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Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition

BACKGROUND: The entomopathogenic Beauveria bassiana is a popular fungus used to control the Japanese pine sawyer, Monochamus alternatus Hope, the key vector of pine wood nematode (Bursaphelenchus xylophilus) that is the causal agent of pine wilt disease, resulting in devastating losses of pines in C...

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Autores principales: Deng, Jundan, Xu, Weikang, Lv, Guochang, Yuan, Hang, Zhang, Qing-He, Wickham, Jacob D., Xu, Letian, Zhang, Longwa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9463743/
https://www.ncbi.nlm.nih.gov/pubmed/36085246
http://dx.doi.org/10.1186/s40793-022-00443-z
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author Deng, Jundan
Xu, Weikang
Lv, Guochang
Yuan, Hang
Zhang, Qing-He
Wickham, Jacob D.
Xu, Letian
Zhang, Longwa
author_facet Deng, Jundan
Xu, Weikang
Lv, Guochang
Yuan, Hang
Zhang, Qing-He
Wickham, Jacob D.
Xu, Letian
Zhang, Longwa
author_sort Deng, Jundan
collection PubMed
description BACKGROUND: The entomopathogenic Beauveria bassiana is a popular fungus used to control the Japanese pine sawyer, Monochamus alternatus Hope, the key vector of pine wood nematode (Bursaphelenchus xylophilus) that is the causal agent of pine wilt disease, resulting in devastating losses of pines in China and Portugal. However, recent studies have demonstrated that some insect-associated bacteria might decrease fungal toxicity and further undermine its biological control efficacy against M. alternatus. Thus, it is of great significance to uncover whether and how associated bacteria of M. alternatus become involved in the infection process of B. bassiana. RESULTS: Here, we show that axenic M. alternatus larvae died significantly faster than non-axenic larvae infected by four increasing concentrations of B. bassiana spores (Log-rank test, P < 0.001). The infection of B. bassiana significantly changed the richness and structure of the beetle-associated bacterial community both on the cuticle and in the guts of M. alternatus; meanwhile, the abundance of Pseudomonas and Serratia bacteria were significantly enriched as shown by qPCR. Furthermore, these two bacteria genera showed a strong inhibitory activity against B. bassiana (One-way ANOVA, P < 0.001) by reducing the fungal conidial germination and growth rather than regulating host immunity. CONCLUSIONS: This study highlights the role of insect-associated bacteria in the interaction between pest insects and entomopathogenic fungi, which should be taken into consideration when developing microbial-based pest control strategies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00443-z.
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spelling pubmed-94637432022-09-11 Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition Deng, Jundan Xu, Weikang Lv, Guochang Yuan, Hang Zhang, Qing-He Wickham, Jacob D. Xu, Letian Zhang, Longwa Environ Microbiome Research BACKGROUND: The entomopathogenic Beauveria bassiana is a popular fungus used to control the Japanese pine sawyer, Monochamus alternatus Hope, the key vector of pine wood nematode (Bursaphelenchus xylophilus) that is the causal agent of pine wilt disease, resulting in devastating losses of pines in China and Portugal. However, recent studies have demonstrated that some insect-associated bacteria might decrease fungal toxicity and further undermine its biological control efficacy against M. alternatus. Thus, it is of great significance to uncover whether and how associated bacteria of M. alternatus become involved in the infection process of B. bassiana. RESULTS: Here, we show that axenic M. alternatus larvae died significantly faster than non-axenic larvae infected by four increasing concentrations of B. bassiana spores (Log-rank test, P < 0.001). The infection of B. bassiana significantly changed the richness and structure of the beetle-associated bacterial community both on the cuticle and in the guts of M. alternatus; meanwhile, the abundance of Pseudomonas and Serratia bacteria were significantly enriched as shown by qPCR. Furthermore, these two bacteria genera showed a strong inhibitory activity against B. bassiana (One-way ANOVA, P < 0.001) by reducing the fungal conidial germination and growth rather than regulating host immunity. CONCLUSIONS: This study highlights the role of insect-associated bacteria in the interaction between pest insects and entomopathogenic fungi, which should be taken into consideration when developing microbial-based pest control strategies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00443-z. BioMed Central 2022-09-09 /pmc/articles/PMC9463743/ /pubmed/36085246 http://dx.doi.org/10.1186/s40793-022-00443-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Deng, Jundan
Xu, Weikang
Lv, Guochang
Yuan, Hang
Zhang, Qing-He
Wickham, Jacob D.
Xu, Letian
Zhang, Longwa
Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition
title Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition
title_full Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition
title_fullStr Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition
title_full_unstemmed Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition
title_short Associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition
title_sort associated bacteria of a pine sawyer beetle confer resistance to entomopathogenic fungi via fungal growth inhibition
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9463743/
https://www.ncbi.nlm.nih.gov/pubmed/36085246
http://dx.doi.org/10.1186/s40793-022-00443-z
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