Symbiont Gene Expression Predicts Insect Host's Response to High Temperatures

Microbial symbionts play crucial roles in host nutrition, defence, and detoxification. However, host-symbiont interactions are context-dependent, and environmental stressors can disrupt these benefits. Diverse hosts, including corals, insects and leguminous plants, have been shown to suffer under thermal stress due to the negative impact of high temperatures on their symbionts. This failure is often linked to a symbiont's poor transcriptional regulation of heat shock genes, causing vulnerability at high temperatures. In the bug-Caballeronia model system, insect performance at elevated temperatures varies based on the hosted symbiont species. Here, we explore the underlying mechanisms that drive this variation using comparative metatranscriptomics and two symbionts with contrasting host outcomes at high temperatures. We evaluated both host and symbiont transcriptional responses to elevated temperature, testing the hypothesis that symbionts conferring improved host outcomes at high temperatures will have more upregulated heat shock genes under thermal stress compared to those conferring worse host outcomes. Our findings reveal that host transcription did not change with different symbionts but rather only at different temperatures. Furthermore, symbionts had distinct gene expression profiles across temperatures. At 36°C, the heat-resistant symbiont not only increased expression of heat shock genes but surprisingly upregulated flagellar genes, which are normally turned off during symbiosis. This suggests that symbiont, not host, transcription underlies host benefits at low versus high temperatures and ultimately furthers our understanding of context dependence in the outcomes of symbiotic associations.