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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.

SUBMITTER: Itoh H

PROVIDER: S-EPMC6842582 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Host-symbiont specificity determined by microbe-microbe competition in an insect gut.

Itoh Hideomi H Jang Seonghan S Takeshita Kazutaka K Ohbayashi Tsubasa T Ohnishi Naomi N Meng Xian-Ying XY Mitani Yasuo Y Kikuchi Yoshitomo Y

Proceedings of the National Academy of Sciences of the United States of America 20191021 45

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 ...[more]

PMID: 31636183

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Project description:Insects share an intimate relationship with their gut microflora and this symbiotic association has developed into an essential evolutionary outcome intended for their survival through extreme environmental conditions. While it has been clearly established that insects, with very few exceptions, associate with several microbes during their life cycle, information regarding several aspects of these associations is yet to be fully unraveled. Acquisition of bacteria by insects marks the onset of microbial symbiosis, which is followed by the adaptation of these bacterial species to the gut environment for prolonged sustenance and successful transmission across generations. Although several insect-microbiome associations have been reported and each with their distinctive features, diversifications and specializations, it is still unclear as to what led to these diversifications. Recent studies have indicated the involvement of various evolutionary processes operating within an insect body that govern the transition of a free-living microbe to an obligate or facultative symbiont and eventually leading to the establishment and diversification of these symbiotic relationships. Data from various studies, summarized in this review, indicate that the symbiotic partners, i.e., the bacteria and the insect undergo several genetic, biochemical and physiological changes that have profound influence on their life cycle and biology. An interesting outcome of the insect-microbe interaction is the compliance of the microbial partner to its eventual genome reduction. Endosymbionts possess a smaller genome as compared to their free-living forms, and thus raising the question what is leading to reductive evolution in the microbial partner. This review attempts to highlight the fate of microbes within an insect body and its implications for both the bacteria and its insect host. While discussion on each specific association would be too voluminous and outside the scope of this review, we present an overview of some recent studies that contribute to a better understanding of the evolutionary trajectory and dynamics of the insect-microbe association and speculate that, in the future, a better understanding of the nature of this interaction could pave the path to a sustainable and environmentally safe way for controlling economically important pests of crop plants.

Dataset Information

Host-symbiont specificity determined by microbe-microbe competition in an insect gut.

Publications

Host-symbiont specificity determined by microbe-microbe competition in an insect gut.

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