Increase in midgut microbiota load induces an apparent immune priming and increases tolerance to Bacillus thuringiensis

Abstract

The insect immune system is comprised of both humoral and cellular components that are mobilized in response to parasitic or pathogenic infections. Activation of the immune response implies a considerable expenditure of energy and that is why insects rely on inducible pathways that are activated after coming into contact with the pathogenic agent. Known as immune priming, insects can prolong the activation of the immune response and transmit their immune status to the next generation. Starting from a laboratory colony of the lepidopteran Spodoptera exigua and using the lytic zone assay as a measure of the immune status, we selected for a sub-colony with high levels of immune activity in the absence of external challenging with bacteria. Immune-activated insect showed characteristics that are typical reported for immune primed insects, such as increased tolerance to pathogens (Bacillus thuringiensis in our case), fitness-cost associated to the immune status, and maternal transmission of the immune status. However, additional analysis revealed that the selection for the immune-activated insects was based on the selection of insects carrying a higher bacterial load in the midgut. Our results suggest that activation of the immune system in S. exigua may not only occur as consequence of the immune priming but also from an increase in midgut microbiota load.

Midgut microbiota and host immunocompetence underlieBacillus thuringiensiskilling mechanism

“…A selective passage through the midgut epithelium could be a possible way to allow a controlled transfer of bacteria to reproductive tissues and eggs. In this way, the egg and newly hatched larvae could receive an early supply of the important microbial complement, which indeed seems to be already present in the eggs of Lepidoptera (51). This reasonable speculation is indirectly supported by a recent study reporting the transit of ingested bacteria into the hemolymph and their accumulation in the ovary (52).…”

The transcriptome of Spodoptera exigua larvae exposed to different types of microbes

“…The ALM colony was originally derived from insects collected in the south of Spain (Hernandez-Martinez et al, 2010a). The FRA colony was kindly provided by M. López-Ferber, INRA (St Christol les Alés, France) (Hernandez-Martinez et al, 2008).…”

“…The doses or concentrations employed for the non-viral microorganisms were previously tested for their ability to activate the immune response in a lytic zone assay as previously described (Hernandez-Martinez et al, 2010a). Synchronized last instar larvae were injected intrahemocelically with 10 ml Phenol red solution (10% in PBS) containing 10 mg/ml of lyophilized Escherichia coli, Micrococcus luteus, or Saccharomyces cerevisiae.…”

Host and symbiont jointly control gut microbiota during complete metamorphosis

“…The gut microbiota of Lepidoptera is limited to a handful of bacterial species that varies with habitat and diet but often is dominated by enterococci that persist through metamorphosis [12]. In the lepidopteran gut, enterococci interact with pathogens through (i) competitive exclusion (ii) attenuation by direct antagonism or (iii) eliciting protective host immune responses and provide lepidopterans including Galleria mellonella with protection against one of the most virulent entomopathogens, Bacillus thuringiensis [21,[27][28][29] (reviewed in [30]). …”

“…Here we exploit an ancient [19], facultative and prevalent [20][21][22][23][24][25][26] symbiosis between Lepidoptera and enterococci to reconcile these approaches by studying the role of host immunity and bacterial competition during metamorphosis within a single system. The gut microbiota of Lepidoptera is limited to a handful of bacterial species that varies with habitat and diet but often is dominated by enterococci that persist through metamorphosis [12].…”