Abstract
In reef-building corals (order Scleractinia) and giant clams (phylum Molluca), V-type H+-ATPase (VHA) in host cells is part of a carbon concentrating mechanism (CCM) that regulates photosynthetic rates of their symbiotic algae. Here, we show that VHA plays a similar role in the sea anemone Anemonia majano, a member of the order Actinaria and sister group to the Scleractinia, which in contrast to their colonial calcifying coral relatives is a solitary, soft-bodied taxa. Western blotting and immunofluorescence revealed that VHA was abundantly present in the host-derived symbiosome membrane surrounding the photosymbionts. Pharmacological inhibition of VHA activity in individual anemones resulted in an approximately 80% decrease of photosynthetic O2 production. These results extend the presence of a host-controlled VHA-dependent CCM to non-calcifying cnidarians of the order Actiniaria, suggesting it is widespread among photosymbiosis between aquatic invertebrates and Symbiodiniaceae algae.
Highlights
Symbiotic associations between animals and microorganisms have facilitated the acquisition of a variety of novel physiological capabilities on relatively short evolutionary time scales [1]
Our results indicate that A. majano uses V-type H+-ATPase (VHA) located in the symbiosome membrane of symbiocytes to promote photosynthesis by their endosymbiotic Symbiodiniaceae algae
An analogous mechanism has since been reported in the photosymbiotic association between giant clams and Symbiodiniaceae algae; in this case, the VHA is located in the lumen-facing membrane of the epithelial cells that line the z-tubules where the algal symbionts are hosted extracellularly [15]
Summary
Symbiotic associations between animals and microorganisms have facilitated the acquisition of a variety of novel physiological capabilities on relatively short evolutionary time scales [1]. Photosymbiotic associations between marine organisms and dinoflagellates in the family Symbiodiniaceae are widespread, providing an excellent opportunity for comparative and evolutionary studies. These associations are often regarded as royalsocietypublishing.org/journal/rsos R. Mutually beneficial, with the algae receiving shelter and nutrients from the animal host in exchange for 2 photosynthetically fixed sugars and other photosynthates [2,3]. Another view considers these relationships as parasitic, whereby the animal forces the release of photosynthates while simultaneously restricting algal growth and reproduction, two key aspects of algal fitness [4,5]. Elucidating the mechanisms that control photosymbiosis is key for determining their physiological and environmental importance, identifying patterns and understanding broader evolutionary principles
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