How a host cell signalling molecule modifies carbon metabolism in symbionts of the coral Plesiastrea versipora

Abstract

Cnidarian cell signalling remains poorly understood. This study has expanded our knowledge of the cell signalling molecule host release factor (HRF) from the coral Plesiastrea versipora. We have now confirmed that HRF is present in coral host cells that lack intracellular algae. Previous studies showed that HRF stimulates the release of photosynthetic products (mainly glycerol) from Symbiodinium algae, thus providing the host with carbon; glycerol release was accompanied by reduced synthesis of algal triacylglycerols and starch. In this study, we have shown that supplying glycerol to algae incubated with HRF does not restore normal triacylglycerol and starch synthesis. Release of 14C‐labelled products from algae may continue after photosynthesis ceases, although at a much lower rate. When algae were placed in the dark for 4 h with HRF following 2 h of photosynthesis in seawater, 14C‐labelled products were released, but at ≤ 15% of the amount released during 2 h of photosynthesis with HRF. HRF did not stimulate the release of compounds derived from a nonphotosynthetic source. The response of Symbiodinium from P. versipora to HRF has been compared with the response of Symbiodinium algae from Tridacna maxima, Heliofungia actiniformis, Aiptasia pulchella and Pocillopora damicornis to both their own HRF and to P. versipora HRF. Algae from P. versipora showed the highest response to both P. versipora HRF and to the other hosts’ HRF. Further purification of P. versipora HRF suggests that HRF is a peptide with an acidic pI. We propose that HRF will provide a useful tool for the study of carbon metabolism.

Growth and Nutritional Quality of Lemnaceae Viewed Comparatively in an Ecological and Evolutionary Context

“…An integrative review of literature on (i) plant performance under high CO 2 and (ii) plant-microbe interaction and symbioses between photosynthetic and non-photosynthetic organisms [58] suggests that microorganisms can enhance plant photosynthetic productivity and nutritional quality (Figures 10 and 11) by (i) serving as an additional sugar sink that prevents carbohydrate build-up [130,132,[135][136][137][138] and resulting excess ROS formation (see above), (ii) balancing nutrient supply (limiting or excess; see above) and producing growth factors [139], (iii) producing gene regulators that safely re-route electrons and, thereby, further counteract disruption of redox homeostasis under both limiting nutrient supply and very high nitrate supply (see, e.g., [108,140]). Alternative outlets for electrons include cyclic electron flow in the chloroplast [141][142][143][144][145][146].…”

Intersections: photosynthesis, abiotic stress, and the plant microbiome

“…5, 6). Evidence that symbiotic partners act as sugar sinks is seen in symbioses between photosynthetic and nonphotosynthetic partners (Grant et al 2006(Grant et al , 2013, where starch is mobilized from the chloroplast at higher rates. Fig.…”

Coupled carbon and nitrogen cycling regulates the cnidarian-algal symbiosis

“…While the evolution of such interactions may in part be limited by selection at the holobiont level, it is likely that, in addition to the passive metabolic regulation, an active regulation of the symbiosis is also required. To this end, so-called host-release factors that actively promote carbon release by algal symbionts could be a key component in maintaining mutualistic interactions in the cnidarian-algal symbiosis (36)(37)(38), although further data is warranted to unequivocally confirm this. Finally, the processes described here improve our understanding of the maintenance of the symbiosis and its widespread breakdown in the Anthropocene (39).…”