ABSTRACT
Insects commonly harbor facultative bacterial endosymbionts, such as
Wolbachia
and
Spiroplasma
species, that are vertically transmitted from mothers to their offspring. These endosymbiontic bacteria increase their propagation by manipulating host reproduction or by protecting their hosts against natural enemies. While an increasing number of studies have reported endosymbiont-mediated protection, little is known about the mechanisms underlying this protection. Here, we analyze the mechanisms underlying protection from parasitoid wasps in
Drosophila melanogaster
mediated by its facultative endosymbiont
Spiroplasma poulsonii
. Our results indicate that
S. poulsonii
exerts protection against two distantly related wasp species,
Leptopilina boulardi
and
Asobara tabida
.
S. poulsonii
-mediated protection against parasitoid wasps takes place at the pupal stage and is not associated with an increased cellular immune response. In this work, we provide three important observations that support the notion that
S. poulsonii
bacteria and wasp larvae compete for host lipids and that this competition underlies symbiont-mediated protection. First, lipid quantification shows that both
S. poulsonii
and parasitoid wasps deplete
D. melanogaster
hemolymph lipids. Second, the depletion of hemolymphatic lipids using the
Lpp
RNA interference (
Lpp RNAi
) construct reduces wasp success in larvae that are not infected with
S. poulsonii
and blocks
S. poulsonii
growth. Third, we show that the growth of
S. poulsonii
bacteria is not affected by the presence of the wasps, indicating that when
S. poulsonii
is present, larval wasps will develop in a lipid-depleted environment. We propose that competition for host lipids may be relevant to endosymbiont-mediated protection in other systems and could explain the broad spectrum of protection provided.
IMPORTANCE
Virtually all insects, including crop pests and disease vectors, harbor facultative bacterial endosymbionts. They are vertically transmitted from mothers to their offspring, and some protect their host against pathogens. Here, we studied the mechanism of protection against parasitoid wasps mediated by the
Drosophila melanogaster
endosymbiont
Spiroplasma poulsonii
. Using genetic manipulation of the host, we provide strong evidence supporting the hypothesis that competition for host lipids underlies
S. poulsonii
-mediated protection against parasitoid wasps. We propose that lipid competition-based protection may not be restricted to
Spiroplasma
bacteria but could also apply other endosymbionts, notably
Wolbachia
bacteria, which can suppress human disease-causing viruses in insect hosts.