Host–symbiont specificity determined by microbe–microbe competition in an insect gut

Abstract

Despite the omnipresence of specific host–symbiont associations with acquisition of the microbial symbiont from the environment, little is known about how the specificity of the interaction evolved and is maintained. The bean bug Riptortus pedestris acquires a specific bacterial symbiont of the genus Burkholderia from environmental soil and harbors it in midgut crypts. The genus Burkholderia consists of over 100 species, showing ecologically diverse lifestyles, and including serious human pathogens, plant pathogens, and nodule-forming plant mutualists, as well as insect mutualists. Through infection tests of 34 Burkholderia species and 18 taxonomically diverse bacterial species, we demonstrate here that nonsymbiotic Burkholderia and even its outgroup Pandoraea could stably colonize the gut symbiotic organ and provide beneficial effects to the bean bug when inoculated on aposymbiotic hosts. However, coinoculation revealed that the native symbiont always outcompeted the nonnative bacteria inside the gut symbiotic organ, explaining the predominance of the native Burkholderia symbiont in natural bean bug populations. Hence, the abilities for colonization and cooperation, usually thought of as specific traits of mutualists, are not unique to the native Burkholderia symbiont but, to the contrary, competitiveness inside the gut is a derived trait of the native symbiont lineage only and was thus critical in the evolution of the insect gut symbiont.

Formicine ants swallow their highly acidic poison for gut microbial selection and control

“…The creation of a challenging gut environment through the ingestion of poison gland substances that is easier to endure if colonizing microbes are mutualists agrees with the theoretical concept of screening, as opposed to signalling, as a means of partner choice in cross-kingdom mutualisms (Archetti et al, 2011a, Archetti et al, 2011b, Biedermann and Kaltenpoth, 2014, Scheuring and Yu, 2012). Experimental evidence for screening is so far limited in insect-microbe associations (Innocent et al, 2018, Itoh et al, 2019, Ranger et al, 2018), but the results of our study provide support for the prediction that screening is more likely to evolve if a host’s challenging environment is derived from defence traits against parasites (Archetti et al, 2011a, Archetti et al, 2011b). Altogether, our study provides evidence that the well-established cross talk between the immune system and gut associated microbes in vertebrates and invertebrates (Chu and Mazmanian, 2013, Rakoff-Nahoum et al, 2004, Slack et al, 2009, Watnick and Jugder, 2020, Xiao et al, 2019) holds for a broader range of immune defence traits ( sensu Otti et al, 2014) and might be realized not only through signalling but also screening.…”

“…In addition to pathogen control, the acidification of the crop lumen might act as a chemical filter for gut associated microbial communities in formicine ants, similar to gut morphological structures that can act as mechanical filters in ants and other insects (Itoh et al, 2019, Lanan et al, 2016, Ohbayashi et al, 2015). To investigate the idea of a chemical filter, we tested the ability of the pathogenic bacterium S. marcescens , and the insect gut associated bacterium Asaia sp.…”

Formicine ants swallow their highly acidic poison for gut microbial selection and control

“…In addition to microbial control, poison acidified formicine ant crops might act as a chemical filter for gut-associated microbial communities, similar to gut morphological structures that can act as mechanical filters in ants ( Cannon, 1998 ; Glancey et al, 1981 ; Lanan et al, 2016 ; Little et al, 2006 ; Quinlan and Cherrett, 1978 ) and other insects ( Itoh et al, 2019 ; Ohbayashi et al, 2015 ). To investigate the idea of a chemical filter, we tested the ability of the insect gut-associated bacterium Asaia sp.…”

“…Contrary to signalling, where costly information is displayed to partners, in screening a costly environment is imposed on partners that excludes all but high-quality ones. Partner choice in a number of cross-kingdom mutualisms is readily explained by screening (see examples in Archetti et al, 2011a ; Archetti et al, 2011b ; Biedermann and Kaltenpoth, 2014 ; Scheuring and Yu, 2012 ) but experimental evidence is so far limited in insect-microbe associations ( Innocent et al, 2018 ; Itoh et al, 2019 ; Ranger et al, 2018 ). Although our experiments can only hint at screening as a means of partner choice in formicine ants, the results of our study would provide support for the prediction that screening is more likely to evolve from a host’s defense trait against parasites ( Archetti et al, 2011a ; Archetti et al, 2011b ), that is, the highly acidic, antimicrobial poison that creates a selective environment for microbes.…”

Using Colonization Assays and Comparative Genomics To Discover Symbiosis Behaviors and Factors in Vibrio fischeri

“…Studies of the squid-vibrio model allow us to examine strain diversity within a single species, and applying an analogous approach can also reveal mechanisms of colonization in morecomplex communities. For example, the competitiveness of diverse bacterial species has been established in the bean bug Riptortus pedestris (36), while on a larger scale, the first bacterial population colonizing the mouse gut has been shown to most influence the composition of its final microbial community (37). The future application of comparative genomics will continue to provide a means to discover strain-level patterns in the evolution and development of microbial symbioses.…”