Infection dynamics of insecticide-degrading symbionts from soil to insects in response to insecticide spraying

Itoh, Hideomi; Hori, Tomoyuki; Sato, Yuya; Nagayama, Atsushi; Tago, Kanako; Hayatsu, Masahito; Kikuchi, Yoshitomo

doi:10.1038/s41396-017-0021-9

Cited by 61 publications

(63 citation statements)

References 61 publications

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“…S1) and only 1 study reported the infection with BCC&P species in overwintering R. pedestris (33). In addition, in insects reared on soil in the laboratory, we occasionally identified infections with PBE Burkholderia as well as Pandoraea, suggesting that colonization of the symbiotic midgut organ is not strictly limited to SBE species (34). Although we revealed that the bacterial sorting organ in the bean bug gut winnows out symbionts from nonsymbionts, only a limited number of bacterial species (i.e., Eschelichia coli, Pseudomonas putida, and Bacillus subtilis) have been tested as nonsymbionts (14).…”

Section: Significancementioning

confidence: 89%

“…Symbiotic Organ in Coinfection Assays. PBE Burkholderia and Pandoraea species are common bacterial groups in soil environments, and detected frequently with SBE Burkholderia (34,38,39). Given the high infectivity and benefits of PBE and Pandoraea, why do only SBE Burkholderia prevail in field populations of the bean bug?…”

Section: Sbe Burkholderia Always Outcompete Pbe and Pandoraea In The Gutmentioning

confidence: 99%

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

Itoh

Jang

Takeshita

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

107

131

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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.

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Section: Significancementioning

confidence: 89%

Section: Sbe Burkholderia Always Outcompete Pbe and Pandoraea In The Gutmentioning

confidence: 99%

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

Itoh

Jang

Takeshita

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

107

131

View full text Add to dashboard Cite

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“…This suggests that horizontal transmission of Burkholderia can occur via enrichment of the symbiont in the local environment by adult insects. While this possibility has been proposed previously (Itoh et al, 2018) to our knowledge this is the first empirical evidence that it can occur in a bug-Burkholderia symbiosis. It seems plausible that horizontal transmission via environmental enrichment also happens in the wild, given the insects' tendency to aggregate.…”

Section: Discussionmentioning

confidence: 64%

Continent-Scale Sampling Reveals Fine-Scale Turnover in a Beneficial Bug Symbiont

et al. 2020

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Many members of animal-associated microbial communities, including the gut flora, are acquired from their host's environment. While many of these communities are species rich, some true bugs (Hemiptera) in the superfamilies Lygaeoidea and Coreidae allow only ingested Burkholderia to colonize and reproduce in a large portion of the midgut. We studied the spatial structuring of Burkholderia associated with a widespread omnivorous bug genus, Jalysus (Berytidae). We sampled Wickham's stilt bug, Jalysus wickhami, across the United States and performed limited sampling of its sister species, the spined stilt bug Jalysus spinosus. We asked: (1) What Burkholderia strains are hosted by Jalysus at different locations? (2) Does host insect species, host plant species, or location influence the strain these insects acquire? (3) How does Burkholderia affect the development and reproductive fitness of J. wickhami? We found: (1) Sixty-one Burkholderia strains were present across a sample of 352 individuals, but one strain dominated, accounting for almost half of all symbiont reads. Most strains were closely related to other hemipteran Burkholderia symbionts. (2) Many individuals hosted more than one strain of Burkholderia. (3) J. wickhami and J. spinosus did not differ in the strains they hosted. (4) Insects that fed on different plant species tended to host different Burkholderia, but this accounted for only 4% of the variation in strains hosted. In contrast, the location at which an insect was collected explained 27% of the variation in symbiont strains. (5) Burkholderia confers important fitness benefits to J. wickhami. In laboratory experiments, aposymbiotic (Burkholderia-free) insects developed more slowly and laid fewer eggs than symbiotic (Burkholderia-colonized) insects. (6) In the lab, nymphs sometimes acquired Burkholderia via indirect exposure to adults, indicating that horizontal symbiont transmission can occur via adult insect-mediated enrichment of Burkholderia in the local environment-a phenomenon not previously reported in bug-Burkholderia relationships. Taken together, the results suggest that for these bugs, critical nutritional requirements are outsourced to a highly diverse and spatially structured collection of Burkholderia strains acquired from the environment and, occasionally, from conspecific adults.

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“…There are a number of remarkable studies that illustrate the substantial impact of locally adapted microbes on hosts, suggesting that microbes may underlie host adaptation to populations in stressful environments. For example, bean bugs can gain pesticide resistance through acquiring a pesticide degrading soil bacterium, Burkholderia [79][80][81] . Many other hosts utilize their microbiome to detoxify harmful chemicals.…”

Section: Hosts Leverage Locally Adapted Microbesmentioning

confidence: 99%

Can the microbiome influence host evolutionary trajectories?

Henry

Bruijning

Forsberg

et al. 2019

Preprint

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The microbiome shapes many traits in hosts, but we still do not understand how it influences host evolution. To impact host evolution, the microbiome must be heritable and have phenotypic effects on the host. However, the complex inheritance and context-dependence of the microbiome challenges traditional models of organismal evolution. Here, we take a multifaceted approach to identify conditions in which the microbiome influences host evolutionary trajectories. We explore quantitative genetic models to highlight how microbial inheritance and phenotypic effects can modulate host evolutionary responses to selection. We synthesize the literature across diverse taxa to find common scenarios of microbiome driven host evolution. First, hosts may leverage locally adapted microbes, increasing survivorship in stressful environments. Second, microbial variation may increase host phenotypic variation, enabling exploration of novel fitness landscapes. We further illustrate these effects by performing a meta-analysis of artificial selection in Drosophila, finding that bacterial diversity also frequently responds to host selection. We conclude by outlining key avenues of research and experimental procedures to improve our understanding of the complex interplay between hosts and microbiomes. By synthesizing perspectives through multiple conceptual and analytical approaches, we show how microbiomes can influence the evolutionary trajectories of hosts.

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Infection dynamics of insecticide-degrading symbionts from soil to insects in response to insecticide spraying

Cited by 61 publications

References 61 publications

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

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

Continent-Scale Sampling Reveals Fine-Scale Turnover in a Beneficial Bug Symbiont

Can the microbiome influence host evolutionary trajectories?

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