Temperature transcends partner specificity in the symbiosis establishment of a cnidarian

Abstract

Coral reef research has predominantly focused on the effect of temperature on the breakdown of coral-dinoflagellate symbioses. However, less is known about how increasing temperature affects the establishment of new coral-dinoflagellate associations. Inter-partner specificity and environment-dependent colonization are two constraints proposed to limit the acquisition of more heat tolerant symbionts. Here, we investigated the symbiotic dynamics of various photosymbionts in different host genotypes under “optimal” and elevated temperature conditions. To do this, we inoculated symbiont-free polyps of the sea anemone Exaiptasia pallida originating from Hawaii (H2), North Carolina (CC7), and the Red Sea (RS) with the same mixture of native symbiont strains (Breviolum minutum, Symbiodinium linucheae, S. microadriaticum, and a Breviolum type from the Red Sea) at 25 and 32 °C, and assessed their ITS2 composition, colonization rates, and PSII photochemical efficiency (Fv/Fm). Symbiont communities across thermal conditions differed significantly for all hosts, suggesting that temperature rather than partner specificity had a stronger effect on symbiosis establishment. Overall, we detected higher abundances of more heat resistant Symbiodiniaceae types in the 32 °C treatments. Our data further showed that PSII photophysiology under elevated temperature improved with thermal pre-exposure (i.e., higher Fv/Fm), yet, this effect depended on host genotype and was influenced by active feeding as photochemical efficiency dropped in response to food deprivation. These findings highlight the role of temperature and partner fidelity in the establishment and performance of symbiosis and demonstrate the importance of heterotrophy for symbiotic cnidarians to endure and recover from stress.

Photophysiological Tolerance and Thermal Plasticity of Genetically Different Symbiodiniaceae Endosymbiont Species of Cnidaria

“…In the second temperature experiment, it became clear that Breviolum minutum SSB 01 was much more susceptible to enhanced temperatures starting at 30 • C. This demonstrates different temperature thresholds between strains of B. minutum, also within the genus Breviolum the species-specific tolerances differ. This is in line with another study, where closely related Breviolum species revealed significant functional variation against elevated temperature (Bayliss et al, 2019;Herrera et al, 2020). The different genotypes exhibited decreasing photosynthetic activity at elevated temperatures, which could be an important feature for the strength of the relationship between the symbiont and the host.…”

“…Furthermore, the NPP max of Symbiodinium linucheae SSA 01 was much lower in contrast to the other eight strains. This strain is also considered "heat tolerant" (Swain et al, 2017;LaJeunesse et al, 2018;Gegner et al, 2019) but might not be so beneficial for the coral host (Stat et al, 2008;Herrera et al, 2020). Although only minor photoinhibition was detected in the studied strains we cannot completely exclude an experimental effect as longer exposure to high irradiances could have resulted in a stronger photoinhibitory response.…”

“…Furthermore, S. linucheae (SSA 01) exhibited a lower photosynthetic rate, suggesting that this strain in symbiosis probably transfers less photosynthetically fixed organic carbon to the host (Stat et al, 2008). Therefore, future studies in which specific symbiont genotypes are introduced into the same host (e.g., Starzak et al, 2014;Hoadley et al, 2015;Herrera et al, 2020) are required to determine the role of host and symbiont in the response patterns. The different response patterns suggest that in symbiosis with a host, the carbon supply from the symbiont to the host might be affected by light and temperature.…”

Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

“…One potential benefit of this strategy is the opportunity to partner with symbionts better suited to the local conditions in which a larva settles and develops. Horizontal transmission thus creates the opportunity for hosts to associate with a greater variety of symbionts, and the degree of flexibility in obligate nutritional symbioses has been subject to much research (6)(7)(8)(9)(10).…”

Museum Genomics Illuminate the High Specificity of a Bioluminescent Symbiosis for a Genus of Reef Fish

“…These four individuals were all collected from more temperate regions in Japan and Australia, which had the lowest minimum annual temperatures of all locations surveyed ( Table 1 ). Temperature is a driving factor of the distribution of bacteria in the marine environment ( Sul et al, 2013 ), and has been shown to influence the symbiotic associations of other marine taxa, such as sepiolid squids ( Nishiguchi, 2000 ; Zamborsky and Nishiguchi, 2011 ) and cnidarians ( Herrera et al, 2020 ). Thus, the symbionts associated with these four specimens could have genetic adaptations to slightly cooler temperatures.…”