomycete of the genus Catellatospora. J Antibiot 75, 655–661 (2022). https://doi.org/10.1038/s41429-022-00567-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41429-022-00567-x

This article is cited by

Search

Quick links