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Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest

Spodoptera frugiperda (Lepidoptera: Noctuidae) is a migratory agricultural pest that is devastating on a global scale. Beauveria bassiana is a filamentous entomopathogenic fungus that has a strong pathogenic effect on Lepidoptera pests but little is known about the microbial community in the host gu...

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Autores principales: Peng, Yuejin, Wen, Shaohai, Wang, Guang, Zhang, Xu, Di, Teng, Du, Guangzu, Chen, Bin, Zhang, Limin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10532432/
https://www.ncbi.nlm.nih.gov/pubmed/37755014
http://dx.doi.org/10.3390/jof9090906
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author Peng, Yuejin
Wen, Shaohai
Wang, Guang
Zhang, Xu
Di, Teng
Du, Guangzu
Chen, Bin
Zhang, Limin
author_facet Peng, Yuejin
Wen, Shaohai
Wang, Guang
Zhang, Xu
Di, Teng
Du, Guangzu
Chen, Bin
Zhang, Limin
author_sort Peng, Yuejin
collection PubMed
description Spodoptera frugiperda (Lepidoptera: Noctuidae) is a migratory agricultural pest that is devastating on a global scale. Beauveria bassiana is a filamentous entomopathogenic fungus that has a strong pathogenic effect on Lepidoptera pests but little is known about the microbial community in the host gut and the dominant populations in fungus-infected insects. B. bassiana AJS91881 was isolated and identified from the infected larvae of Spodoptera litura. The virulence of AJS91881 to the eggs, larvae, pupae and adults of S. frugiperda was measured. Moreover, the gut microbial community diversity of healthy and fungus-infected insects was analyzed. Our results showed that after treatment with B. bassiana AJS91881, the egg hatching rate, larval survival rate and adult lifespan of the insects were significantly reduced, and the pupae rigor rate was significantly increased compared to that of the control group. Additionally, the gut microbial community was reconstructed after B. bassiana infection. At the phylum and genus level, the relative abundance of the Proteobacteria and Serratia increased significantly in the B. bassiana treatment group. The KEGG function prediction results showed that fungal infection affected insect gut metabolism, environmental information processing, genetic information processing, organism systems and cellular processes. Fungal infection was closely related to the metabolism of various substances in the insect gut. Serratia marcescens was the bacterium with the highest relative abundance after infection by B. bassiana; intestinal bacteria S. marcescens inhibited the infection of insect fungi B. bassiana against the S. frugiperda. The presence of gut bacteria also significantly reduced the virulence of the fungi against the insects when compared to the group with the larvae fed antibiotics that were infected with fungal suspension (Germfree, GF) and healthy larvae that were infected with fungal suspension prepared with an antibiotic solution (+antibiotic). In conclusion, the reconstruction of the insect intestinal bacterial community is an indispensable link for understanding the pathogenicity of B. bassiana against S. frugiperda. Most importantly, in the later stage of fungal infection, the increased abundance of S. marcescens in the insect intestine inhibited the virulence of B. bassiana to some extent. The findings aid in understanding changes in the gut microbiota during the early stages of entomopathogenic fungal infection of insects and the involvement of insect gut microbes in host defense mediated by pathogenic fungal infection. This study is also conducive to understanding the interaction between entomopathogenic fungi, hosts and gut microbes, and provides a new idea for the joint use of entomopathogenic fungi and gut bacteria to control pests.
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spelling pubmed-105324322023-09-28 Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest Peng, Yuejin Wen, Shaohai Wang, Guang Zhang, Xu Di, Teng Du, Guangzu Chen, Bin Zhang, Limin J Fungi (Basel) Article Spodoptera frugiperda (Lepidoptera: Noctuidae) is a migratory agricultural pest that is devastating on a global scale. Beauveria bassiana is a filamentous entomopathogenic fungus that has a strong pathogenic effect on Lepidoptera pests but little is known about the microbial community in the host gut and the dominant populations in fungus-infected insects. B. bassiana AJS91881 was isolated and identified from the infected larvae of Spodoptera litura. The virulence of AJS91881 to the eggs, larvae, pupae and adults of S. frugiperda was measured. Moreover, the gut microbial community diversity of healthy and fungus-infected insects was analyzed. Our results showed that after treatment with B. bassiana AJS91881, the egg hatching rate, larval survival rate and adult lifespan of the insects were significantly reduced, and the pupae rigor rate was significantly increased compared to that of the control group. Additionally, the gut microbial community was reconstructed after B. bassiana infection. At the phylum and genus level, the relative abundance of the Proteobacteria and Serratia increased significantly in the B. bassiana treatment group. The KEGG function prediction results showed that fungal infection affected insect gut metabolism, environmental information processing, genetic information processing, organism systems and cellular processes. Fungal infection was closely related to the metabolism of various substances in the insect gut. Serratia marcescens was the bacterium with the highest relative abundance after infection by B. bassiana; intestinal bacteria S. marcescens inhibited the infection of insect fungi B. bassiana against the S. frugiperda. The presence of gut bacteria also significantly reduced the virulence of the fungi against the insects when compared to the group with the larvae fed antibiotics that were infected with fungal suspension (Germfree, GF) and healthy larvae that were infected with fungal suspension prepared with an antibiotic solution (+antibiotic). In conclusion, the reconstruction of the insect intestinal bacterial community is an indispensable link for understanding the pathogenicity of B. bassiana against S. frugiperda. Most importantly, in the later stage of fungal infection, the increased abundance of S. marcescens in the insect intestine inhibited the virulence of B. bassiana to some extent. The findings aid in understanding changes in the gut microbiota during the early stages of entomopathogenic fungal infection of insects and the involvement of insect gut microbes in host defense mediated by pathogenic fungal infection. This study is also conducive to understanding the interaction between entomopathogenic fungi, hosts and gut microbes, and provides a new idea for the joint use of entomopathogenic fungi and gut bacteria to control pests. MDPI 2023-09-06 /pmc/articles/PMC10532432/ /pubmed/37755014 http://dx.doi.org/10.3390/jof9090906 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Peng, Yuejin
Wen, Shaohai
Wang, Guang
Zhang, Xu
Di, Teng
Du, Guangzu
Chen, Bin
Zhang, Limin
Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest
title Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest
title_full Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest
title_fullStr Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest
title_full_unstemmed Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest
title_short Reconstruction of Gut Bacteria in Spodoptera frugiperda Infected by Beauveria bassiana Affects the Survival of Host Pest
title_sort reconstruction of gut bacteria in spodoptera frugiperda infected by beauveria bassiana affects the survival of host pest
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10532432/
https://www.ncbi.nlm.nih.gov/pubmed/37755014
http://dx.doi.org/10.3390/jof9090906
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