Mutualism meltdown in insects: bacteria constrain thermal adaptation

Abstract

Predicting whether and how organisms will successfully cope with climate change presents critical questions for biologists and environmental scientists. Models require knowing how organisms interact with their abiotic environment, as well understanding biotic interactions that include a network of symbioses in which all species are embedded. Bacterial symbionts of insects offer valuable models to examine how microbes can facilitate and constrain adaptation to a changing environment. While some symbionts confer plasticity that accelerates adaptation, long-term bacterial mutualists of insects are characterized by tight lifestyle constraints, genome deterioration, and vulnerability to thermal stress. These essential bacterial partners are eliminated at high temperatures, analogous to the loss of zooanthellae during coral bleaching. Recent field-based studies suggest that thermal sensitivity of bacterial mutualists constrains insect responses. In this sense, highly dependent mutualisms may be the Achilles' heel of thermal responses in insects.

Figure 1. Examples of conditions under which obligate mutualists are eliminated from insects

Examples shown are detailed in the text.

Figure 2. Potential mechanisms underlying heat-susceptibility of obligate mutualists

Heat sensitivity may be rooted in the distinct features of these reduced bacterial genomes. Clockwise: Despite high expression of GroEL, degraded proteins may have unstable structures and be susceptible to destabilization by heat stress. Moreover, thermolabile structural RNAs [23] could contribute to heat sensitivity. In addition, the typically extreme AT-rich DNA of mutualists (though fascinating exceptions exist [18]) could be unstable under high temperatures, due to the lower thermostability of AT pairs or destabilizing effects of AT pairs on DNA stacking [39]. The loss of membrane proteins may reduce the stability of endosymbiont cells. In addition to these features, it is also possible that heat susceptibility of endosymbionts involves disruption of host functions that are involved in symbiont maintenance.