An ancient but promiscuous host–symbiont association between <i>Burkholderia</i> gut symbionts and their heteropteran hosts

Kikuchi, Yoshitomo; Hosokawa, Takahiro; Fukatsu, Takema

doi:10.1038/ismej.2010.150

Cited by 237 publications

(334 citation statements)

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“…The oriental chinch bug Cavelerius saccharivorus (Fig. 5B) is among the major pests of sugarcane in subtropical Asia (11) and harbors Burkholderia symbiont in the midgut (17). Among adult insects of C. saccharivorus collected at sugarcane fields in Minami-Daito, 8% (47/582) exhibited remarkable fenitrothion-degrading activities in the posterior midgut ( Fig.…”

Section: Natural Infection Of Fenitrothion-degrading Symbiont In a Pestmentioning

confidence: 99%

“…In our extensive field survey, all 846 individuals of R. pedestris from 13 localities exhibited no fenitrothion-degrading activity when their dissected symbiotic organ was subjected to the degradation assay (Table S4). Furthermore, we examined field populations of the rice bug Leptocorisa chinensis, which is known as a pest of rice (11) and also associated with the Burkholderia gut symbiont (12,17). All 542 individuals from seven localities exhibited no significant fenitrithion-degrading activity in the symbiotic organ (Table S4).…”

Section: Fenitrothion-degrading Burkholderia Symbionts Confer Insectimentioning

confidence: 99%

“…Recent extensive surveys revealed that a number of stinkbug species allied to R. pedestris are also associated with the Burkholderia gut symbionts (17). The stinkbugBurkholderia associations are promiscuous both evolutionarily and ecologically: The symbiont phylogeny does not reflect the host phylogeny, and the stinkbug-associated symbiont strains form a mixed clade with soil-derived Burkholderia isolates (12,13,17). Notably, the symbiont clade contains a number of soil-derived, fenitrothion-degrading Burkholderia isolates (Fig.…”

mentioning

confidence: 99%

“…In contrast to vertical symbiont transmission ubiquitously found in many insects (14,15), R. pedertris environmentally acquires the Burkholderia symbiont at the second instar stage from the soil (16), which is similar to environmental acquisition of Rhizobium by leguminous plants. Recent extensive surveys revealed that a number of stinkbug species allied to R. pedestris are also associated with the Burkholderia gut symbionts (17). The stinkbugBurkholderia associations are promiscuous both evolutionarily and ecologically: The symbiont phylogeny does not reflect the host phylogeny, and the stinkbug-associated symbiont strains form a mixed clade with soil-derived Burkholderia isolates (12,13,17).…”

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confidence: 99%

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Symbiont-mediated insecticide resistance

Kikuchi

Hayatsu

Hosokawa

et al. 2012

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

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696

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Development of insecticide resistance has been a serious concern worldwide, whose mechanisms have been attributed to evolutionary changes in pest insect genomes such as alteration of drug target sites, up-regulation of degrading enzymes, and enhancement of drug excretion. Here, we report a previously unknown mechanism of insecticide resistance: Infection with an insecticide-degrading bacterial symbiont immediately establishes insecticide resistance in pest insects. The bean bug Riptortus pedestris and allied stinkbugs harbor mutualistic gut symbiotic bacteria of the genus Burkholderia , which are acquired by nymphal insects from environmental soil every generation. In agricultural fields, fenitrothion-degrading Burkolderia strains are present at very low densities. We demonstrated that the fenitrothion-degrading Burkholderia strains establish a specific and beneficial symbiosis with the stinkbugs and confer a resistance of the host insects against fenitrothion. Experimental applications of fenitrothion to field soils drastically enriched fenitrothion-degrading bacteria from undetectable levels to >80% of total culturable bacterial counts in the field soils, and >90% of stinkbugs reared with the enriched soil established symbiosis with fenitrothion-degrading Burkholderia . In a Japanese island where fenitrothion has been constantly applied to sugarcane fields, we identified a stinkbug population wherein the insects live on sugarcane and ≈8% of them host fenitrothion-degrading Burkholderia . Our finding suggests the possibility that the symbiont-mediated insecticide resistance may develop even in the absence of pest insects, quickly establish within a single insect generation, and potentially move around horizontally between different pest insects and other organisms.

