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Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis.

ABSTRACT: Many bacteria accumulate granules of polyhydroxyalkanoate (PHA) within their cells, which confer resistance to nutritional depletion and other environmental stresses. Here, we report an unexpected involvement of the bacterial endocellular storage polymer, PHA, in an insect-bacterium symbiotic association. The bean bug Riptortus pedestris harbors a beneficial and specific gut symbiont of the ?-proteobacterial genus Burkholderia, which is orally acquired by host nymphs from the environment every generation and easily cultivable and genetically manipulatable. Biochemical and cytological comparisons between symbiotic and cultured Burkholderia detected more PHA granules consisting of poly-3-hydroxybutyrate and associated phasin (PhaP) protein in the symbiotic Burkholderia. Among major PHA synthesis genes, phaB and phaC were disrupted by homologous recombination together with the phaP gene, whereby ?phaB, ?phaC, and ?phaP mutants were generated. Both in culture and in symbiosis, accumulation of PHA granules was strongly suppressed in ?phaB and ?phaC, but only moderately in ?phaP. In symbiosis, the host insects infected with ?phaB and ?phaC exhibited significantly lower symbiont densities and smaller body sizes. These deficient phenotypes associated with ?phaB and ?phaC were restored by complementation of the mutants with plasmids encoding a functional phaB/phaC gene. Retention analysis of the plasmids revealed positive selection acting on the functional phaB/phaC in symbiosis. These results indicate that the PHA synthesis genes of the Burkholderia symbiont are required for normal symbiotic association with the Riptortus host. In vitro culturing analyses confirmed vulnerability of the PHA gene mutants to environmental stresses, suggesting that PHA may play a role in resisting stress under symbiotic conditions.

SUBMITTER: Kim JK

PROVIDER: S-EPMC3696747 | biostudies-literature | 2013 Jun

REPOSITORIES: biostudies-literature

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Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis.

Kim Jiyeun Kate JK Won Yeo Jin YJ Nikoh Naruo N Nakayama Hiroshi H Han Sang Heum SH Kikuchi Yoshitomo Y Rhee Young Ha YH Park Ha Young HY Kwon Jeong Yun JY Kurokawa Kenji K Dohmae Naoshi N Fukatsu Takema T Lee Bok Luel BL

Proceedings of the National Academy of Sciences of the United States of America 20130611 26

Many bacteria accumulate granules of polyhydroxyalkanoate (PHA) within their cells, which confer resistance to nutritional depletion and other environmental stresses. Here, we report an unexpected involvement of the bacterial endocellular storage polymer, PHA, in an insect-bacterium symbiotic association. The bean bug Riptortus pedestris harbors a beneficial and specific gut symbiont of the β-proteobacterial genus Burkholderia, which is orally acquired by host nymphs from the environment every g ...[more]

PMID: 23757494

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Project description:Global warming impacts diverse organisms not only directly but also indirectly via other organisms with which they interact. Recently, the possibility that elevated temperatures resulting from global warming may substantially affect biodiversity through disrupting mutualistic/parasitic associations has been highlighted. Here we report an experimental demonstration that global warming can affect a pest insect via suppression of its obligate bacterial symbiont. The southern green stinkbug Nezara viridula depends on a specific gut bacterium for its normal growth and survival. When the insects were reared inside or outside a simulated warming incubator wherein temperature was controlled at 2.5°C higher than outside, the insects reared in the incubator exhibited severe fitness defects (i.e., retarded growth, reduced size, yellowish body color, etc.) and significant reduction of symbiont population, particularly in the midsummer season, whereas the insects reared outside did not. Rearing at 30°C or 32.5°C resulted in similar defective phenotypes of the insects, whereas no adult insects emerged at 35°C. Notably, experimental symbiont suppression by an antibiotic treatment also induced similar defective phenotypes of the insects, indicating that the host's defective phenotypes are attributable not to the heat stress itself but to the suppression of the symbiont population induced by elevated temperature. These results strongly suggest that high temperature in the midsummer season negatively affects the insects not directly but indirectly via the heat-vulnerable obligate bacterial symbiont, which highlights the practical relevance of mutualism collapse in this warming world. Climate change is among the biggest environmental issues in the contemporary world, and its impact on the biodiversity and ecosystem is not only of scientific interest but also of practical concern for the general public. On the basis of our laboratory data obtained under strictly controlled environmental conditions and our simulated warming data obtained in seminatural settings (elevated 2.5°C above the normal temperature), we demonstrate here that Nezara viridula, the notorious stinkbug pest, suffers serious fitness defects in the summer season under the simulated warming conditions, wherein high temperature acts on the insect not directly but indirectly via suppression of its obligate gut bacterium. Our finding highlights that heat-susceptible symbionts can be the "Achilles' heel" of symbiont-dependent organisms under climate change conditions.

Dataset Information

Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis.

Publications

Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis.

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