Disruption of Host-Symbiont Associations for the Symbiotic Control and Management of Pentatomid Agricultural Pests—A Review

Abstract

The family Pentatomidae (Hemiptera: Heteroptera) includes several invasive stink bug species capable to attack a large number of wild and cultivated plants, causing several damages to different crops. Pentatomids rely on obligate symbiotic associations with bacteria of the family Enterobacteriaceae, mainly of the genus Pantoea. A distinctive trait of these associations is the transmission route: during oviposition, females smear egg masses with symbiont-containing secretions, which are ingested by newly hatched nymphs, allowing the symbiont to pass through their digestive tract and establish in the crypts of the posterior midgut. Preventing newborns from orally acquiring symbionts seriously affects their fitness and survival. This symbiont inheritance process can be manipulated to develop innovative pest control measures by sterilization of egg masses prior to nymph hatching. This review summarizes the recent knowledge advances concerning the gut primary symbionts of pentatomids, with a specific focus on the most troubling pest species for agriculture. Current understanding of host colonization dynamics in pentatomids is presented, as well as the phenotypic effects determined in different insect species by the alteration of vertical transmission. Details on the current knowledge on the whole bacterial communities accompanying primary symbionts are analyzed. The recent research exploiting the perturbation of symbiont acquisition by pentatomid nymphs is discussed, by considering published work on laboratory and field trials with several active substances. These translational strategies are presently regarded as promising for limiting the populations of many important pentatomid pests in a sustainable way.

The Gut Microbiota of the Insect Infraorder Pentatomomorpha (Hemiptera: Heteroptera) for the Light of Ecology and Evolution

“…[ 7 , 17 , 62 , 71 , 87 ]. On the other hand, the obligate partners are essential or important for host survival, development or fecundity, indicating the symbionts may serve as targets for pest control and therefore the disruption of these microbial associations would lead to low vitality of the pest [ 128 ]. Specifically, the change of the obligate gut symbionts for a plataspid stinkbug will reverse the pest M. punctatissima to be a non-pest status on the legumes crop, indicating the potential microbial targets for pest control [ 117 ].…”

Episyrphus balteatus symbiont variation across developmental stages, living states, two sexes, and potential horizontal transmission from prey or environment

“…In addition, plentiful evidence indicates that symbionts can also undergo horizontal transfer among different insects or be acquired directly from the environment or diets (Hosokawa et al, 2016;Tzuri et al, 2021;Du et al, 2022;Pons et al, 2022), and acquisition of novel symbiont strains for the insects via horizontal transmission can provide fitness benefits to the host, with significant ecological and evolutionary consequences (Łukasik et al, 2015). In contrast to considerable studies about microbiota structure and diversity in aphids (Guo et al, 2017), bees (Steffan et al, 2023), flies (Noman et al, 2020), bugs (Gonella et al, 2020), and beetles (Salem and Kaltenpoth, 2022), knowledge about symbionts in hoverflies was rare.…”

Pantoea bathycoeliae sp. nov and Sodalis sp. are core gut microbiome symbionts of the two-spotted stink bug

“…The stink bug invasions in the orchards are predominantly controlled with insecticides, which is damaging to the environment and could lead to the development of insecticide resistance (Schoeman, 2019). The development of an integrated pest management approach, for example, targeting essential gut symbionts could improve control measures and reduce the use of insecticides (Gonella et al, 2020).…”