The nematode symbiotic bacterium Xenorhabdus griffiniae can sense and respond to the presence of its host Steinernema hermaphroditum

Abstract

The mutualistic symbiosis between Xenorhabdus bacteria and Steinernema nematodes has both ecological and practical importance. Their relationship co-evolved to make them dependent on each other in their life cycle where they kill, feed and reproduce within insect larvae together. This behavior has shed light on them as promising candidates to replace conventional pesticides. Despite the importance of the Xenorhabdus in insect-killing, the mechanisms by which the bacteria might sense and respond to the presence of their nematode host are not well understood. We performed an RNA-sequencing experiment on the bacterial partner, X. griffiniae, in close proximity, but not in direct contact with their host nematode, Steinernema hermaphroditum, to identify differentially regulated genes in these conditions, followed by genetic analysis to determine their functional significance. We show that X. griffiniae changes its transcriptomic profile in a small number of genes in the presence of axenic nematodes, but not in the presence of nematodes that are already colonized by X. griffiniae. We select the most differentially regulated gene, ymdA, for further investigation, and show that it plays a role in biofilm formation and affects host colonization efficiency. This work advances our understanding of bacterial sensing of nematodes and motivates future research in deepening our understanding of this underexplored ecological interaction. ImportanceInteractions between different organisms in the soil environment are enabled by the ability to sense and respond to organisms nearby. In many cases, the underlying sensing mechanisms that mediate these ecologically important interactions are not known. Filling in the knowledge gap of how these interactions occur can help us understand how microbial populations organize themselves, establish symbiotic relationships, or compete with other species in complex environments. Furthermore, elucidating these mechanisms may inform the development of new tools in agriculture, such as improved biological control agents. Here we use the bacterial symbiont Xenorhabdus griffiniae of the entomopathogenic nematode Steinernema hermaphroditum to study whether symbiotic bacteria of nematodes are able to sense their presence. Our results suggest that X. griffiniae can sense the presence of its nematode host and respond by modulating the gene expression level of several genes, where at least one, ymdA, has implications for host colonization.