Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis

Abstract

Bleaching (dinoflagellate symbiont loss) is one of the greatest threats facing coral reefs. The functional cnidarian-dinoflagellate symbiosis, which forms coral reefs, is based on the bi-directional exchange of nutrients. During thermal stress this exchange breaks down; however, major gaps remain in our understanding of the roles of free metabolite pools in symbiosis and homeostasis. In this study we applied gas chromatography-mass spectrometry (GC-MS) to explore thermally induced changes in intracellular pools of amino and nonamino organic acids in each partner of the model sea anemone Aiptasia sp. and its dinoflagellate symbiont. Elevated temperatures (32°C for 6 days) resulted in symbiont photoinhibition and bleaching. Thermal stress induced distinct changes in the metabolite profiles of both partners, associated with alterations to central metabolism, oxidative state, cell structure, biosynthesis and signalling. Principally, we detected elevated pools of polyunsaturated fatty acids (PUFAs) in the symbiont, indicative of modifications to lipogenesis/lysis, membrane structure and nitrogen assimilation. In contrast, reductions of multiple PUFAs were detected in host pools, indicative of increased metabolism, peroxidation and/or reduced translocation of these groups. Accumulations of glycolysis intermediates were also observed in both partners, associated with photoinhibition and downstream reductions in carbohydrate metabolism. Correspondingly, we detected accumulations of amino acids and intermediate groups in both partners, with roles in gluconeogenesis and acclimation responses to oxidative stress. These data further our understanding of cellular responses to thermal stress in the symbiosis and generate hypotheses relating to the secondary roles of a number of compounds in homeostasis and heatstress resistance.

Warm-preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone

“…Our data present an incomplete picture of holobiont metabolism, and application of histological analyses (Dunn et al, 2012) and 'omics' techniques at the post-translational level (Drake et al, 2013;Hillyer et al, 2015;Oakley et al, 2015;Weston et al, 2015), respectively, is needed to confirm or refute the hypothesised changes in aerobic metabolic pathways and mitochondrial densities. Notwithstanding these limitations, this investigation provides some of the first evidence for significant effects of thermal preconditioning on the heat sensitivity of symbiotic cnidarian and Symbiodinium mitochondrial activity.…”

“…It is probably not increased by NAD + reduction via the TCA cycle, as host CS activity remained unchanged. Glycolysis is an alternative pathway for NADH production (Berg et al, 2002), and a build-up of glycolytic products has been noted for this species of sea anemone during heat stress (Hillyer et al, 2015). Whatever the compensatory source of NADH, its increased oxidation by NQO could shift the cellular NAD + /NADH balance, with potential consequences for cell viability (Ying, 2008;Santidrian et al, 2013).…”

Mapping carbon fate during bleaching in a model cnidarian symbiosis: the application of 13C metabolomics

“…Thermal acclimation is energetically costly and will necessitate downstream changes in metabolic pathways (Kaplan et al ., ); as such, given the central role of starch as a readily mobilized energy store in the dinoflagellate (Kopp et al ., ), increased turnover and reduced input into symbiont starch stores under conditions of ATP limitation are perhaps unsurprising. However, the increased 13 C enrichment of the symbiont's galactose pool was notable and probably indicative of downstream changes to fatty acid synthesis and lipogenesis (see the Modifications to fatty acid metabolism and lipogenesis during bleaching subsection), which are also well documented during thermal stress (Papina et al ., ; Díaz‐Almeyda et al ., ; Hillyer et al ., ), inhibited starch synthesis (Li et al ., ) and nitrogen limitation (Dagenais Bellefeuille et al ., ; Jiang et al ., ) (Fig. ).…”

Elucidating the sponge stress response; lipids and fatty acids can facilitate survival under future climate scenarios

“…Bleached phototrophic sponges (characterized by reduced chlorophyll a content) experienced significant declines in their dominant SFA (16:0), whereas the concentration of the second most abundant SFA in these two species (22:0 for C. foliascens and 14:0 for C. coralliophila ) increased with temperature. The decline in 16:0 in thermally stressed phototrophic sponges is either due to loss of symbionts or reflects a breakdown in symbiont FA biosynthesis, and the subsequent reduced translocation of this FA to the sponge host (Figueiredo et al., ; Hillyer, Tumanov, Villas‐Bôas, & Davy, ; Imbs & Yakovleva, ). Meanwhile, the increase in other abundant SFA either reflects a switch in diet, e.g.…”