Synergistic interaction of gut microbiota enhances the growth of nematode through neuroendocrine signaling

Animals are associated with a diverse bacterial community that impacts host physiology. It is well known that nutrients and enzymes synthesized by bacteria largely expand host metabolic capacity. Bacteria also impact a wide range of animal physiology that solely depends on host genetics through direct interaction. However, studying the synergistic effects of the bacterial community remains challenging due to its complexity. The omnivorous nematode Pristionchus pacificus has limited digestive efficiency on bacteria. Therefore, we established a bacterial collection that represents the natural gut microbiota that are resistant to digestion. Using this collection, we show that the bacterium Lysinibacillus xylanilyticus by itself provides limited nutritional value, but in combination with Escherichia coli, it significantly promotes life-history traits of P. pacificus by regulating the neuroendocrine peptide in sensory neurons. This gut-to-brain communication depends on undigested L. xylanilyticus providing Pristionchus nematodes a specific fitness advantage to compete with nematodes that rupture bacteria efficiently. Using RNA-seq and CRISPR-induced mutants, we show that 1-h exposure to L. xylanilyticus is sufficient to stimulate the expression of daf-7-type TGF-β signaling ligands, which induce a global transcriptome change. In addition, several effects of L. xylanilyticus depend on TGF-β signaling, including olfaction, body size regulation, and a switch of energy allocation from lipid storage to reproduction. Our results reveal the beneficial effects of a gut bacterium to modify life-history traits and maximize nematode survival in natural habitats. [Display omitted] •The bacterium L. xylanilyticus promotes fitness of its nematode host P. pacificus•L. xylanilyticus induces a global transcriptome change in P. pacificus•The host phenotypic changes are regulated by the DAF-7 TGF-β signaling pathway Lo et al. find a synergistic interaction between the nematode P. pacificus and a member of its gut microbiota. They show that the combination of E. coli and a member of nematodes’ natural microbiota L. xylanilyticus increase the fitness of P. pacificus via induction of the neuroendocrine peptide of P. pacificus.