Behavioural phase transitions in the migratory locust, Locusta migratoria, are related to changes in the gut...

Locusta migratoria is a grasshopper species that can change its behaviour from solitary to gregarious. Previous studies have implicated metabolites such as serotonin and dopamine in the regulation of behavioural transition in this species. While many studies using cultured microbes have demonstrated that some microbes harbor the neuroactive metabolic potential of these neurotransmitters, the association between microbial community composition and phase transition remains poorly understood. Here, we employed 16S rRNA gene amplicon sequencing and shotgun metagenomic sequencing analyses to compare the composition of gut microbial communities of L. migratoria in different behavioural phases. We found that Serratia ureilytica was enriched in the gut of gregarious individuals in contrast to the decreased presence of Klebsiella aerogenes, one of the most abundant taxa in wild individuals. The gut microbiome of gregarious individuals was functionally characterised by enriched kynurenine and tryptophan synthesis pathways, and by reduced representation of GABA, indole, and dopamine metabolism pathways compared with that of solitary individuals. These compositional changes were consistent with the enrichment of S. ureilytica and depletion of K. aerogenes, which possess the corresponding genes. In particular, the genes for kynurenine synthesis encoded by S. ureilytica specific to the gregarious phase, are known to be involved in the tryptophan production and are associated with reduced serotonin synthesis. These results highlight a distinct shift in both the taxonomic and functional composition of the gut microbiome across behavioural phases and suggest a potential microbial contribution to the behavioural changes of L. migratoria.