Mechanisms Underpinning Morphogenesis of a Symbiotic Organ Specialized for Hosting an Indispensable Microbial Symbiont in Stinkbugs

Abstract

Diverse organisms are associated with microbial mutualists, in which specialized host organs often develop for retaining the microbial partners. In light of the origin of evolutionary novelties, it is important to understand what mechanisms underpin the elaborate morphogenesis of such symbiotic organs, which must have been shaped through interactions with the microbial symbionts.

The importance of host physical niches for the stability of gut microbiome composition

“…The specificity of a beneficial host-microbe association is determined by both the host and the microbe, and there are various degrees of specificity with different mechanisms [11,13,15,19,28]. When the host constructs a physical niche that selectively binds with molecular specificity certain bacteria to the exclusion of others, this represents one of the highest degrees of host control [13,32].…”

“…Physical niches represent the utmost host control over a symbiont because they control not only which symbiont strain colonizes, but also where it colonizes, how many cells colonize and how long the symbiont cells spend in the niche before they are expelled ( [13,32,33]; figure 1c). Physical niches hold host-selected bacterial symbionts in squid [13], fishes [34,35], bugs [28] and other insects [15]. While numerous other stochastically acquired bacteria may be present, the specific symbionts reside in privileged physical niches.…”

“…How bacteria are selected contributes to the co-phylogenetic patterns between host and bacterial symbiont. The posterior midgut crypts that are colonized by Burkholderia in bugs lie distal to the 'constricted region', which filters out undesirable bacteria using a combination of physical, chemical and immune mechanisms, similar to the selective mechanisms that regulate squid light organ colonization [13,20,28]. Factors such as the mechanism of symbiont acquisition (vertical versus environmental), the host diet that influences the environment for the association, and the prevalence of the bacteria in the environment can influence symbiont acquisition [29].…”

Extracellular symbiont colonizes insect during embryo development

“…Acanthosomatidae [54], Alydidae [22,29,55], and Pentatomidae [56][57][58][59] families all house their symbionts in crypts developing in the posterior midgut. Recent findings indicate that the underlying molecular and cellular processes appear to be decoupled from symbiont presence, at least in a subset of species [57].…”

“…Acanthosomatidae [54], Alydidae [22,29,55], and Pentatomidae [56][57][58][59] families all house their symbionts in crypts developing in the posterior midgut. Recent findings indicate that the underlying molecular and cellular processes appear to be decoupled from symbiont presence, at least in a subset of species [57]. In the case of the pentatomid Plautia stali, the experimental loss of its obligate Pantoea symbiont does not alter crypt formation and cellular differentiation [57]; an observation that is consistent with our finding that the foregut symbiotic organs also develop independently of Stammera in tortoise beetles (Figure 4).…”