Abstract
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.
Highlights
Long term associations between organisms are largely widespread in nature
Recent studies have shown that Steinernema infective juvenile (IJ) release venom proteins that are lethal to several insects including Drosophila melanogaster (Lu et al, 2017)
Transcriptomic analyses of the Xenorhabdus are not showed in the current study due to the low number of sequenced reads belonging to the endosymbiont
Summary
Long term associations between organisms are largely widespread in nature. Among these, mutualistic symbiosis is characterized by reciprocal fitness advantages that often play a role in the function and development of both the hosts and the symbionts (Russell et al, 2014; Stoy et al, 2020). The level of specialization of Steinernema nematodes with their native and non-native Xenorhabdus symbionts have been investigated (Sicard et al, 2004, 2005;Murfin et al, 2015 ; McMullen et al, 2017) Results from these studies revealed that nematode fitness declines with the increase of the phylogenetic distance between the native and tested non-cognate bacteria suggesting that specificity of the association may impact the virulence and the longevity of the nematodes (Murfin et al, 2015; McMullen et al, 2017). Co-phylogenetic studies have revealed no universal co-evolution pattern between Steinernema-Xenorhabdus and suggested horizontal transfer of symbionts (Lee and Stock, 2010) These associations appear to have evolved from different acquisition events and may represent different stages of a host-dependent adaptation (Sicard et al, 2005). When the IJ stages emerge from the insect host, they are associated with their Xenorhabdus symbiont, so in order to study aposymbiotic IJ stages nematodes are obtained from in vitro reared eggs which aresymbiont-free (McMullen and Patricia Stock, 2014)
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