How do insects react to novel inherited symbionts? A microarray analysis of Drosophila melanogaster response to the presence of natural and introduced Spiroplasma

Abstract

Maternally inherited endosymbionts are found in numerous insect species and have various effects on host ecology. New symbioses are most commonly established following lateral transfer of an existing symbiont from one host species to another. Laboratory study has demonstrated that symbionts commonly perform poorly in novel hosts, with weak vertical transmission and maladaptive pathogenicity being observed in the generations following transfer. This poor performance probably limits symbiont occurrence. We here use microarray technology to test whether poor symbiont performance observed following 1 year of vertical transmission through a new host is associated with alteration in host gene expression or whether it occurs independently of this. We utilize the Drosophila melanogaster--Spiroplasma interaction and test the response of the host in the presence of both natural Spiroplasma infections and novel Spiroplasma infections transinfected previously from other host species. None of the Spiroplasma infections investigated produced upregulation in host haemolymph/fat body-based immune responses, and we therefore rejected the hypothesis that failure to thrive was associated with immune upregulation. One infection was associated with a downregulation of genes associated with egg production compared to uninfected controls, indicative of damage to the host. The Spiroplasma infection showed that the weakest vertical transmission showed no significant disturbance to host gene expression compared to uninfected controls. We conclude that the failure of Spiroplasma in novel host species is associated either with causing harm to their new hosts or through a failure to thrive in the new host that occurs independently of host responses to infection.

Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

“…It is also worth noting that a recent microarray study of D . melanogaster harboring different strains of Spiroplasma revealed that these had the capacity to perturb the expression of host yolk genes (40). This suggests that that the interaction between Spiroplasma and yolk might be multifaceted, but the implications of these gene expression changes for Spiroplasma transmission are not clear.…”

Host Defense via Symbiosis in Drosophila

“…Spiroplasma typically occur extracellularly in the host hemolymph while Wolbachia are predominately intracellular, and Spiroplasma cause little apparent immune activation in their hosts [30],[31]. Spiroplasma may be more susceptible to immune effectors active in the host hemolymph due to their extracellular lifestyle, and thus under selection to avoid or even suppress host immune activation (e.g., [30]). Mechanisms other than host immune priming might therefore account for Spiroplasma -mediated defense.…”

Correlation and causation between the microbiome, Wolbachia and host functional traits in natural populations of drosophilid flies

“…The literature on possible mechanisms is fragmentary and contradictory. Spiroplasma in D. melanogaster is known to evade systemic immune attack (Hurst, Anbutsu, Kutsukake, & Fukatsu, ; Hutchence, Fischer, Paterson, & Hurst, ) and to compete with the host for key nutrients, specifically lipids (Herren et al, ), raising the possibility that Wolbachia in D. neotestacea may promote Spiroplasma populations by attenuating the systemic immune system or enhancing lipid availability in the haemolymph. However, these inferences fit poorly with other data sets that point to Wolbachia ‐mediated promotion of host immune responsiveness (Gupta et al, ) and depletion of nutrients, notably sterols (Caragata et al, ) which are required by Spiroplasma .…”