The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses

Zooxanthella symbioses are arguably the most important ecological interaction on coral reefs because they energetically subsidize the entire community, and enhance the calcification process that provides structure for all other organisms. While we have developed a detailed understanding of the diversity among and within the Symbiodinium clades, we currently lack a mechanistic explanation for which factors favoured zooxanthella invasion of the intracellular habitat in heterotrophic hosts, and for what molecular mechanisms permit residence within the cell. We propose two hypotheses that explain important evolutionary and ecological features of zooxanthella symbioses. The magnesium inhibition hypothesis (MIH) states that increases in the Mg/Ca ratio in sea water that occurred over the last 100 million years created a situation where Mg2+ inhibited Ca2+ transport to zooxanthellae. The MIH predicts, among other things, that the intracellular niche was invaded as a response to this abiotic stressor. The arrested phagosome hypothesis (APH) states that Symbiodinium spp. mimic host cell endosomal digestive machinery via the symbiosome to appear like digesting prey through perpetual release of zooxanthella-derived compounds. The APH represents a subtle but important distinction from previous hypotheses regarding interactions between symbiont and host at the cellular level. The APH predicts that symbionts tune rates of material release to match expectations of host cellular machinery. An outcome of the APH is that intra-host residence time becomes a vital parameter to consider. Both hypotheses shift control of the symbiosis away from the host, and instead focus attention on the niche requirements of Symbiodinium spp.