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 <i>Riptortus pedestris</i> acquires a specific bacterial symbiont of the genus <i>Burkholderia</i> from environmental soil and harbors it in midgut crypts. The genus <i>Burkholderia</i> 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 <i>Burkholderia</i> species and 18 taxonomically diverse bacterial species, we demonstrate here that nonsymbiotic <i>Burkholderia</i> and even its outgroup <i>Pandoraea</i> 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 <i>Burkholderia</i> 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 <i>Burkholderia</i> 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.