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Thermal Tolerance in Green Hydra: Identifying the Roles of Algal Endosymbionts and Hosts in a Freshwater Holobiont Under Stress

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Abstract

It has been proposed that holobionts (host-symbiont units) could swap endosymbionts, rapidly alter the hologenome (host plus symbiont genome), and increase their stress tolerance. However, experimental tests of individual and combined contributions of hosts and endosymbionts to holobiont stress tolerance are needed to test this hypothesis. Here, we used six green hydra (Hydra viridissima) strains to tease apart host (hydra) and symbiont (algae) contributions to thermal tolerance. Heat shock experiments with (1) hydra with their original symbionts, (2) aposymbiotic hydra (algae removed), (3) novel associations (a single hydra strain hosting different algae individually), and (4) control hydra (aposymbiotic hydra re-associated with their original algae) showed high variation in thermal tolerance in each group. Relative tolerances of strains were the same within original, aposymbiotic, and control treatments, but reversed in the novel associations group. Aposymbiotic hydra had similar or higher thermal tolerance than hydra with algal symbionts. Selection on the holobiont appears to be stronger than on either partner alone, suggesting endosymbiosis could become an evolutionary trap under climate change. Our results suggest that green hydra thermal tolerance is strongly determined by the host, with a smaller, non-positive role for the algal symbiont. Once temperatures exceed host tolerance limits, swapping symbionts is unlikely to allow these holobionts to persist. Rather, increases in host tolerance through in situ adaptation or migration of pre-adapted host strains appear more likely to increase local thermal tolerance. Overall, our results indicate green hydra is a valuable system for studying aquatic endosymbiosis under changing environmental conditions, and demonstrate how the host and the endosymbiont contribute to holobiont stress tolerance.

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Acknowledgments

We thank Hiroshi Shimizu, Daniel Martinez, and David Dunigan for providing study materials. We thank Daniel Wagner and Thomas Clements for their assistance with micro-injections. We also thank Rudy Guerra for his statistical advice. This work was supported by Theodore Roosevelt Memorial Fund provided by American Museum of Natural History.

Funding

This study was funded by the Theodore Roosevelt Memorial Fund provided by American Museum of Natural History.

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  1. Department of Biosciences, Rice University, 6100 S. Main St., Houston, TX, 77005, USA

    Siao Ye, Meenakshi Bhattacharjee & Evan Siemann

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  1. Siao Ye
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Correspondence to Siao Ye.

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Ye, S., Bhattacharjee, M. & Siemann, E. Thermal Tolerance in Green Hydra: Identifying the Roles of Algal Endosymbionts and Hosts in a Freshwater Holobiont Under Stress. Microb Ecol 77, 537–545 (2019). https://doi.org/10.1007/s00248-018-01315-1

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