Immune-mediated competition benefits protective microbes over pathogens in a novel host species

Microbes that protect against infection inhabit hosts across the tree of life. It is unclear whether and how the host immune system may affect the formation of new protective symbioses. We investigated the transcriptomic response of Caenorhabditis elegans following novel interactions with a protective microbe (Enterococcus faecalis) able to defend against infection by pathogenic Staphylococcus aureus. We have previously shown that E. faecalis can directly limit pathogen growth within hosts. In this study, we show that colonisation by protective E. faecalis caused the differential expression of 1,557 genes in pathogen infected hosts, including the upregulation of immune genes such as lysozymes and C-type lectins. The most significantly upregulated host lysozyme gene, lys-7, impacted the competitive abilities of E. faecalis and S. aureus when knocked out. E. faecalis has an increased ability to resist lysozyme activity compared to S. aureus, suggesting that the protective microbe could gain a competitive advantage from this host response. Our finding that protective microbes can benefit from immune-mediated competition after introduction opens up new possibilities for biocontrol design and our understanding of symbiosis evolution. Crosstalk between the host immune response and microbe-mediated protection should favour the continued investment in host immunity and avoid the potentially risky evolution of host dependence.

Automated summary

This study investigates the impact of interactions between the host Caenorhabditis elegans and the protective microbe Enterococcus faecalis on the host immune system. The results show that colonization by E. faecalis causes differential expression of 1,557 genes in pathogen-infected hosts, including the upregulation of immune genes such as lysozymes and C-type lectins. The upregulation of lysozyme gene lys-7 affects the competitive abilities of E. faecalis and Staphylococcus aureus, with E. faecalis having increased resistance to lysozyme activity. This suggests that protective microbes can benefit from host immune-mediated competition.