Symbiont type and environmental factors affect transcriptome-wide gene expression in the coral Montipora capitata.

Misaki Takabayashi,M Renee Bellinger,Martin Helmkampf,Monika Frazier

doi:10.1002/ece3.4756

Abstract

Reef‐building corals may harbor genetically distinct lineages of endosymbiotic dinoflagellates in the genus Symbiodinium, which have been shown to affect important colony properties, including growth rates and resilience against environmental stress. However, the molecular processes underlying these differences are not well understood. In this study, we used whole transcriptome sequencing (RNA‐seq) to assess gene expression differences between 27 samples of the coral Montipora capitata predominantly hosting two different Symbiodinium types in clades C and D. The samples were further characterized by their origin from two field sites on Hawai‘i Island with contrasting environmental conditions. We found that transcriptome‐wide gene expression profiles clearly separated by field site first, and symbiont clade second. With 273 differentially expressed genes (DEGs, 1.3% of all host transcripts), symbiont clade had a measurable effect on host gene expression, but the effect of field site proved almost an order of magnitude higher (1,957 DEGs, 9.6%). According to SNP analysis, we found moderate evidence for host genetic differentiation between field sites (F ST = 0.046) and among corals harboring alternative symbiont clades (F ST = 0.036), suggesting that site‐related gene expression differences are likely due to a combination of local adaptation and acclimatization to environmental factors. The correlation between host gene expression and symbiont clade may be due to several factors, including host genotype or microhabitat selecting for alternative clades, host physiology responding to different symbionts, or direct modulation of host gene expression by Symbiodinium. However, the magnitude of these effects at the level of transcription was unexpectedly small considering the contribution of symbiont type to holobiont phenotype.

Highlights

Symbiosis, the persistent, intimate association between species (Bouchard, 2009), shapes all aspects of the biosphere from molecular structure to ecosystem function
The objective of the present study was to expand upon this incipient knowledge of how different coral–Symbiodinium partnerships affect gene expression, and to shed more light on how interactions between symbiont partners are regulated at the genetic level in Montipora capitata, one of the most common coral species in Hawai‘i. Using whole transcriptome sequencing (RNA‐seq), we examined the transcriptional profiles of M. capitata colonies in field populations harboring Symbiodinium types representing clades C and D
We investigated transcriptome‐wide differences in host gene expression associated with two dominant types of Symbiodinium clade C and D in the coral M. capitata, which is of particular interest considering some clade D symbionts may convey higher resistance to elevated water temperatures and are globally increasing in prevalence

Summary

| INTRODUCTION

The persistent, intimate association between species (Bouchard, 2009), shapes all aspects of the biosphere from molecular structure to ecosystem function. Most transcriptomic studies have focused on the establishment of symbiosis in coral larvae (Mohamed et al, 2016; Schnitzler & Weis, 2010; Voolstra et al, 2009), recently settled coral polyps (O'Rourke et al, 2017), and adult symbiotic and nonsymbiotic sea anemones (Lehnert et al, 2014; Rodriguez‐Lanetty, Phillips, & Weis, 2006) In most of these studies, significant changes in host gene expression suggested an active role of the host in the establishment and regulation of symbiosis. The first to show a correlation between Symbiodinium type and host transcription, DeSalvo et al (2010) reported expression changes in genes involved in protein metabolism in the coral Montastraea faveolata. We provided a list of host genes whose expression was correlated with Symbiodinium clade, and employed coexpression network analysis to illuminate the connectivity and function of genes that might be responsive to the presence of different symbiont clades

| MATERIALS AND METHODS

| DISCUSSION

Findings

| CONCLUSIONS