Trehalose Is a Chemical Attractant in the Establishment of Coral Symbiosis

Abstract

Coral reefs have evolved with a crucial symbiosis between photosynthetic dinoflagellates (genus Symbiodinium) and their cnidarian hosts (Scleractinians). Most coral larvae take up Symbiodinium from their environment; however, the earliest steps in this process have been elusive. Here we demonstrate that the disaccharide trehalose may be an important signal from the symbiont to potential larval hosts. Symbiodinium freshly isolated from Fungia scutaria corals constantly released trehalose (but not sucrose, maltose or glucose) into seawater, and released glycerol only in the presence of coral tissue. Spawning Fungia adults increased symbiont number in their immediate area by excreting pellets of Symbiodinium, and when these naturally discharged Symbiodinium were cultured, they also released trehalose. In Y-maze experiments, coral larvae demonstrated chemoattractant and feeding behaviors only towards a chamber with trehalose or glycerol. Concomitantly, coral larvae and adult tissue, but not symbionts, had significant trehalase enzymatic activities, suggesting the capacity to utilize trehalose. Trehalase activity was developmentally regulated in F. scutaria larvae, rising as the time for symbiont uptake occurs. Consistent with the enzymatic assays, gene finding demonstrated the presence of a trehalase enzyme in the genome of a related coral, Acropora digitifera, and a likely trehalase in the transcriptome of F. scutaria. Taken together, these data suggest that adult F. scutaria seed the reef with Symbiodinium during spawning and the exuded Symbiodinium release trehalose into the environment, which acts as a chemoattractant for F. scutaria larvae and as an initiator of feeding behavior- the first stages toward establishing the coral-Symbiodinium relationship. Because trehalose is a fixed carbon compound, this cue would accurately demonstrate to the cnidarian larvae the photosynthetic ability of the potential symbiont in the ambient environment. To our knowledge, this is the first report of a chemical cue attracting the motile coral larvae to the symbiont.

Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians

“…Each step, alone or in conjunction with others, may play a role during the establishment of suitable host/symbiont combinations. Further, each step may be influenced by specific molecular mechanisms as well as physical factors (3654, this study). In the first step, encounter efficiency may be important for initial uptake into the gastric cavity; for example, we have previously shown that symbiont uptake efficiency is concentration-dependent in Aiptasia larvae24.…”

Heritability of theSymbiodiniumcommunity in vertically- and horizontally-transmitting broadcast spawning corals

“…Sugars have also been found to influence bacterial communities in corals 78 and may have similar roles in regulating Symbiodinium communities. Trehalose, in particular, has been identified as an important chemical attractant between Symbiodinium and coral larvae and may help to regulate the early stages of symbiosis 79 . Human studies also provide examples of sugars (both maternal and offspring derived) that make infant intestines less habitable for harmful bacteria, setting up conditions for preferential colonization by favourable bacteria 80 .…”

Potential bleaching effects on coral reproduction

“…Therefore, we were interested in detailing the reproductive profile of Fungia scutaria and Montipora capitata coral populations in Kaneohe Bay (most of which bleached in October 2014), 9 months after their recovery. We compared the details of their post-bleaching reproductive profile to the more than 30 years of reproductive data on F. scutaria in Kaneohe Bay (Krupp 1983;Schwarz et al 1999;Hagedorn et al 2006Hagedorn et al , 2010Hagedorn et al , 2012Hagedorn et al , 2015a) and the almost 20 years of data for M. capitata reproduction (Field 1998;Cox 2007;Padilla-Gamiño et al 2011, 2014PadillaGamiño and Gates 2012;Hagedorn et al 2015b). Nevertheless, without consistent yearly reproductive profiles assessed in a similar manner, these historical comparisons can only be suggestive at best.…”