Symbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection

ABSTRACT Colonization resistance, i.e., the protective effects of associated microbiota for the animal host against pathogen infection, has been studied widely over the last 100 years. However, few molecules mediating colonization resistance have been identified. In the symbiosis formed by Delia ant...

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Autores principales: Fangyuan Zhou, Letian Xu, Xiaoqing Wu, Xiaoyan Zhao, Mei Liu, Xinjian Zhang
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:fbb74e8c5c0b46eca51d16e9adab22b32021-12-02T19:47:37ZSymbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection10.1128/mSystems.00778-202379-5077https://doaj.org/article/fbb74e8c5c0b46eca51d16e9adab22b32020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00778-20https://doaj.org/toc/2379-5077ABSTRACT Colonization resistance, i.e., the protective effects of associated microbiota for the animal host against pathogen infection, has been studied widely over the last 100 years. However, few molecules mediating colonization resistance have been identified. In the symbiosis formed by Delia antiqua and its associated microbes, six bacteria protect larvae from infection with the entomopathogen Beauveria bassiana, providing an ideal model to investigate the chemical mechanism for colonization resistance. Subsequently using this symbiotic system, we first compared effects of the six bacterial species, and one control bacterium (Klebsiella oxytoca) that showed no antifungal effects, on B. bassiana and its infection of D. antiqua. Second, metabolomic profiles of the six bacteria and K. oxytoca were compared to identify candidate metabolites that may prevent infection. Third, the concentrations of candidate metabolites in situ from axenic and nonaxenic larvae were determined. Finally, effects of artificial metabolite cocktails on B. bassiana and its infection of D. antiqua larvae were determined. Results showed that compared to K. oxytoca, the six bacteria produced a metabolite cocktail showing inhibitory effects on conidial germination, mycelial growth of B. bassiana, and fungal infection. Our work revealed novel molecules that mediate colonization resistance, which could help in developing chemical mechanisms of colonization resistance. Moreover, this work may aid in discovery and expansion of new bioactive antibiotics, promoting development of prophylactic and therapeutic approaches for treating infectious diseases. IMPORTANCE The protection of associated microbiota for their animal hosts against pathogen infection has been studied widely over the last 100 years. However, how those microbes protect the animal host remains unclear. In former studies, body surface microbes of one insect, Delia antiqua, protected the insect larvae from infection with the entomopathogen Beauveria bassiana. By comparing the metabolites produced by microbes that protect the insect and microbes that cannot protect the insect, the question of how the microbes protect the insect is answered. It turns out that body surface bacteria produce a metabolite cocktail that inhibits colonization of B. bassiana and consequently protects the insect. This work reveals novel molecules with antifungal activity, which may aid in discovery and expansion of new prophylactic and therapeutic natural chemicals for treating infectious diseases.Fangyuan ZhouLetian XuXiaoqing WuXiaoyan ZhaoMei LiuXinjian ZhangAmerican Society for Microbiologyarticlecolonization resistanceinsect-microbe symbiosisdefensive associationmutualismMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution DOAJ
collection DOAJ
language EN
topic colonization resistance
insect-microbe symbiosis
defensive association
mutualism
Microbiology
QR1-502
spellingShingle colonization resistance
insect-microbe symbiosis
defensive association
mutualism
Microbiology
QR1-502
Fangyuan Zhou
Letian Xu
Xiaoqing Wu
Xiaoyan Zhao
Mei Liu
Xinjian Zhang
Symbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection
description ABSTRACT Colonization resistance, i.e., the protective effects of associated microbiota for the animal host against pathogen infection, has been studied widely over the last 100 years. However, few molecules mediating colonization resistance have been identified. In the symbiosis formed by Delia antiqua and its associated microbes, six bacteria protect larvae from infection with the entomopathogen Beauveria bassiana, providing an ideal model to investigate the chemical mechanism for colonization resistance. Subsequently using this symbiotic system, we first compared effects of the six bacterial species, and one control bacterium (Klebsiella oxytoca) that showed no antifungal effects, on B. bassiana and its infection of D. antiqua. Second, metabolomic profiles of the six bacteria and K. oxytoca were compared to identify candidate metabolites that may prevent infection. Third, the concentrations of candidate metabolites in situ from axenic and nonaxenic larvae were determined. Finally, effects of artificial metabolite cocktails on B. bassiana and its infection of D. antiqua larvae were determined. Results showed that compared to K. oxytoca, the six bacteria produced a metabolite cocktail showing inhibitory effects on conidial germination, mycelial growth of B. bassiana, and fungal infection. Our work revealed novel molecules that mediate colonization resistance, which could help in developing chemical mechanisms of colonization resistance. Moreover, this work may aid in discovery and expansion of new bioactive antibiotics, promoting development of prophylactic and therapeutic approaches for treating infectious diseases. IMPORTANCE The protection of associated microbiota for their animal hosts against pathogen infection has been studied widely over the last 100 years. However, how those microbes protect the animal host remains unclear. In former studies, body surface microbes of one insect, Delia antiqua, protected the insect larvae from infection with the entomopathogen Beauveria bassiana. By comparing the metabolites produced by microbes that protect the insect and microbes that cannot protect the insect, the question of how the microbes protect the insect is answered. It turns out that body surface bacteria produce a metabolite cocktail that inhibits colonization of B. bassiana and consequently protects the insect. This work reveals novel molecules with antifungal activity, which may aid in discovery and expansion of new prophylactic and therapeutic natural chemicals for treating infectious diseases.
format article
author Fangyuan Zhou
Letian Xu
Xiaoqing Wu
Xiaoyan Zhao
Mei Liu
Xinjian Zhang
author_facet Fangyuan Zhou
Letian Xu
Xiaoqing Wu
Xiaoyan Zhao
Mei Liu
Xinjian Zhang
author_sort Fangyuan Zhou
title Symbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection
title_short Symbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection
title_full Symbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection
title_fullStr Symbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection
title_full_unstemmed Symbiotic Bacterium-Derived Organic Acids Protect <italic toggle="yes">Delia antiqua</italic> Larvae from Entomopathogenic Fungal Infection
title_sort symbiotic bacterium-derived organic acids protect <italic toggle="yes">delia antiqua</italic> larvae from entomopathogenic fungal infection
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/fbb74e8c5c0b46eca51d16e9adab22b3
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