Diaphorin, a polyketide synthesized by an intracellular symbiont of the Asian citrus psyllid, is potentially harmful for biological control agents

Abstract

The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Sternorrhyncha: Psylloidea: Liviidae) is an important pest of citrus species worldwide because it transmits Candidatus Liberibacter spp. ( Alphaproteobacteria ), the causative agents of an incurable citrus disease known as huanglongbing or greening disease. Diaphorina citri possesses a vertically-transmitted intracellular symbiont, Candidatus Profftella armatura ( Betaproteobacteria ), which produces diaphorin, a polyketide that is significantly toxic to mammalian cells. Diaphorin is an analog of pederin, a defensive polyketide in the body fluid of Paederus rove beetles (Coleoptera: Staphylinidae) that deters predators. In the present study, as a first step to assess the possibility that diaphorin is toxic to biological control agents, we assayed diaphorin activities against insects and fungi. The target cells and organisms were (a) the Sf9 cell line derived from the fall armyworm moth Spodoptera frugiperda (Lepidoptera: Noctuidae), (b) the pea aphid Acyrthosiphon pisum (Hemiptera: Sternorrhyncha: Aphidoidea: Aphididae), a phloem sap-sucking insect that is closely related to psyllids, (c) the Asian lady beetle Harmonia axyridis (Coleoptera: Coccinellidae), one of the major predators of D . citri , and (d) the budding yeast Saccharomyces cerevisiae (Ascomycota: Saccharomycetes) as a model of fungal pathogens. For a comparison, we also evaluated pederin activities. The results of our analyses revealed the following: (1) Diaphorin and pederin are significantly toxic to the tested insects and yeast; (2) Their toxicities vary widely among the target cells and organisms; (3) Diaphorin is generally less toxic than pederin; (4) The toxicities of diaphorin and pederin are considerably different in the Sf9 insect cell line and S . cerevisiae , but similar in A . pisum and H . axyridis ; and (5) The amount of diaphorin contained in D . citri is toxic to all of the tested cells and organisms, suggesting that this polyketide is potentially harmful for biological control agents.

A multiproducer microbiome generates chemical diversity in the marine sponge Mycale hentscheli

“…The data support extensive horizontal gene transfer and retention in extraordinarily diverse host-symbiont systems, including intracellular organelle-like bacteria with minimalistic genomes (34) as well as multicellular prokaryotes featuring genomes of around 10 Mb (10,14). Pederin-type metabolites might thus represent ancient, "symbiotically privileged" natural products that have driven the evolution of multiple symbioses through host protection (76,77). However, more recently, pederin-type compounds were also reported from two free-living bacteria (38,39).…”

Microbiome diversity in Diaphorina citri populations from Kenya and Tanzania shows links to China

“…Wolbachia is known to cause cytoplasmic incompatibility between uninfected females and infected males resulting in increased infected lineages in the host population [13]. The ability of Wolbachia to cause incompatibility in insects can be exploited as a potential strategy to control D. citri in addition to other control methods, as has been shown in the Mediterranean…”

“…Key endosymbionts of D. citri such as Wolbachia pipientis wDi, "Candidatus Profftella" and "Candidatus Carsonella" have diverse roles within the insect. "Candidatus Carsonella" is a putative nutrition provider, while "Candidatus Profftella" has been reported as a defensive symbiont [12,13]. Wolbachia is maternally transmitted in the egg cytoplasm and performs reproductive manipulations to increase the fitness of Wolbachia-infected matrilines resulting in cytoplasmic incompatibility between uninfected females and infected males [13].…”

“…"Candidatus Carsonella" is a putative nutrition provider, while "Candidatus Profftella" has been reported as a defensive symbiont [12,13]. Wolbachia is maternally transmitted in the egg cytoplasm and performs reproductive manipulations to increase the fitness of Wolbachia-infected matrilines resulting in cytoplasmic incompatibility between uninfected females and infected males [13]. This activity of Wolbachia has been exploited as a potential control measure to decrease insect populations such as Ceratitis capitata, Aedes aegypti and Aedes albopictus [14][15][16][17][18].…”

Plant Metabolites in Plant Defense Against Pathogens

“…On the other hand, the study of medicinal plants as possible natural sources of obtaining active compound (secondary metabolites) against phytopathogens has gained increasing interest in recent years, due to several aspects, mainly that they are obtained from a natural source through the production or synthesis of secondary metabolites considered as nontoxic such as phenols, flavonoids, terpenes, alkaloids, etc. [10][11][12][13]. Another advantage is that phytopathogens still do not develop resistance to the antifungal, antimicrobial, and nematicide effect of the phytochemical compounds produced by some medicinal plants.…”