Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control

Esam H Hummadi; Alexander Dearden; Tomas Generalovic; Benjamin Clunie; Alexandria Harrott; Yarkin Cetin; Merve Demirbek; Salim Khoja; Dan Eastwood; Ed Dudley; Selcuk Hazir; Mustapha Touray; Derya Ulug; Sebnem Hazal Gulsen; Harun Cimen; Tariq Butt

doi:10.1016/j.biocontrol.2020.104527

Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control

Biol Control. 2021 Apr:155:104527. doi: 10.1016/j.biocontrol.2020.104527.

Authors

Esam H Hummadi^{1

2}, Alexander Dearden², Tomas Generalovic², Benjamin Clunie², Alexandria Harrott², Yarkin Cetin², Merve Demirbek², Salim Khoja², Dan Eastwood², Ed Dudley³, Selcuk Hazir⁴, Mustapha Touray⁴, Derya Ulug⁴, Sebnem Hazal Gulsen⁴, Harun Cimen⁴, Tariq Butt²

Affiliations

¹ Department of Biotechnology, College of Science, University of Diyala, Diyala, Iraq.
² Department of Biosciences, College of Science, Swansea University, SA2 8PP, UK.
³ School of Medicine, Swansea University, Singleton Park, SA2 8PP, UK.
⁴ Department of Biology, Faculty of Arts and Sciences, Aydin Adnan Menderes University, Aydin, Turkey.

Abstract

The entomopathogenic fungus (EPF) Metarhizium brunneum occupies the same ecological niche as entomopathogenic nematodes (EPN), with both competing for insects as a food source in the rhizosphere. Interactions between these biocontrol agents can be antagonistic or synergistic. To better understand these interactions, this study focussed on investigating the effect of M. brunneum volatile organic compounds (VOCs), 1-octen-3-ol and 3-octanone, on EPN survival and behaviour. These VOCs proved to be highly toxic to the infective juveniles (IJs) of the EPN Steinernema carpocapsae, Steinernema feltiae and Heterorhabditis bacteriophora with mortality being dose dependent. Chemotaxis studies of H. bacteriophora IJs in Pluronic F127 gel revealed significant preference for the VOCs compared with controls for all tested concentrations. The VOCs also impacted on the test insects in a dose-dependent manner with 3-octanone being more toxic to Galleria mellonella, Cydia splendana and Curculio elephas larvae than 1-octen-3-ol. Mortality of C. splendana and G. mellonella larvae was significantly higher when exposed to relatively high doses (>25%) of 3-octanone. Lower doses of 3-octanone and 1-octen-3-ol immobilised test insects, which recovered after exposure to fresh air for 2 hrs. In depth studies on H. bacteriophora showed that exposure of IJs to > 10% concentration of 3-octanone or 1-octen-3-ol negatively affected infectivity whereas exposure to lower doses (0.1%, 0.01%) had no effect. The VOCs affected IJs, reducing penetration efficacy and the number of generations inside G. mellonella but they failed to inhibit the bacterial symbiont, Photorhabdus kayaii. The ecological significance of VOCs and how they could influence EPF-EPN insect interactions is discussed.

Keywords: Entomopathogenic nematodes; Metarhizium brunneum; Nematicide; Semiochemicals; Volatile organic compounds.