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. 2022 Feb 23;10(1):e0257721.
doi: 10.1128/spectrum.02577-21. Epub 2022 Feb 9.

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

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

Ayako Kusakabe et al. Microbiol Spectr. .

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 + PPA + 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. IMPORTANCE Two phenylpropanoid and one alkaloid secondary metabolites were isolated and identified from culture filtrates of Photorhabdus l. sonorensis strain Caborca. The three identified metabolites showed selective nematicidal and/or nematistatic activities against two important plant parasitic nematodes, the root-knot nematode (Meloidogyne incognita) and the citrus nematode (Tylenchulus semipenetrans). The mixture of all three metabolites had a synergistic nematicidal effect on both targeted nematodes, while other combinations showed compound- and nematode-dependent interactions.

Keywords: Meloidogyne; Photorhabdus; Tylenchulus; nematicidal activity; secondary metabolites; synergy.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIG 1
FIG 1
Nematicidal secondary metabolites from P. l. sonorensis Caborca. (A) trans-cinnamic acid (t-CA). (B) (4E)-5-phenylpent-4-enoic acid (PPA). (C) Indole.
FIG 2
FIG 2
Nematicidal effects of t-CA. (A) Acute toxicity exerted by various concentrations of t-CA against the indicated nematodes after 24-h exposure. (B) Acute toxicity exerted by various concentrations of t-CA against M. incognita after 24-h, 48-h, or 72-h exposure. (C) Acute toxicity exerted by various concentrations of t-CA against T. semipenetrans after 24-h, 48-h, or 72-h exposure.
FIG 3
FIG 3
Nematicidal effects of PPA. (A) Acute toxicity exerted by various concentrations of PPA against the indicated nematodes after 24-h exposure. (B) Acute toxicity exerted by various concentrations of PPA against M. incognita after 24-h, 48-h, or 72-h exposure. (C) Acute toxicity exerted by various concentrations of PPA against T. semipenetrans after 24-h, 48-h, or 72-h exposure.
FIG 4
FIG 4
Nematistatic effects of indole. (A) Temporary paralysis exerted by various concentrations of indole against the indicated nematodes after 24 h exposure. (B) Temporary paralysis exerted by various concentrations of indole against M. incognita after 24-h, 48-h, or 72-h exposure. (C) Temporary paralysis exerted by various concentrations of indole against T. semipenetrans after 24-h, 48-h, or 72-h exposure.

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