Bacteria commonly interact with aphids in intimate symbioses, where symbionts increase host fitness (for a review see Russell and Moran, 2006). Interestingly, several evidences suggested that symbiotic bacteria present in the insect gut are involved not only in the degradation of specific substances in the food (Russell and Moran, 2006), but also in other complex interactions protecting the host from invasion by pathogenic microorganisms (a process known as “colonization resistance”) and modulating the insect immune system. Microbiome seems therefore to act in aphids (and actually not only in insects) as a sort of ecological immunity or extended immune system being able of affecting the efficiency of the host immune system and limiting the accumulation of pathobionts. As evident in the photo from a Nancy Moran paper, aphid bacteriocytes possess several symbiotic bacteria including the larger Buchnera primary symbionts (arrowheads) and the smaller H. defensa secondary symbionts (arrows).
In a recent paper, Chiu et al. (2012) reported a low survival of nymphs of the aphid Myzus varians at high temperatures as a consequence of the elimination of endosymbionts, such as Buchnera. This effect probably results from a temperature-mediated decrease in aphid endosymbionts, which synthesize amino acids essential for their insect hosts. In the last years, different roles have been suggested for symbionts other than the synthesis of amino acids only (Russell and Moran, 2006). Buchnera might, for instance, play a key role in aphid thermal tolerance since endosymbionts code for heat shock proteins, which deter degradation of host protein secondary structure (Dunbar et al., 2007). Secondary endosymbionts, such as Serratia simbiotica, play a similar role in the thermal tolerance of their host strengthening the ability of aphids to evolve further adaptations to overcome the impacts of warming (Russell and Moran, 2006).
Buchnera are at least partly able to survive at high temperatures because of constitutive expression of genes that are normally up-regulated in response to heat and aphids could be able to thrive under temperatures as high as 35°C in the laboratory (Dunbar et al., 2007). Surprisingly, a single nucleotide deletion in the Buchnera ibpA gene encoding for a small heat-shock protein virtually eliminates the transcriptional response of ibpA to heat stress and lowers its expression even at cool or moderate temperatures (Dunbar et al., 2007). In the present of this mutant allele, a short heat exposure in juveniles has strong effects on aphids that produce few or no progeny and contain almost no Buchnera, in contrast to aphids bearing symbionts without the deletion.
The ibpA mutated allele has appreciable frequencies in field populations supporting the view that lowering of ibpA expression improves host fitness under some conditions (Dunbar et al., 2007). As previously suggested, the response to stress (including thermal stress) is part of a large trade-off that related stress response to reproduction and immunity. This mutation by switching off the response to heat stimuli could favor aphid reproduction and immunity. However, the prolonged permanence of aphids at high temperatures (for instance in hot summer with daily mean temperature of 32.5 °C) results in the elimination of Buchnera reducing not only the thermal tolerance of aphids, but also their fecundity since the lack of endosymbionts results in a lost synthesis of amino acids essential for the hosts (Chiu et al., 2012).
According to these results, global warming could be difficultly faced by aphids in tropical regions due to Buchnera symbiont depletion. Interestingly, in the presence of low density of primary symbionts, secondary symbionts (such as Hamiltonella defensa, Serratia symbiotica, Regiella insecticola) could be more present affecting not only the aphid thermal tolerance to high temperatures clearly suggesting, but also their immune response due to symbionts (Poirié and Coustau, 2011).
The effects of global warming on the composition of aphid microbiota are of particular interest since, as recently reviewed by Poirié and Coustau (2011), the immune deficiency (IMD) signalling pathway was apparently non functional in aphids and no genes coding for peptidoglycan recognition proteins (PGRPs) and several well-conserved antimicrobial peptides, such as defensins and cecropins, have been predicted in the pea aphid Acyrthosiphon pisum genome (Gerardo et al., 2010), making the microbiota-based immunity essential to protect the host against natural enemies (Poirié and Coustau, 2011).
Even if effective, the symbiont-associated immunity appears to be more ephemeral and less stable than genetic resistance (Poirié and Coustau, 2011). Indeed, the rate of vertical transmission of symbionts is not always 100 %, so that bacteria can be lost, and their presence seems to be more energetically costly (Poirié and Coustau, 2011).
References
Chiu, M., Chen, Y., & Kuo, M. (2012). The effect of experimental warming on a low-latitude aphid, Myzus varians Entomologia Experimentalis et Applicata, 142 (3), 216-222 DOI: 10.1111/j.1570-7458.2011.01213.x
Dunbar, H.E., Wilson, A.C., Ferguson, N.R. & Moran, N.A. (2007). Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS biology, 5 (5) PMID: 17425405
Poirié, M. & Coustau, C. (2011). The evolutionary ecology of aphids’ immunity. Inv. Surv. J., 8, 247-255
Russell, J.A & Moran, N.A. (2006). Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings. Biological sciences / The Royal Society, 273 (1586), 603-10 PMID: 16537132