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Section: Natural Infection Of Fenitrothion-degrading Symbiont In a Pestmentioning

confidence: 99%

Section: Fenitrothion-degrading Burkholderia Symbionts Confer Insectimentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Symbiont-mediated insecticide resistance

Kikuchi

Hayatsu

Hosokawa

et al. 2012

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

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696

623

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“…This symbiont belongs to a member of the betaproteobacterial genus Burkholderia, and is acquired orally by host nymphs from the environment every generation. Further, Burkholderia can be easily cultivable and genetically manipulatable (Kikuchi et al, 2007(Kikuchi et al, , 2011aKikuchi and Fukatsu, 2013;Kim et al, 2013a, b). Using this model system, we performed transposon-mediated random mutagenesis of Burkholderia symbiont strain and screened the mutant strains for their symbiotic capabilities in the Riptortus host.…”

Section: Introductionmentioning

confidence: 99%

Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug

et al. 2013

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The Riptortus–Burkholderia symbiotic system represents a promising experimental model to study the molecular mechanisms involved in insect–bacterium symbiosis due to the availability of genetically manipulated Burkholderia symbiont. Using transposon mutagenesis screening, we found a symbiosis-deficient mutant that was able to colonize the host insect but failed to induce normal development of host’s symbiotic organ. The disrupted gene was identified as purL involved in purine biosynthesis. In vitro growth impairment of the purL mutant and its growth dependency on adenine and adenosine confirmed the functional disruption of the purine synthesis gene. The purL mutant also showed defects in biofilm formation, and this defect was not rescued by supplementation of purine derivatives. When inoculated to host insects, the purL mutant was initially able to colonize the symbiotic organ but failed to attain a normal infection density. The low level of infection density of the purL mutant attenuated the development of the host’s symbiotic organ at early instar stages and reduced the host’s fitness throughout the nymphal stages. Another symbiont mutant-deficient in a purine biosynthesis gene, purM, showed phenotypes similar to those of the purL mutant both in vitro and in vivo, confirming that the purL phenotypes are due to disrupted purine biosynthesis. These results demonstrate that the purine biosynthesis genes of the Burkholderia symbiont are critical for the successful accommodation of symbiont within the host, thereby facilitating the development of the host’s symbiotic organ and enhancing the host’s fitness values.

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SYMBIOTIC FACTORS IN Burkholderia ESSENTIAL FOR ESTABLISHING AN ASSOCIATION WITH THE BEAN BUG, Riptortus pedestris

Kim

Lee

2014

Arch Insect Biochem Physiol

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Symbiotic bacteria are common in insects and intimately affect the various aspects of insect host biology. In a number of insect symbiosis models, it has been possible to elucidate the effects of the symbiont on host biology, whereas there is a limited understanding of the impact of the association on the bacterial symbiont, mainly due to the difficulty of cultivating insect symbionts in vitro. Furthermore, the molecular features that determine the establishment and persistence of the symbionts in their host (i.e., symbiotic factors) have remained elusive. However, the recently established model, the bean bug Riptortus pedestris, provides a good opportunity to study bacterial symbiotic factors at a molecular level through their cultivable symbionts. Bean bugs acquire genus Burkholderia cells from the environment and harbor them as gut symbionts in the specialized posterior midgut. The genome of the Burkholderia symbiont was sequenced, and the genomic information was used to generate genetically manipulated Burkholderia symbiont strains. Using mutant symbionts, we identified several novel symbiotic factors necessary for establishing a successful association with the host gut. In this review, these symbiotic factors are classified into three categories based on the colonization dynamics of the mutant symbiont strains: initiation, accommodation, and persistence factors. In addition, the molecular characteristics of the symbiotic factors are described. These newly identified symbiotic factors and on-going studies of the Riptortus-Burkholderia symbiosis are expected to contribute to the understanding of the molecular cross-talk between insects and bacterial symbionts that are of ecological and evolutionary importance.

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An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts

Cited by 237 publications

References 59 publications

Symbiont-mediated insecticide resistance

Symbiont-mediated insecticide resistance

Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug

SYMBIOTIC FACTORS IN Burkholderia ESSENTIAL FOR ESTABLISHING AN ASSOCIATION WITH THE BEAN BUG, Riptortus pedestris

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