Pupal cell antibiosis suppresses plant and insect pathogenic fungi and is associated with a bacterium related to Serratia nematodiphila i

Authors: WU, SHAOHUI - University Of Georgia; Blackburn, Michael - Mike; MIZELL, RUSSELL - University Of Florida; DUNCAN, LARRY - University Of Florida; TOEWS, MICHAEL - University Of Georgia; Sparks, Michael; EL-BORAI, FAHEIM - University Of Florida; Bock, Clive; Shapiro Ilan, David

Submitted to: Journal of Invertebrate Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/30/2021
Publication Date: 8/16/2021
Citation: Wu, S., Blackburn, M.B., Mizell, R.F., Duncan, L.W., Toews, M.D., Sparks, M., El-Borai, F., Bock, C.H., Shapiro Ilan, D.I. 2021. Pupal cell antibiosis suppresses plant and insect pathogenic fungi and is associated with a bacterium related to Serratia nematodiphila i. Journal of Invertebrate Pathology. 184/107655. https://doi.org/10.1016/j.jip.2021.107655.
DOI: https://doi.org/10.1016/j.jip.2021.107655

Interpretive Summary: Many insects that go through a pupal stage create a pupal cell in which they reside until they emerge as adults. For example, some insects, such as pecan weevil (a major pest of pecans), make a pupal cell in soil; it is kind of like a little house they stay in until they come out as adult weevils. The soil cell provides protection to the pupae from predators. Previously, we discovered that the pupal cell also has antibiotic properties – extracts from the pecan weevil’s soil cell suppressed insect-killing fungi. These fungi are natural enemies of the pecan weevil, so the antibiotic properties in the soil cell serve as a self-defense mechanisms for the weevil. In this new study, we wanted to know if the antibiotic properties extend to other weevil pupal cells and can suppress other fungi including those that cause plant diseases. We found that the pupal cell of several other weevil species possess antibiotic properties (cells from the citrus root weevil, plum curculio, and deodar weevil). We also discovered that the antibiotic effect from soil cells can suppress several fungi that cause serious disease in plants. Moreover, we discovered that a novel bacterium called Serratia species, was associated with pecan weevil soil cells and possesses some of the same antibiotic properties. Thus, it is possible the bacteria works as a partner to help protect the weevil while it lives inside its pupal cell. Our study provides new insight into the function of insect pupal cells. Additionally, the finding the pupal cell suppression of disease-causing fungi may lead to the development of new natural fungicides that can be used in crop protection.

Technical Abstract: The pupal cell of the pecan weevil, Curculio caryae (Coleoptera: Curculionidae), was reported previously to exhibit antibiosis to an entomopathogenic fungus, Beauveria bassiana. The objectives of this study were to examine 1) if the antimicrobial effect occurs in other insects that form pupal cells, 2) whether the effect extends to plant pathogenic fungi, and 3) identify the source of antibiosis in pupal cells. Antibiosis of pupal cells against B. bassiana was confirmed in-vitro in three additional curculionids, Diaprepes abbreviatus, Conotrachelus nenuphar, and Pissodes nemorensis, all of which had fewer fungal colonies relative to controls. Pupal cells were found to suppress phytopathogenic fungi in-vitro, including Alternaria solani by D. abbreviatus, and Monilinia fructicola by C. caryae. The detection of antibiosis of pupal cells formed by surface-sterilized insects using sterile soil implies the antimicrobial effect stemmed from inside the insect. A novel biotic mechanism of antibiosis was identified: a bacterium related to Serratia nematodiphila was isolated from C. caryae pupal cells and was found to be associated with antibiosis. The bacterial cultures and their supernatants had similar effects but were not as potent as pupal cells for suppressing B. bassiana. Also, autoclaved pupal cells and autoclaved bacterial supernatant suppressed M. fructicola but were not as inhibitory as non-autoclaved pupal cells. This indicates that antibiosis may be due to bacterial metabolites, while other factors may also be involved. Our findings suggest potential to develop the antibiotic compounds as novel bio-fungicides and leverage control of insect pests and plant diseases.