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Entomopathogenic nematodes of the genus  Steinernema  have a mutualistic relationship with bacteria of the genus  Xenorhabdus  and together they form an antagonist partnership against their insect hosts. The nematodes (third-stage infective juveniles, or IJs) protect the bacteria from the external environmental stressors and vector them from one insect host to another.  Xenorhabdus  produce secondary metabolites and antimicrobial compounds inside the insect that protect the cadaver from soil saprobes and scavengers. The bacteria also become the nematodes’ food, allowing them to grow and reproduce. Despite these benefits, it is yet unclear what the potential metabolic costs for  Steinernema  IJs are relative to the maintenance and vectoring of  Xenorhabdus . In this study, we performed a comparative dual RNA-seq analysis of IJs of two nematode-bacteria partnerships:  Steinernema carpocapsae - Xenorhabdus nematophila  and  Steinernema. puntauvense - Xenorhbdus bovienii . For each association, three conditions were studied: (1) IJs reared in the insect ( in vivo  colonized), (2) colonized IJs reared on liver-kidney agar ( in vitro  colonized), and (3) IJs depleted by the bacteria reared on liver-kidney agar ( in vitro  aposymbiotic). Our study revealed the downregulation of numerous genes involved in metabolism pathways, such as carbohydrate, amino acid, and lipid metabolism when IJs were reared  in vitro , both colonized and without the symbiont. This downregulation appears to impact the longevity pathway, with the involvement of glycogen and trehalose metabolism, as well as arginine metabolism. Additionally, a differential expression of the venom protein known to be secreted by the nematodes was observed when both  Steinernema  species were depleted of their symbiotic partners. These results suggest  Steinernema  IJs may have a mechanism to adapt their virulence in absence of their symbionts.

Transcriptomic Analysis of Steinernema Nematodes Highlights Metabolic Costs Associated to Xenorhabdus Endosymbiont Association and Rearing Conditions