Symbiosis induces unique volatile profiles in the model cnidarian Aiptasia

Abstract

The establishment and maintenance of the symbiosis between a cnidarian host and its dinoflagellate symbionts is central to the success of coral reefs. To explore the metabolite production underlying this symbiosis, we focused on a group of low weight secondary metabolites, biogenic volatile organic compounds (BVOCs). BVOCs are released from an organism or environment, and can be collected in the gas phase, allowing non-invasive analysis of an organism's metabolism (i.e. ‘volatilomics’). We characterised volatile profiles of the sea anemone Exaiptasia diaphana (‘Aiptasia’), a model system for cnidarian–dinoflagellate symbiosis, using comprehensive two-dimensional gas chromatography coupled with time-of-flight mass spectrometry. We compared volatile profiles between: 1) symbiotic anemones containing their native symbiont, Breviolum minutum; 2) aposymbiotic anemones; and 3) cultured isolates of B. minutum. Overall, 152 BVOCs were detected, and classified into 14 groups based on their chemical structure, the most numerous groups being alkanes and aromatic compounds. A total of 53 BVOCs were differentially abundant between aposymbiotic anemones and B. minutum cultures; 13 between aposymbiotic and symbiotic anemones; and 60 between symbiotic anemones and cultures of B. minutum. More BVOCs were differentially abundant between cultured and symbiotic dinoflagellates than between aposymbiotic and symbiotic anemones, suggesting that symbiosis may modify symbiont physiology more than host physiology. This is the first volatilome analysis of the Aiptasia model system and provides a foundation from which to explore how BVOC production is perturbed under environmental stress, and ultimately the role they play in this important symbiosis.

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

“…Dimethyl sulphide (DMS) was found in high abundance in the volatilome of both Aiptasia-Symbiodiniaceae combinations, irrespective of symbiont identity, but was absent in the volatilome of aposymbiotic anemones. This contrasts with our previous study in which we did identify small amounts of DMS in the volatilome of aposymbiotic anemones [43], potentially arising from the bacterial metabolism of dimethylsulphoniopropionate (DMSP) to DMS and acrylate [99]; nevertheless, in all reported cases, the presence of Symbiodiniaceae is associated with a much more prolific release of DMS from the holobiont, highlighting a central role for the algal partner in its synthesis [43,100]. Moreover, we found DMS production to be greatest in the presence of the heterologous D. trenchii.…”

“…Biogenic volatile organic compounds (BVOCs) are low-molecular-weight (<200 Da) chemicals with high vapour pressure [36] that are produced by a broad diversity of organisms. BVOCs are emitted by all organisms, including bacteria [37], fungi [38], algae [39], plants [40], insects [41], corals [42], sea anemones [43], and mammals [44]. On a global scale, the emission of organically produced VOCs exceeds that of VOCs from anthropogenic sources [45].…”

“…Furthermore, Aiptasia can reproduce asexually, allowing the maintenance of clonal populations [56]. While previous work has shown how the microbiome and volatilome change in Aiptasia in response to symbiosis with a homologous symbiont [31,43] and in response to thermal stress [57], there is a gap regarding the impact of symbiont identity on the microbiome and BVOC production. We therefore explored how the microbiome and volatilome change in response to a switch in the dinoflagellate endosymbiont community of Aiptasia.…”

TheSymbiodiniumProteome Response to Thermal and Nutrient Stresses

“…Established Symbiodiniaceae cultures also have distinct microbiomes, which may positively or negatively affect algal nutrient transport ( Camp et al. 2020 , Wuerz et al. 2022 ).…”