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The larval gut of Spodoptera frugiperda harbours culturable bacteria with metabolic versatility after insecticide exposure

The larval gut of Spodoptera frugiperda harbours culturable bacteria with metabolic versatility after insecticide exposure
The larval gut of Spodoptera frugiperda harbours culturable bacteria with metabolic versatility after insecticide exposure

Spodoptera frugiperda (fall armyworm) poses a substantial risk to crops worldwide, resulting in considerable economic damage. The gut microbiota of insects plays crucial roles in digestion, nutrition, immunity, growth and, sometimes, the degradation of insecticides. The current study examines the effect of synthetic insecticides on the gut microbiome of third instar S. frugiperda larvae using both culture-dependent techniques and 16S rRNA gene sequencing for bacterial community profiling and diversity analysis. In untreated larvae, the sequencing approach revealed a diverse microbiome dominated by the phyla Firmicutes, Proteobacteria and Bacteroidota, with key genera including Bacteroides, Faecalibacterium and Pelomonas. In parallel, 323 bacterial strains were isolated and assigned to the orders Bacillales, Burkholderiales, Enterobacterales, Flavobacteriales, Lactobacillales, Micrococcales, Neisseriaies, Pseudomonadales, Sphingobacteriales and Xanthomonadales. The prevailing culturable species included Serratia marcescens, Klebsiella variicola and Enterobacter quasiroggenkampii. Treatment with sublethal concentrations of three insecticides (broflanilide, spinosad and indoxacarb) caused significant changes in gut microbiome diversity and composition. Treated larvae showed a shift towards increased Proteobacteria abundance and decreased Firmicutes. Specifically, Acinetobacter and Rhodococcus were dominant in treated samples. Functional predictions highlighted significant metabolic versatility involving nutrient processing, immune response, detoxification, xenobiotic metabolism, and stress response, suggesting microbial adaptation to insecticide exposure. Network correlation analysis highlighted disrupted microbial interactions and altered community structures under insecticide treatment. These findings enhance our understanding of how insecticides impact the gut microbiota in S. frugiperda and may inform future strategies for managing pest resistance through microbiome-based approaches.

bacterial communities, gut microbiome, insect microbiome, insecticide toxicity, microbial diversity, microbial interactions, pest management, synthetic insecticides
0962-1075
452-469
Siddiqui, Junaid Ali
f6ef14d5-3fe6-4fe1-9dda-a4828c223991
Fan, Ruidong
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Liu, Yanjiang
cb5ec9ab-272a-4781-b12e-0e26a6de3c6e
Syed, Ali Hassan
e096513e-17d7-4949-8dbb-b1d8d28447e4
Benlin, Yi
7d73a33c-4837-4766-bd67-63c255c2b88f
Chu, Qingshuai
a5b3c4cd-ec6c-431f-b9a4-875deb965367
Ding, Zeyang
8522fdf9-f362-45b9-96a0-bed0d53467be
Ghani, Muhammad Imran
e55fd3f1-9b8e-4e10-99c5-b7efbb9e6ab4
Liu, Xuemi
c48cc3d9-7386-4d62-9aa5-8f98c1bb3c43
Wakil, Waqas
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Liu, Dong‐Dong
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Chen, Xiaoyulong
02c0a0f6-0927-47d3-80ab-68b70e81c9fb
Cernava, Tomislav
a13d65aa-2529-479a-ba90-69ebbc4ba07f
Smagghe, Guy
dd96063a-ac19-45b2-8ed2-6b402cb22ce0
Siddiqui, Junaid Ali
f6ef14d5-3fe6-4fe1-9dda-a4828c223991
Fan, Ruidong
e9574784-4e25-485a-9792-4222dbdc1c9a
Liu, Yanjiang
cb5ec9ab-272a-4781-b12e-0e26a6de3c6e
Syed, Ali Hassan
e096513e-17d7-4949-8dbb-b1d8d28447e4
Benlin, Yi
7d73a33c-4837-4766-bd67-63c255c2b88f
Chu, Qingshuai
a5b3c4cd-ec6c-431f-b9a4-875deb965367
Ding, Zeyang
8522fdf9-f362-45b9-96a0-bed0d53467be
Ghani, Muhammad Imran
e55fd3f1-9b8e-4e10-99c5-b7efbb9e6ab4
Liu, Xuemi
c48cc3d9-7386-4d62-9aa5-8f98c1bb3c43
Wakil, Waqas
24eb4f3f-6f18-4afe-9952-ac8cd6960445
Liu, Dong‐Dong
bc68497e-fd45-4f0c-87c2-9c4176787406
Chen, Xiaoyulong
02c0a0f6-0927-47d3-80ab-68b70e81c9fb
Cernava, Tomislav
a13d65aa-2529-479a-ba90-69ebbc4ba07f
Smagghe, Guy
dd96063a-ac19-45b2-8ed2-6b402cb22ce0

