Selective Toxicity of Secondary Metabolites from the Entomopathogenic Bacterium Photorhabdus luminescens sonorensis against Selected Plant Parasitic Nematodes of the Tylenchina Suborder

Ayako Kusakabe, Chen Wang, Ya Ming Xu, István Molnár, S. Patricia Stock

Research output: Contribution to journalArticlepeer-review

Abstract

Entomopathogenic Photorhabdus bacteria (Enterobacteriaceae: Gamma-proteobacteria), the natural symbionts of Heterorhabditis nematodes, are a rich source for the discovery of biologically active secondary metabolites (SMs). This study describes the isolation of three nematicidal SMs from in vitro culture supernatants of the Arizona-native Photorhabdus luminescens sonorensis strain Caborca by bioactivity-guided fractionation. Nuclear magnetic resonance spectroscopy and comparison to authentic synthetic standards identified these bioactive metabolites as trans-cinnamic acid (t-CA), (4E)-5-phenylpent-4- enoic acid (PPA), and indole. PPA and t-CA displayed potent, concentration-dependent nematicidal activities against the root-knot nematode (Meloidogyne incognita) and the citrus nematode (Tylenchulus semipenetrans), two economically and globally important plant parasitic nematodes (PPNs) that are ubiquitous in the United States. Southwest. Indole showed potent, concentration-dependent nematistatic activity by inducing the temporary rigid paralysis of the same targeted nematodes. While paralysis was persistent in the presence of indole, the nematodes recovered upon removal of the compound. All three SMs were found to be selective against the tested PPNs, exerting little effects on non-target species such as the bacteria-feeding nematode Caenorhabditis elegans or the entomopathogenic nematodes Steinernema carpocapsae, Heterorhabditis bacteriophora, and Hymenocallis sonorensis. Moreover, none of these SMs showed cytotoxicity against normal or neoplastic human cells. The combination of t-CA 1 PPA 1 indole had a synergistic nematicidal effect on both targeted PPNs. Two-component mixtures prepared from these SMs revealed complex, compound-, and nematode species-dependent interactions. These results justify further investigations into the chemical ecology of Photorhabdus SMs, and recommend t-CA, PPA and indole, alone or in combinations, as lead compounds for the development of selective and environmentally benign nematicides against the tested PPNs.

Original languageEnglish (US)
Article numbere02577-21
JournalMicrobiology Spectrum
Volume10
Issue number1
DOIs
StatePublished - Feb 2022
Externally publishedYes

Keywords

  • Meloidogyne
  • Nematicidal activity
  • Photorhabdus
  • Secondary metabolites
  • Synergy
  • Tylenchulus

ASJC Scopus subject areas

  • Physiology
  • Ecology
  • Immunology and Microbiology(all)
  • Genetics
  • Microbiology (medical)
  • Cell Biology
  • Infectious Diseases

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