Symbiont Identity Impacts the Microbiome and Volatilome of a Model Cnidarian-Dinoflagellate Symbiosis

SIMPLE SUMMARY: The success of coral reefs is underpinned by the symbiosis between corals and their dinoflagellate symbionts. Crucially, metabolic interactions between the two partners support coral metabolism and survival, although these can be influenced by symbiont identity and inter-partner compatibility. Here, we measured how symbiont identity influences the release of biogenic volatile organic compounds (BVOCs) via the symbiosis, and related this to concurrent shifts in the host microbiome; BVOCs are end-products of metabolism and important biological signal molecules. We used the sea anemone Aiptasia, a model system for cnidarian-dinoflagellate symbiosis, when either symbiont-free, populated with its native symbiont, or populated with a non-native symbiont. We detected 142 BVOCs across all treatments. The volatile profiles of symbiont-free anemones and those containing the native symbiont were distinct, while the volatile profile of anemones containing the non-native symbiont shared characteristics with both. The symbiotic state also caused a change in the host microbiome, but this did not explain the changes seen in BVOC release. These findings contribute to our understanding of how corals may respond to climate change should they acquire novel symbionts post-bleaching. Furthermore, we provide a platform for future studies of the metabolic and/or signalling roles of BVOCs in this important symbiosis. ABSTRACT: The symbiosis between cnidarians and dinoflagellates underpins the success of reef-building corals in otherwise nutrient-poor habitats. Alterations to symbiotic state can perturb metabolic homeostasis and thus alter the release of biogenic volatile organic compounds (BVOCs). While BVOCs can play important roles in metabolic regulation and signalling, how the symbiotic state affects BVOC output remains unexplored. We therefore characterised the suite of BVOCs that comprise the volatilome of the sea anemone Exaiptasia diaphana (‘Aiptasia’) when aposymbiotic and in symbiosis with either its native dinoflagellate symbiont Breviolum minutum or the non-native symbiont Durusdinium trenchii. In parallel, the bacterial community structure in these different symbiotic states was fully characterised to resolve the holobiont microbiome. Based on rRNA analyses, 147 unique amplicon sequence variants (ASVs) were observed across symbiotic states. Furthermore, the microbiomes were distinct across the different symbiotic states: bacteria in the family Vibrionaceae were the most abundant in aposymbiotic anemones; those in the family Crocinitomicaceae were the most abundant in anemones symbiotic with D. trenchii; and anemones symbiotic with B. minutum had the highest proportion of low-abundance ASVs. Across these different holobionts, 142 BVOCs were detected and classified into 17 groups based on their chemical structure, with BVOCs containing multiple functional groups being the most abundant. Isoprene was detected in higher abundance when anemones hosted their native symbiont, and dimethyl sulphide was detected in higher abundance in the volatilome of both Aiptasia-Symbiodiniaceae combinations relative to aposymbiotic anemones. The volatilomes of aposymbiotic anemones and anemones symbiotic with B. minutum were distinct, while the volatilome of anemones symbiotic with D. trenchii overlapped both of the others. Collectively, our results are consistent with previous reports that D. trenchii produces a metabolically sub-optimal symbiosis with Aiptasia, and add to our understanding of how symbiotic cnidarians, including corals, may respond to climate change should they acquire novel dinoflagellate partners.