Abstract
BackgroundThe holistic view of bacterial symbiosis, incorporating both host and microbial environment, constitutes a major conceptual shift in studies deciphering host-microbe interactions. Interactions between Steinernema entomopathogenic nematodes and their bacterial symbionts, Xenorhabdus, have long been considered monoxenic two partner associations responsible for the killing of the insects and therefore widely used in insect pest biocontrol. We investigated this “monoxenic paradigm” by profiling the microbiota of infective juveniles (IJs), the soil-dwelling form responsible for transmitting Steinernema-Xenorhabdus between insect hosts in the parasitic lifecycle.ResultsMultigenic metabarcoding (16S and rpoB markers) showed that the bacterial community associated with laboratory-reared IJs from Steinernema carpocapsae, S. feltiae, S. glaseri and S. weiseri species consisted of several Proteobacteria. The association with Xenorhabdus was never monoxenic. We showed that the laboratory-reared IJs of S. carpocapsae bore a bacterial community composed of the core symbiont (Xenorhabdus nematophila) together with a frequently associated microbiota (FAM) consisting of about a dozen of Proteobacteria (Pseudomonas, Stenotrophomonas, Alcaligenes, Achromobacter, Pseudochrobactrum, Ochrobactrum, Brevundimonas, Deftia, etc.). We validated this set of bacteria by metabarcoding analysis on freshly sampled IJs from natural conditions. We isolated diverse bacterial taxa, validating the profile of the Steinernema FAM. We explored the functions of the FAM members potentially involved in the parasitic lifecycle of Steinernema. Two species, Pseudomonas protegens and P. chlororaphis, displayed entomopathogenic properties suggestive of a role in Steinernema virulence and membership of the Steinernema pathobiome.ConclusionsOur study validates a shift from monoxenic paradigm to pathobiome view in the case of the Steinernema ecology. The microbial communities of low complexity associated with EPNs will permit future microbiota manipulation experiments to decipher overall microbiota functioning in the infectious process triggered by EPN in insects and, more generally, in EPN ecology.
Highlights
The holistic view of bacterial symbiosis, incorporating both host and microbial environment, constitutes a major conceptual shift in studies deciphering host-microbe interactions
A bacterial community is frequently associated with S. carpocapsae infective juveniles (IJs) Is there a core community associated with the laboratory-reared Steinernema species? We explored this question by focusing on S. carpocapsae species and comparing the community composition of IJs from six S. carpocapsae strains reared in the laboratory for several years (Additional file 1)
Likewise, when we compared the IJ microbiota of the American strains on reception at our laboratory (All_USDA_t0 and DD136 USDA_t0) and after just one round of multiplication in Galleria larvae in our laboratory (All_USDA_t1 and DD136 USDA_t1), we found that a quarter of the variance depended on batch (t0 versus t1 in Fig. 4c and Additional file 7) (Permanova V3V4, t0 versus t1, Df = 1, R2 = 0.27, p value = 10−4; Permanova rpoB, t0 versus t1, Df = 1, R2 = 0.24, p value = 2.10−4)
Summary
The holistic view of bacterial symbiosis, incorporating both host and microbial environment, constitutes a major conceptual shift in studies deciphering host-microbe interactions. Interactions between Steinernema entomopathogenic nematodes and their bacterial symbionts, Xenorhabdus, have long been considered monoxenic two partner associations responsible for the killing of the insects and widely used in insect pest biocontrol. We investigated this “monoxenic paradigm” by profiling the microbiota of infective juveniles (IJs), the soil-dwelling form responsible for transmitting Steinernema-Xenorhabdus between insect hosts in the parasitic lifecycle. Invertebrates rely on symbionts for many of their life history traits [8, 9] Their microbial communities can be analysed with methodologies that cannot be used on vertebrates. In the lepidopteran Spodoptera littoralis, the silencing of host immune pathways by RNAi revealed that Serratia and Clostridium species in the gut microbiota switched from asymptomatic symbionts to haemocoel pathogens during Bacillus thuringiensis infection [12]
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