Cell Biology of Cnidarian-Dinoflagellate Symbiosis

Abstract

SUMMARY The symbiosis between cnidarians (e.g., corals or sea anemones) and intracellular dinoflagellate algae of the genus Symbiodinium is of immense ecological importance. In particular, this symbiosis promotes the growth and survival of reef corals in nutrient-poor tropical waters; indeed, coral reefs could not exist without this symbiosis. However, our fundamental understanding of the cnidarian-dinoflagellate symbiosis and of its links to coral calcification remains poor. Here we review what we currently know about the cell biology of cnidarian-dinoflagellate symbiosis. In doing so, we aim to refocus attention on fundamental cellular aspects that have been somewhat neglected since the early to mid-1980s, when a more ecological approach began to dominate. We review the four major processes that we believe underlie the various phases of establishment and persistence in the cnidarian/coral-dinoflagellate symbiosis: (i) recognition and phagocytosis, (ii) regulation of host-symbiont biomass, (iii) metabolic exchange and nutrient trafficking, and (iv) calcification. Where appropriate, we draw upon examples from a range of cnidarian-alga symbioses, including the symbiosis between green Hydra and its intracellular chlorophyte symbiont, which has considerable potential to inform our understanding of the cnidarian-dinoflagellate symbiosis. Ultimately, we provide a comprehensive overview of the history of the field, its current status, and where it should be going in the future.

Molecular signatures of host specificity linked to habitat specialization in Exaiptasia sea anemones

“…Gene set enrichment analyses revealed overrepresentation of loci in the complement pathway and thrombospondin‐type‐1 repeat (TSR) domain genes (Table 4). A locus in complement C3, a protein that opsonizes foreign microbes and then enhances their phagocytosis by binding to receptors on the surface of host cells (Davy et al., 2012; Poole et al., 2016), was highly differentiated in our dataset. Loci in several TSR domain genes were also highly differentiated.…”

“…Loci in N ‐glycanase 1 and cytoplasmic FMR1‐interacting protein 2 (CYFIP2) were also strongly associated with divergence of the Bocas‐specific population (Table 3). N ‐glycanase 1 is an enzyme that cleaves N‐ linked glycans preferentially from high‐mannose glycoproteins (Zhou et al., 2006) and may be of interest given evidence for an important role of glycan/lectin interactions in recognition of cnidarian symbionts (Davy et al., 2012; Wood‐Charlson, Hollingsworth, Krupp, & Weis, 2006). CYFIP2 is a pro‐apoptotic gene involved in adhesion of human immune cells (Mayne et al., 2004) and is part of WAVE1, a protein complex that activates actin filament reorganization and regulates formation of cytoplasmic projections prior to phagocytosis.…”

“…The coral‐ Symbiodinium symbiosis funnels energy from sunlight through algal photosynthesis and into cnidarian metabolism to generate energy and the calcium carbonate framework of coral reef ecosystems (Gattuso, Allemand, & Frankignouelle, 1999). Symbiodinium living inside host endodermal cells receive access to carbon dioxide, inorganic nutrients, protection from herbivory, and a stable position in the water column to access light (Davy, Allemand, & Weis, 2012). In return, the coral host receives fixed carbon compounds that enhance calcification and support a large portion of host metabolic demands (Muscatine, Falkowski, Porter, & Dubinsky, 1984; Yellowlees, Rees, & Leggat, 2008).…”

Investigating the Driving Mechanisms Behind Differences in Bleaching and Disease Susceptibility Between Two Scleractinian Corals, Pseudodiploria Strigosa and Diploria Labyrinthiformis

“…Alternatively, lectins were found to be upregulated in Acropora cervicornis with white band disease (Libro et al 2013), thermally stressed S. pistillata (MaorLandaw et al 2014) and naturally bleached A. millepora (Seneca et al 2010). While lectins often have innate immune roles such as pathogen recognition, they are also associated with Symbiodinium uptake (Davy et al 2012), as well as many other functions.…”

“…Calumenin is a calcium binding protein associated with protein folding and sorting, the coagulation system, wound healing, and has loosely been tied to lung fibrosis and arterial pulmonal hypertension diseases in humans (Honoré 2009). In corals, calumenin is attributed to other roles, such as calcification (Libro et al 2013) and the endosymbiosis of Symbiodinium (Davy et al 2012). Additionally, it has been found to be upregulated in white band infected A. cervicornis (Libro et al 2013) and thermotolerant A. millepora .…”