Adaptation to Bleaching: Are Thermotolerant Symbiodiniaceae Strains More Successful Than Other Strains Under Elevated Temperatures in a Model Symbiotic Cnidarian?

Casandra R Newkirk,Christine E Schnitzler,Mark Q Martindale,Thomas K Frazer

doi:10.3389/fmicb.2020.00822

Casandra R Newkirk, Christine E Schnitzler + Show 2 more

Open Access

https://doi.org/10.3389/fmicb.2020.00822

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Abstract

The ability of some symbiotic cnidarians to resist and better withstand stress factors that cause bleaching is a trait that is receiving increased attention. The adaptive bleaching hypothesis postulates that cnidarians that can form a stable symbiosis with thermotolerant Symbiodiniaceae strains may cope better with increasing seawater temperatures. We used polyps of the scyphozoan, Cassiopea xamachana, as a model system to test symbiosis success under heat stress. We sought to determine: (1) if aposymbiotic C. xamachana polyps could establish and maintain a symbiosis with both native and non-native strains of Symbiodiniaceae that all exhibit different tolerances to heat, (2) whether polyps with these newly acquired Symbiodiniaceae strains would strobilate (produce ephyra), and (3) if thermally tolerant Symbiodiniaceae strains that established and maintained a symbiosis exhibited greater success in response to heat stress (even if they are not naturally occurring in Cassiopea). Following recolonization of aposymbiotic C. xamachana polyps with different strains, we found that: (1) strains Smic, Stri, Slin, and Spil all established a stable symbiosis that promoted strobilation and (2) strains Bmin1 and Bmin2 did not establish a stable symbiosis and strobilation did not occur. Strains Smic, Stri, Slin, and Spil were used in a subsequent bleaching experiment; each of the strains was introduced to a subset of aposymbiotic polyps and once polyp tissues were saturated with symbionts they were subjected to elevated temperatures - 32°C and 34°C - for 2 weeks. Our findings indicate that, in general, pairings of polyps with Symbiodiniaceae strains that are native to Cassiopea (Stri and Smic) performed better than a non-native strain (Slin) even though this strain has a high thermotolerance. This suggests a degree of partner specificity that may limit the adaptive potential of certain cnidarians to increased ocean warming. We also observed that the free-living, non-native thermotolerant strain Spil was relatively successful in resisting bleaching during experimental trials. This suggests that free-living Symbiodiniaceae may provide a supply of potentially “new” thermotolerant strains to cnidarians following a bleaching event.

Highlights

Endosymbiosis between dinoflagellate algae in the family Symbiodiniaceae and cnidarian hosts is common among many members of the phylum Cnidaria (Muscatine and Porter, 1977; Davy et al, 2012)
All four Symbiodinium species strains of algae, i.e., Symbiodinium microadriaticum (Smic), S. tridacnidorum (Stri), S. linucheae (Slin), and S. pilosum (Spil), were able to establish a stable symbiosis with their host polyps (Figure 2A)
Strobilation occurred within 5–6 weeks for polyps reinoculated with Smic, Stri, and Slin (Figures 2B–D)

Summary

Introduction

Endosymbiosis between dinoflagellate algae in the family Symbiodiniaceae and cnidarian hosts is common among many members of the phylum Cnidaria (Muscatine and Porter, 1977; Davy et al, 2012). The symbiosis between cnidarians and these dinoflagellate algae has been characterized mainly in stony corals due, in large part, to the fact that coral reefs are highly vulnerable to increased ocean warming associated with a changing climate (Walther et al, 2002; Douglas, 2003; Hughes et al, 2003) and is a focus of concern and research. Vulnerability and death of symbiotic coral hosts, is exacerbated by the expulsion of symbionts from host tissues. This expulsion and loss of symbionts is known as “bleaching” and is one of the most pressing environmental issues facing contemporary marine resource managers (HoeghGuldberg, 1999; West and Salm, 2003; Ainsworth et al, 2016; Genevier et al, 2019). Characteristics of the algae are attributed with primary importance (Loya et al, 2001; Bhagooli and Hidaka, 2003; Stat and Gates, 2011; Hume et al, 2015; Cziesielski et al, 2018)

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