Published On: Wed, Mar 27th, 2019

Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species [RESEARCH ARTICLE]


Many cnidarians including corals, sea anemones and jellyfish host endosymbiotic dinoflagellates of the family Symbiodinaceae (Davy et al., 2012). Translocation of photosynthetic products, including carbohydrates and lipids, from the symbionts supports host respiration, growth and, in the case of stony corals calcification. In return, 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 (e.g. Coffroth et al., 2010; Rädecker et al., 2018; Voolstra et al., 2009; Weis et al., 2001; Yuyama and Higuchi, 2014). Although many aspects of the interaction remain unclear, the establishment of a stable cnidarian-dinoflagellate relationship is thought to involve a complex series of processes including recognition, suppression of the normal host phagocytotic pathway and ultimately metabolite trafficking (Davy et al., 2012; Matthews et al., 2017; Mohamed et al., 2016), however less is known about the molecular events beyond that point.

Symbiodinium is a highly diverse genus; nine clades are currently recognized and each of these includes many different phylotypes or species (reviewed by LaJeunesse, 2017; Pochon and Gates, 2010). Physiological characteristics – such as photosynthetic activity, growth and stress tolerance – differ among Symbiodinium taxa (Baird and Maynard, 2008; Díaz-Almeyda et al., 2017; Klueter et al., 2015). Initial uptake of potential symbionts appears to be a relatively promiscuous process (Biquand et al., 2017; Cumbo et al., 2013), but there are likely to be several subsequent opportunities for the host to reject phylotypes of Symbiodinium that do not fit its physiological requirements (or vice versa; Dunn and Weis, 2009). Each host organism harbors one or several different Symbiodinium phylotypes in a polyp or colony, and the dominant Symbiodinium phylotype can differ among cnidarian species, seasons, and environmental light and temperature conditions (Baker, 2003; Kuguru et al., 2008; Wilkinson et al., 2015). It is conceivable that the host cnidarian changes the dominant Symbiodinium phylotype to adapt to environmental change (Buddemeier and Fautin, 1993; Rouzé et al., 2017).

Symbionts provide carbon and nitrogen metabolites to the host, but the efficiency with which this occurs differs among Symbiodinium phylotypes (Baker et al., 2013). The coral Isopora palifera naturally associates with either Symbiodinium C or D types and nanoscale secondary ion mass spectrometry (NanoSIMS) has clearly demonstrated that the type C Symbiodinium fixes and transfers more carbon and nitrogen to its host than does the type D symbiont (Pernice et al., 2015). This work, together with studies conducted in the Davy laboratory (Matthews et al., 2017) implies that genes associated with carbon and nitrogen metabolism in the host are likely to differ markedly in expression levels when different Symbiodinium phylotypes are present.

Few data are available concerning the effects of different Symbiodinium phylotypes on host gene expression. Yuyama et al. (2011) used high-coverage gene expression profiling (HiCEP) to examine the response of aposymbiotic juveniles of Acropora tenuis to two different symbiont types but, although 765 genes were differentially expressed between the two groups, only 33 (some of which may be involved in lipid metabolism) could be annotated and validated. Moreover, the presence of different symbiont types has been shown to affect expression levels of specific host genes (Yuyama et al., 2011). In the case of the symbiotic sea anemone Exaiptasia pallida (‘Aiptasia’), colonization by heterologous symbionts (S. trenchii) essentially induced an expression pattern that was intermediate between the symbiotic (i.e. colonized to a similar density by S. minutum=ITS2 type B1) and aposymbiotic states with respect to several pathways associated with symbiosis (Matthews et al., 2017).

A number of investigations have established that the growth and/or nutrition of cnidarian hosts may be compromised by the ‘wrong’ symbiont type, and the Matthews et al. (2017) study highlights the transcriptional consequences of colonization by a heterologous symbiont at a fixed time point. However, to our knowledge, the transcriptional effects in the host during the process of colonization by a heterologous symbiont have not yet been investigated.

In the present study, the temporal effects of colonization by heterologous or homologous Symbiodinium taxa on the host transcriptome were examined. For this purpose, the tropical corallimorpharian, Ricordea yuma, served as host and was infected with either the native (‘homologous’) Symbiodinium goreaui (ITS2 type C1) or the non-native (‘heterologous’) Symbiodinium trenchii (ITS2 type D1a), an opportunistic, thermally tolerant species, isolated from a different corallimorpharian host (Rhodactis indosinensis). Transcriptomic analyses indicate major differences between hosts harboring different Symbiodinium species. We discuss the influences of the two symbiont species on host gene expression and consequent implications for host physiology.

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