Siddiqui, Junaid Ali, Fan, Ruidong, Liu, Yanjiang, Syed, Ali Hassan, Benlin, Yi, Chu, Qingshuai, Ding, Zeyang, Ghani, Muhammad Imran, Liu, Xuemi, Wakil, Waqas, Liu, Dong‐Dong, Chen, Xiaoyulong, Cernava, Tomislav and Smagghe, Guy (2025) The larval gut of Spodoptera frugiperda harbours culturable bacteria with metabolic versatility after insecticide exposure. Journal of Insect Molecular Biology, 34 (3), 452-469. (doi:10.1111/imb.12983).

Record type: Article

Abstract

Spodoptera frugiperda (fall armyworm) poses a substantial risk to crops worldwide, resulting in considerable economic damage. The gut microbiota of insects plays crucial roles in digestion, nutrition, immunity, growth and, sometimes, the degradation of insecticides. The current study examines the effect of synthetic insecticides on the gut microbiome of third instar S. frugiperda larvae using both culture-dependent techniques and 16S rRNA gene sequencing for bacterial community profiling and diversity analysis. In untreated larvae, the sequencing approach revealed a diverse microbiome dominated by the phyla Firmicutes, Proteobacteria and Bacteroidota, with key genera including Bacteroides, Faecalibacterium and Pelomonas. In parallel, 323 bacterial strains were isolated and assigned to the orders Bacillales, Burkholderiales, Enterobacterales, Flavobacteriales, Lactobacillales, Micrococcales, Neisseriaies, Pseudomonadales, Sphingobacteriales and Xanthomonadales. The prevailing culturable species included Serratia marcescens, Klebsiella variicola and Enterobacter quasiroggenkampii. Treatment with sublethal concentrations of three insecticides (broflanilide, spinosad and indoxacarb) caused significant changes in gut microbiome diversity and composition. Treated larvae showed a shift towards increased Proteobacteria abundance and decreased Firmicutes. Specifically, Acinetobacter and Rhodococcus were dominant in treated samples. Functional predictions highlighted significant metabolic versatility involving nutrient processing, immune response, detoxification, xenobiotic metabolism, and stress response, suggesting microbial adaptation to insecticide exposure. Network correlation analysis highlighted disrupted microbial interactions and altered community structures under insecticide treatment. These findings enhance our understanding of how insecticides impact the gut microbiota in S. frugiperda and may inform future strategies for managing pest resistance through microbiome-based approaches.

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More information

Accepted/In Press date: 2 January 2025
e-pub ahead of print date: 14 February 2025
Published date: June 2025
Keywords: bacterial communities, gut microbiome, insect microbiome, insecticide toxicity, microbial diversity, microbial interactions, pest management, synthetic insecticides

Identifiers

Local EPrints ID: 499714
URI: http://eprints.soton.ac.uk/id/eprint/499714
ISSN: 0962-1075
PURE UUID: b82b39b2-dd5e-4900-b12c-fb1922284c1c
ORCID for Tomislav Cernava: ORCID iD orcid.org/0000-0001-7772-4080

Catalogue record

Date deposited: 01 Apr 2025 16:39
Last modified: 19 Aug 2025 02:08

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Contributors

Author: Junaid Ali Siddiqui
Author: Ruidong Fan
Author: Yanjiang Liu
Author: Ali Hassan Syed
Author: Yi Benlin
Author: Qingshuai Chu
Author: Zeyang Ding
Author: Muhammad Imran Ghani
Author: Xuemi Liu
Author: Waqas Wakil
Author: Dong‐Dong Liu
Author: Xiaoyulong Chen
Author: Tomislav Cernava ORCID iD
Author: Guy Smagghe

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