Riptortus pedestris and Burkholderia symbiont: an ideal model system for insect–microbe symbiotic associations

Takeshita, Kazutaka; Kikuchi, Yoshitomo

doi:10.1016/j.resmic.2016.11.005

Cited by 99 publications

(100 citation statements)

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“…The specificity and dynamics of these interactions are variable, as some insect groups associate with a wide range of Burkholderia in the plant beneficial and environmental group (Flórez et al, ; Garcia et al, ; Kikuchi, Hosokawa, & Fukatsu, ). Burkholderia symbioses are more promiscuous in the Riptortus bean bug system, where these insects are colonized each generation by genetically diverse Burkholderia strains (Takeshita & Kikuchi, ). Environmental acquisition of these Burkholderia symbionts is determined by physical sorting of symbiont from nonsymbiont bacteria in the insect gut using a specialized organ.…”

Section: Discussionmentioning

confidence: 99%

“…Environmental acquisition of these Burkholderia symbionts is determined by physical sorting of symbiont from nonsymbiont bacteria in the insect gut using a specialized organ. Other colonization factors necessary for establishing a symbiosis have been explored in this system, including the involvement of cysteine rich peptides (Takeshita & Kikuchi, ).…”

Section: Discussionmentioning

confidence: 99%

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The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

et al. 2019

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The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To persist after ingestion, bacteria must first survive phagocytosis. In the social amoeba Dictyostelium discoideum, certain strains of Burkholderia bacteria are able to resist amoebal digestion and maintain a persistent relationship that includes carriage throughout the amoeba's social cycle that culminates in spore formation. Some Burkholderia strains allow their host to carry other bacteria, as food. This carried food is released in new environments in a trait called farming. To better understand the diversity and prevalence of Burkholderia symbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates of D. discoideum and found 25% infected with Burkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions by Burkholderia to the symbiotic lifestyle. Finally, we tested the ability of 38 strains of Burkholderia from D. discoideum, as well as strains isolated from other sources, for traits relevant to symbiosis in D. discoideum. Only D. discoideum native isolates belonging to the Burkholderia agricolaris, B. hayleyella, and B. bonniea species were able to form persistent symbiotic associations with D. discoideum. The Burkholderia–Dictyostelium relationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

et al. 2019

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“…), and a field survey in South Korea indicates that the SBE Burkholderia are fairly prevalent in soil (Kim, unpublished data). In addition, recent studies suggest that R. pedestris can be infected with more diverse Burkholderia strains, compared to the previously known ones, including those in the plant‐associated beneficial and environmental clade (PBE clade) and B. cepacia complex and B. pseudomallei (BCC clade) (Takeshita & Kikuchi ; Jung, unpublished data). Therefore, it would be possible that symbiotic Burkholderia are simply widespread and abundant in soil environments to the extent, in which R. pedestris will encounter the bacteria with high probability in the course of searching for water and food sources.…”

Section: Discussionmentioning

confidence: 99%

Behavioral response of Riptortus pedestris (Hemiptera: Alydidae) 2nd instar nymphs to their gut symbiont, Burkholderia sp., in laboratory conditions

Kim

Lee

2019

Entomological Research

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Many arthropods including insects have symbiotic relationships with diverse microorganisms that can confer fitness benefits to their hosts. Riptortus pedestris is a serious pest on leguminous crops in East Asia including South Korea and Japan. Recently, has been reported that R. pedestris form symbiosis with Gram‐negative bacteria in the genus Burkholderia where they acquire symbionts from soil environments without vertical transmission from each generation. In order to address how R. pedestris acquire their symbiont from environment, we hypothesized that R. pedestris would detect and exhibit preference toward the Burkholderia symbionts. In this study, we conducted a series of dual‐choice experiments and Y‐tube olfactometer experiments to monitor and evaluate behavioral responses by 2nd instar R. pedestris toward the Burkholderia treatment and untreated control under various experimental settings in the laboratory. In dual‐choice experiments, there was no significant preference by R. pedestris to the Burkholderia treatment compared with untreated control. Also, no significant difference was detected in the first choice frequency, visiting frequency, and residence time of the insects between the two treatments. Likewise, there was no detectable preference by R. pedestris to microbial odors from the symbionts in Y‐tube experiments. Therefore, our results indicate that there was no evidence supporting that 2nd instar R. pedestris exhibit preference to the Burkholderia symbiont in the laboratory conditions of this study. Further studies are required to evaluate behavioral responses of later immature stages (i.e., 3rd and 4th instar) to the symbionts and provide choice settings at larger semi‐field arenas.

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“…Evolutionary loss of one type of symbiosis might have been also accelerated by the behavioural or ecological adaptations of the hosts, through which the insects acquire or transmit their symbionts (Salem et al, 2015;Onchuru et al, 2018). For example, lygaeoid bugs with gut crypts ingest the symbionts from the soil every generation (Kikuchi et al, 2011;Itoh et al, 2014;Xu et al, 2016;Takeshita and Kikuchi, 2017). On the other hand, bacteriocyte-associated lygaeoid species infesting and feeding primarily on seeds or stem of their host plants generally stay away from the ground.…”

Section: Evolutionary Origins Of Bacteriocytes and Bacteriomes Associmentioning

confidence: 99%

Repeated evolution of bacteriocytes in lygaeoid stinkbugs

Kuechler

Fukatsu

Matsuura

2019

Environmental Microbiology

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Summary Host–microbe symbioses often evolved highly complex developmental processes and colonization mechanisms for establishment of stable associations. It has long been recognized that many insects harbour beneficial bacteria inside specific symbiotic cells (bacteriocytes) or organs (bacteriomes). However, the evolutionary origin and mechanisms underlying bacterial colonization in bacteriocyte/bacteriome formation have been poorly understood. In order to uncover the origin of such evolutionary novelties, we studied the development of symbiotic organs in five stinkbug species representing the superfamily Lygaeoidea in which diverse bacteriocyte/bacteriome systems have evolved. We tracked the symbiont movement within the eggs during the embryonic development and determined crucial stages at which symbiont infection and bacteriocyte formation occur, using whole‐mount fluorescence in situ hybridization. In summary, three distinct developmental patterns were observed: two different modes of symbiont transfer from initial symbiont cluster (symbiont ball) to presumptive bacteriocytes in the embryonic abdomen, and direct incorporation of the symbiont ball without translocation of bacterial cells. Across the host taxa, only closely related species seemed to have evolved relatively conserved types of bacteriome development, suggesting repeated evolution of host symbiotic cells and organs from multiple independent origins.

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Riptortus pedestris and Burkholderia symbiont: an ideal model system for insect–microbe symbiotic associations

Cited by 99 publications

References 135 publications

The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

Behavioral response of Riptortus pedestris (Hemiptera: Alydidae) 2nd instar nymphs to their gut symbiont, Burkholderia sp., in laboratory conditions

Repeated evolution of bacteriocytes in lygaeoid stinkbugs

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