Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species.

Mei-Fang Lin,Sylvain Forêt,David J Miller,Shunichi Takahashi,Simon K Davy

doi:10.1242/bio.038281

Abstract

ABSTRACTReef-building corals and some other cnidarians form symbiotic relationships with members of the dinoflagellate family Symbiodinaceae. As Symbiodinaceae is a highly diverse taxon, the physiological interactions between its members and their hosts are assumed to differ between associations. The presence of different symbiont types is known to affect expression levels of specific host genes, but knowledge of the effects on the transcriptome more broadly remains limited. In the present study, transcriptome profiling was conducted on the tropical corallimorpharian, Ricordea yuma, following the establishment of symbiosis with either the ‘homologous’ symbiont Symbiodinium goreaui (also known as Cladocopium goreaui; ITS2 type C1) or ‘heterologous’ symbionts (predominantly S. trenchii, which is also known as Durusdinium trenchii; ITS2 type D1a) isolated from a different corallimorpharian host (Rhodactis indosinensis). Transcriptomic analyses showed that genes encoding host glycogen biosynthesis pathway components are more highly induced during colonization by the homologous symbiont than by the heterologous symbiont. Similar patterns were also observed for several other genes thought to facilitate symbiotic nutrient exchange, including those involved in lipid translocation/storage and metabolite transport. The gene expression results presented here imply that colonization by homologous or heterologous Symbiodinium types may have very different metabolic consequences for the Ricordea host, supporting the notion that even though some cnidarians may be able to form novel symbioses after bleaching, the metabolic performance of these may be compromised.This article has an associated First Person interview with the first author of the paper.

Highlights

Many cnidarians including corals, sea anemones and jellyfish host endosymbiotic dinoflagellates of the family Symbiodinaceae (Davy et al, 2012)
Uptake of Symbiodinium in bleached Ricordea As described above, bleached Ricordea specimens inoculated with homologous (ITS type C1) or heterologous symbionts, and the control group are referred to as Groups C, D and N respectively
Transcriptomic analyses demonstrated that the expression of genes related to the glycogen biosynthetic pathway was higher in hosts containing S. goreaui than those containing S. trenchii, implying that in the Ricordea association S. goreaui may translocate more photosynthetically-fixed carbon to the host than S. trenchii

Summary

Introduction

Sea anemones and jellyfish host endosymbiotic dinoflagellates of the family Symbiodinaceae (Davy et al, 2012). The host provides inorganic carbon, nitrogen and phosphorus to the symbionts (Davy et al, 2012). The cnidarian-Symbiodinium symbiosis is a cornerstone of biologically-enriched coral reef ecosystems. Whilst some species inherit Symbiodinium maternally (vertical transmission), the majority of coral species acquire their symbionts from the environment (horizontal transmission) during the early stages of each generation (Baird et al, 2009). Symbiodinium cells isolated from cnidarian hosts can often infect a range of other host species, at least under experimental conditions Many aspects of the interaction remain unclear, the establishment of a stable cnidariandinoflagellate relationship is thought to involve a complex series of processes including recognition, suppression of the normal host phagocytotic pathway and metabolite trafficking (Davy et al, 2012; Matthews et al, 2017; Mohamed et al, 2016), less is known about the molecular events beyond that point

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