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

<i>Spodoptera frugiperda</i> (Lepidoptera: Noctuidae) is a migratory agricultural pest that is devastating on a global scale. <i>Beauveria bassiana</i> is a filamentous entomopathogenic fungus that has a strong pathogenic effect on Lepidoptera pests but little is known about...

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Main Authors: Yuejin Peng, Shaohai Wen, Guang Wang, Xu Zhang, Teng Di, Guangzu Du, Bin Chen, Limin Zhang
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/9/9/906
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author Yuejin Peng
Shaohai Wen
Guang Wang
Xu Zhang
Teng Di
Guangzu Du
Bin Chen
Limin Zhang
author_facet Yuejin Peng
Shaohai Wen
Guang Wang
Xu Zhang
Teng Di
Guangzu Du
Bin Chen
Limin Zhang
author_sort Yuejin Peng
collection DOAJ
description <i>Spodoptera frugiperda</i> (Lepidoptera: Noctuidae) is a migratory agricultural pest that is devastating on a global scale. <i>Beauveria bassiana</i> 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. <i>B. bassiana</i> AJS91881 was isolated and identified from the infected larvae of <i>Spodoptera litura</i>. The virulence of AJS91881 to the eggs, larvae, pupae and adults of <i>S. frugiperda</i> was measured. Moreover, the gut microbial community diversity of healthy and fungus-infected insects was analyzed. Our results showed that after treatment with <i>B. bassiana</i> 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 <i>B. bassiana</i> infection. At the phylum and genus level, the relative abundance of the Proteobacteria and <i>Serratia</i> increased significantly in the <i>B. bassiana</i> 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. <i>Serratia marcescens</i> was the bacterium with the highest relative abundance after infection by <i>B. bassiana</i>; intestinal bacteria <i>S. marcescens</i> inhibited the infection of insect fungi <i>B. bassiana</i> against the <i>S. frugiperda</i>. 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 <i>B. bassiana</i> against <i>S</i>. <i>frugiperda</i>. Most importantly, in the later stage of fungal infection, the increased abundance of <i>S. marcescens</i> in the insect intestine inhibited the virulence of <i>B. bassiana</i> 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 doaj.art-ad310f08385f428090d76bc7430604732023-11-19T11:28:56ZengMDPI AGJournal of Fungi2309-608X2023-09-019990610.3390/jof9090906Reconstruction of Gut Bacteria in <i>Spodoptera frugiperda</i> Infected by <i>Beauveria bassiana</i> Affects the Survival of Host PestYuejin Peng0Shaohai Wen1Guang Wang2Xu Zhang3Teng Di4Guangzu Du5Bin Chen6Limin Zhang7Yunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaYunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaYunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaYunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaYunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaYunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaYunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, ChinaYunnan State Key Laboratory of Conservation and Utilization of Biological Resources, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, China<i>Spodoptera frugiperda</i> (Lepidoptera: Noctuidae) is a migratory agricultural pest that is devastating on a global scale. <i>Beauveria bassiana</i> 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. <i>B. bassiana</i> AJS91881 was isolated and identified from the infected larvae of <i>Spodoptera litura</i>. The virulence of AJS91881 to the eggs, larvae, pupae and adults of <i>S. frugiperda</i> was measured. Moreover, the gut microbial community diversity of healthy and fungus-infected insects was analyzed. Our results showed that after treatment with <i>B. bassiana</i> 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 <i>B. bassiana</i> infection. At the phylum and genus level, the relative abundance of the Proteobacteria and <i>Serratia</i> increased significantly in the <i>B. bassiana</i> 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. <i>Serratia marcescens</i> was the bacterium with the highest relative abundance after infection by <i>B. bassiana</i>; intestinal bacteria <i>S. marcescens</i> inhibited the infection of insect fungi <i>B. bassiana</i> against the <i>S. frugiperda</i>. 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 <i>B. bassiana</i> against <i>S</i>. <i>frugiperda</i>. Most importantly, in the later stage of fungal infection, the increased abundance of <i>S. marcescens</i> in the insect intestine inhibited the virulence of <i>B. bassiana</i> 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.https://www.mdpi.com/2309-608X/9/9/906<i>Beauveria bassiana</i><i>Spodoptera frugiperda</i>gut microbial diversityvirulence<i>Serratia marcescens</i>host defense
spellingShingle Yuejin Peng
Shaohai Wen
Guang Wang
Xu Zhang
Teng Di
Guangzu Du
Bin Chen
Limin Zhang
Reconstruction of Gut Bacteria in <i>Spodoptera frugiperda</i> Infected by <i>Beauveria bassiana</i> Affects the Survival of Host Pest
Journal of Fungi
<i>Beauveria bassiana</i>
<i>Spodoptera frugiperda</i>
gut microbial diversity
virulence
<i>Serratia marcescens</i>
host defense
title Reconstruction of Gut Bacteria in <i>Spodoptera frugiperda</i> Infected by <i>Beauveria bassiana</i> Affects the Survival of Host Pest
title_full Reconstruction of Gut Bacteria in <i>Spodoptera frugiperda</i> Infected by <i>Beauveria bassiana</i> Affects the Survival of Host Pest
title_fullStr Reconstruction of Gut Bacteria in <i>Spodoptera frugiperda</i> Infected by <i>Beauveria bassiana</i> Affects the Survival of Host Pest
title_full_unstemmed Reconstruction of Gut Bacteria in <i>Spodoptera frugiperda</i> Infected by <i>Beauveria bassiana</i> Affects the Survival of Host Pest
title_short Reconstruction of Gut Bacteria in <i>Spodoptera frugiperda</i> Infected by <i>Beauveria bassiana</i> Affects the Survival of Host Pest
title_sort reconstruction of gut bacteria in i spodoptera frugiperda i infected by i beauveria bassiana i affects the survival of host pest
topic <i>Beauveria bassiana</i>
<i>Spodoptera frugiperda</i>
gut microbial diversity
virulence
<i>Serratia marcescens</i>
host defense
url https://www.mdpi.com/2309-608X/9/9/906
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