Diversity, antibacterial and phytotoxic activities of actinomycetes associated with Periplaneta fuliginosa

PeerJ. 2024 Nov 25:12:e18575. doi: 10.7717/peerj.18575. eCollection 2024.

Abstract

Background: Insect-associated actinomycetes represent a potentially rich source for discovering bioactive metabolites. However, the diversity, antibacterial and phytotoxic activities of symbiotic actinomycetes associated with Periplaneta fuliginosa have not yet been conducted.

Results: A total of 86 strains of actinomycetes were isolated from the cornicles and intestines of both nymphs and adults of P. fuliginosa. Diversity analysis revealed that the isolated strains were preliminarily identified as 17 species from two genera, and the dominant genus was Streptomyces. A total of 36 crude extracts (60%) obtained from the supernatant of the 60 fermented strains exhibited a potent antibacterial activity against at least one tested pathogenic bacterium. Among these active strains, 27 crude extracts (75%) exhibited phytotoxic activity against the radicle of Echinochloa crusgalli. Furthermore, seven known compounds, including methoxynicotine (1), (3Z,6Z)-3-(4-methoxybenzylidene)-6-(2-methylpropyl) piperazine-2,5-dione (2), XR334 (3), 1-hydroxy-4-methoxy-2-naphthoic acid (4), nocapyrone A (5), β-daucosterol (6), and β-sitosterol (7) were isolated from an active rare actinomycete Nocardiopsis sp. ZLC-87 which was isolated from the gut of adult P. fuliginosa. Among them, compound 4 exhibited moderate antibacterial activity against Micrococcus tetragenus, Staphylococcus aureus, Escherichia coli, and Pseudomonas syringae pv. actinidiae with the zone of inhibition (ZOI) of 14.5, 12.0, 12.5, and 13.0 mm at a concentration of 30 μg/disc, respectively, which was weaker than those of gentamicin sulfate (ZOI of 29.5, 19.0, 18.5, and 24.5 mm). In addition, the compound 4 had potent phytotoxic activity against the radicle of E. crusgalli and Abutilon theophrasti with the inhibition rate of 65.25% and 92.68% at the concentration of 100 μg/mL.

Conclusion: Based on these findings, this study showed that P. fuliginosa-associated actinomycetes held promise for the development of new antibiotic and herbicide resources.

Keywords: Actinomycetes; Antibacterial activity; Nocardiopsis; Periplaneta fuliginosa; Phytotoxic activity; Secondary metabolites.

MeSH terms

  • Actinobacteria* / metabolism
  • Animals
  • Anti-Bacterial Agents* / chemistry
  • Anti-Bacterial Agents* / isolation & purification
  • Anti-Bacterial Agents* / pharmacology
  • Echinochloa / drug effects
  • Herbicides / chemistry
  • Herbicides / isolation & purification
  • Herbicides / pharmacology
  • Nymph / drug effects
  • Nymph / microbiology
  • Periplaneta* / drug effects
  • Periplaneta* / microbiology
  • Symbiosis

Substances

  • Anti-Bacterial Agents
  • Herbicides

Grants and funding

This work was supported by the National Natural Science Foundation of China (NSFC) (32102272) and the Scientific Research Project of Higher Universities in Anhui Province (2024AH050463). Qihua Liu received scholarship support from Anhui Agricultural University. The School of Life Sciences, Anhui Agricultural University and the Biotechnology center of Anhui Agriculture University provided convenient laboratory conditions. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.