Collapse of Insect Gut Symbiosis under Simulated Climate Change

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...

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Main Authors: Yoshitomo Kikuchi, Akiyo Tada, Dmitry L. Musolin, Nobuhiro Hari, Takahiro Hosokawa, Kenji Fujisaki, Takema Fukatsu
Format: Article
Language:English
Published: American Society for Microbiology 2016-10-01
Series:mBio
Online Access:http://mbio.asm.org/cgi/content/full/7/5/e01578-16
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spelling doaj-dfea285af518426eaf575e44b41f258a2021-07-02T03:26:54ZengAmerican Society for MicrobiologymBio2150-75112016-10-0175e01578-1610.1128/mBio.01578-16Collapse of Insect Gut Symbiosis under Simulated Climate ChangeYoshitomo KikuchiAkiyo TadaDmitry L. MusolinNobuhiro HariTakahiro HosokawaKenji FujisakiTakema FukatsuGlobal 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.http://mbio.asm.org/cgi/content/full/7/5/e01578-16
collection DOAJ
language English
format Article
sources DOAJ
author Yoshitomo Kikuchi
Akiyo Tada
Dmitry L. Musolin
Nobuhiro Hari
Takahiro Hosokawa
Kenji Fujisaki
Takema Fukatsu
spellingShingle Yoshitomo Kikuchi
Akiyo Tada
Dmitry L. Musolin
Nobuhiro Hari
Takahiro Hosokawa
Kenji Fujisaki
Takema Fukatsu
Collapse of Insect Gut Symbiosis under Simulated Climate Change
mBio
author_facet Yoshitomo Kikuchi
Akiyo Tada
Dmitry L. Musolin
Nobuhiro Hari
Takahiro Hosokawa
Kenji Fujisaki
Takema Fukatsu
author_sort Yoshitomo Kikuchi
title Collapse of Insect Gut Symbiosis under Simulated Climate Change
title_short Collapse of Insect Gut Symbiosis under Simulated Climate Change
title_full Collapse of Insect Gut Symbiosis under Simulated Climate Change
title_fullStr Collapse of Insect Gut Symbiosis under Simulated Climate Change
title_full_unstemmed Collapse of Insect Gut Symbiosis under Simulated Climate Change
title_sort collapse of insect gut symbiosis under simulated climate change
publisher American Society for Microbiology
series mBio
issn 2150-7511
publishDate 2016-10-01
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.
url http://mbio.asm.org/cgi/content/full/7/5/e01578-16
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