Collapse of Insect Gut Symbiosis under Simulated Climate Change

ABSTRACT 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 asso...

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Autores principales:	Yoshitomo Kikuchi, Akiyo Tada, Dmitry L. Musolin, Nobuhiro Hari, Takahiro Hosokawa, Kenji Fujisaki, Takema Fukatsu
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/928bc87b2164450a8922e684fa71174d
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spelling	oai:doaj.org-article:928bc87b2164450a8922e684fa71174d2021-11-15T15:50:14ZCollapse of Insect Gut Symbiosis under Simulated Climate Change10.1128/mBio.01578-162150-7511https://doaj.org/article/928bc87b2164450a8922e684fa71174d2016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01578-16https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE 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.Yoshitomo KikuchiAkiyo TadaDmitry L. MusolinNobuhiro HariTakahiro HosokawaKenji FujisakiTakema FukatsuAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Yoshitomo Kikuchi Akiyo Tada Dmitry L. Musolin Nobuhiro Hari Takahiro Hosokawa Kenji Fujisaki Takema Fukatsu Collapse of Insect Gut Symbiosis under Simulated Climate Change
description	ABSTRACT 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. IMPORTANCE 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.
format	article
author	Yoshitomo Kikuchi Akiyo Tada Dmitry L. Musolin Nobuhiro Hari Takahiro Hosokawa Kenji Fujisaki Takema Fukatsu
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
publishDate	2016
url	https://doaj.org/article/928bc87b2164450a8922e684fa71174d
work_keys_str_mv	AT yoshitomokikuchi collapseofinsectgutsymbiosisundersimulatedclimatechange AT akiyotada collapseofinsectgutsymbiosisundersimulatedclimatechange AT dmitrylmusolin collapseofinsectgutsymbiosisundersimulatedclimatechange AT nobuhirohari collapseofinsectgutsymbiosisundersimulatedclimatechange AT takahirohosokawa collapseofinsectgutsymbiosisundersimulatedclimatechange AT kenjifujisaki collapseofinsectgutsymbiosisundersimulatedclimatechange AT takemafukatsu collapseofinsectgutsymbiosisundersimulatedclimatechange
_version_	1718427473024122880

Collapse of Insect Gut Symbiosis under Simulated Climate Change

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