Collapse of insect gut symbiosis under simulated climate change

Yoshitomo Kikuchi, Akiyo Tada, Dmitry L. Musolin, Nobuhiro Hari, Takahiro Hosokawa, Kenji Fujisaki, Takema Fukatsu

研究成果: ジャーナルへの寄稿記事

40 引用 (Scopus)

抄録

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.

元の言語英語
記事番号e01578-16
ジャーナルmBio
7
発行部数5
DOI
出版物ステータス出版済み - 9 1 2016

Fingerprint

Symbiosis
Climate Change
Insects
Global Warming
Incubators
Temperature
Phenotype
Hot Temperature
Biodiversity
Body Size
Growth
Population
Color
Anti-Bacterial Agents
Bacteria

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Virology

これを引用

Kikuchi, Y., Tada, A., Musolin, D. L., Hari, N., Hosokawa, T., Fujisaki, K., & Fukatsu, T. (2016). Collapse of insect gut symbiosis under simulated climate change. mBio, 7(5), [e01578-16]. https://doi.org/10.1128/mBio.01578-16

Collapse of insect gut symbiosis under simulated climate change. / Kikuchi, Yoshitomo; Tada, Akiyo; Musolin, Dmitry L.; Hari, Nobuhiro; Hosokawa, Takahiro; Fujisaki, Kenji; Fukatsu, Takema.

:: mBio, 巻 7, 番号 5, e01578-16, 01.09.2016.

研究成果: ジャーナルへの寄稿記事

Kikuchi, Y, Tada, A, Musolin, DL, Hari, N, Hosokawa, T, Fujisaki, K & Fukatsu, T 2016, 'Collapse of insect gut symbiosis under simulated climate change', mBio, 巻. 7, 番号 5, e01578-16. https://doi.org/10.1128/mBio.01578-16
Kikuchi Y, Tada A, Musolin DL, Hari N, Hosokawa T, Fujisaki K その他. Collapse of insect gut symbiosis under simulated climate change. mBio. 2016 9 1;7(5). e01578-16. https://doi.org/10.1128/mBio.01578-16
Kikuchi, Yoshitomo ; Tada, Akiyo ; Musolin, Dmitry L. ; Hari, Nobuhiro ; Hosokawa, Takahiro ; Fujisaki, Kenji ; Fukatsu, Takema. / Collapse of insect gut symbiosis under simulated climate change. :: mBio. 2016 ; 巻 7, 番号 5.
@article{e85cfbdc1c1e4319b179de7d7df2a2e0,
title = "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 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.",
author = "Yoshitomo Kikuchi and Akiyo Tada and Musolin, {Dmitry L.} and Nobuhiro Hari and Takahiro Hosokawa and Kenji Fujisaki and Takema Fukatsu",
year = "2016",
month = "9",
day = "1",
doi = "10.1128/mBio.01578-16",
language = "English",
volume = "7",
journal = "mBio",
issn = "2161-2129",
publisher = "American Society for Microbiology",
number = "5",

}

TY - JOUR

T1 - Collapse of insect gut symbiosis under simulated climate change

AU - Kikuchi, Yoshitomo

AU - Tada, Akiyo

AU - Musolin, Dmitry L.

AU - Hari, Nobuhiro

AU - Hosokawa, Takahiro

AU - Fujisaki, Kenji

AU - Fukatsu, Takema

PY - 2016/9/1

Y1 - 2016/9/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84994791396&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84994791396&partnerID=8YFLogxK

U2 - 10.1128/mBio.01578-16

DO - 10.1128/mBio.01578-16

M3 - Article

C2 - 27703075

AN - SCOPUS:84994791396

VL - 7

JO - mBio

JF - mBio

SN - 2161-2129

IS - 5

M1 - e01578-16

ER -