Trehalose is a chemical attractant in the establishment of coral symbiosis.

Mary Hagedorn,Micaiah Phillips,Virginia Carter,Nikolas Zuchowicz,Frederick W Kleinhans,Paul H Yancey,Elizabeth A Vallen,Kelly Peterson,Meghan White,Chelsea Penfield,Brittany Shamenek

doi:10.1371/journal.pone.0117087

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.

Highlights

Symbiotic partnerships between microorganisms and their hosts are critical for the health and function of biological systems ranging from individuals to ecosystems [1]
Our analysis shows lower levels of trehalose in the presence of coral larvae compared to other samples, but it might be that trehalose levels in these samples are somewhat decreased by the uptake and utilization of trehalose by the larvae in those samples
Trehalose was produced and excreted by recently excised and wild Symbiodinium without the need of a host factor. Fungia larvae followed both a glycerol and trehalose gradient, but as glycerol was only released by Symbiodinium in close proximity to live coral tissue, this cue is unlikely to play a role in the orienting events

Summary

Introduction

Symbiotic partnerships between microorganisms and their hosts are critical for the health and function of biological systems ranging from individuals to ecosystems [1]. Muscatine and colleagues pioneered an understanding of the marine microalgae-invertebrate association from the late 1950’s onwards [2]. These partnerships allow corals, anemones and sponges to receive fixed carbon from photosynthetic dinoflagellates of the genus Symbiodinium. Symbiodinium can release 50–90% of their reduced carbon to their cnidarian host [3,4,5,6], providing a critical supply of energy and forming the trophic basis of coral reef ecosystems. The Symbiodinium receive a stable location with light for photosynthesis, protection from herbivory and waste products from their host [7]

Objectives

Methods

Results

Discussion

Conclusion