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Abstract Increasing ocean temperatures are causing dysbiosis between coral hosts and their symbionts. Previous work suggests that coral host gene expression responds more strongly to environmental stress compared to their intracellular symbionts; however, the causes and consequences of this phenomenon remain untested. We hypothesized that symbionts are less responsive because hosts modulate symbiont environments to buffer stress. To test this hypothesis, we leveraged the facultative symbiosis between the scleractinian coralOculina arbusculaand its symbiontBreviolum psygmophilumto characterize gene expression responses of both symbiotic partners in and ex hospite under thermal challenges. To characterize host and in hospite symbiont responses, symbiotic and aposymbioticO. arbusculawere exposed to three treatments: (1) control (18°C), (2) heat (32°C), and (3) cold (6°C). This experiment was replicated withB. psygmophilumcultured fromO. arbusculato characterize ex hospite symbiont responses. Both thermal challenges elicited classic environmental stress responses (ESRs) inO. arbuscularegardless of symbiotic state, with hosts responding more strongly to cold challenge. Hosts also exhibited stronger responses than in hospite symbionts. In and ex hospiteB. psygmophilumboth down‐regulated gene ontology pathways associated with photosynthesis under thermal challenge; however, ex hospite symbionts exhibited greater gene expression plasticity and differential expression of genes associated with ESRs. Taken together, these findings suggest thatO. arbusculahosts may buffer environments ofB. psygmophilumsymbionts; however, we outline the future work needed to confirm this hypothesis.
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Symbiont Gene Expression Predicts Insect Host's Response to High Temperatures
ABSTRACT 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‐Caballeroniamodel 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.
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- Award ID(s):
- 2146512
- PAR ID:
- 10662999
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 34
- Issue:
- 22
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/mec.70154
