AUTHOR=Lefoulon Emilie , McMullen John G. , Stock S. Patricia 

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

JOURNAL=Frontiers in Physiology

VOLUME=13

YEAR=2022

URL=https://www.frontiersin.org/journals/physiology/articles/10.3389/fphys.2022.821845

DOI=10.3389/fphys.2022.821845

ISSN=1664-042X

ABSTRACT=<p>Entomopathogenic nematodes of the genus <italic>Steinernema</italic> have a mutualistic relationship with bacteria of the genus <italic>Xenorhabdus</italic> 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. <italic>Xenorhabdus</italic> 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 <italic>Steinernema</italic> IJs are relative to the maintenance and vectoring of <italic>Xenorhabdus</italic>. In this study, we performed a comparative dual RNA-seq analysis of IJs of two nematode-bacteria partnerships: <italic>Steinernema carpocapsae</italic>-<italic>Xenorhabdus nematophila</italic> and <italic>Steinernema. puntauvense</italic>-<italic>Xenorhbdus bovienii</italic>. For each association, three conditions were studied: (1) IJs reared in the insect (<italic>in vivo</italic> colonized), (2) colonized IJs reared on liver-kidney agar (<italic>in vitro</italic> colonized), and (3) IJs depleted by the bacteria reared on liver-kidney agar (<italic>in vitro</italic> 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 <italic>in vitro</italic>, 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 <italic>Steinernema</italic> species were depleted of their symbiotic partners. These results suggest <italic>Steinernema</italic> IJs may have a mechanism to adapt their virulence in absence of their symbionts.</p>