Open Access Research article

Transcriptomic analysis of differential host gene expression upon uptake of symbionts: a case study with Symbiodinium and the major bioeroding sponge Cliona varians

Ana Riesgo12, Kristin Peterson34, Crystal Richardson35, Tyler Heist3, Brian Strehlow36, Mark McCauley37, Carlos Cotman3, Malcolm Hill3* and April Hill3*

Author Affiliations

1 Department of Organismic and Evolutionary Biology, Harvard University, Barcelona, Spain

2 Department of Animal Biology, Universitat de Barcelona, Barcelona, Spain

3 Department of Biology, University of Richmond, Richmond, VA, USA

4 Department of Molecular Physiology and Biophysics, Vanderbilt School of Medicine, Nashville, TN, USA

5 Department of Cell Biology, University of Virginia, Charlottesville, VA, USA

6 University of Western Australia, Australian Institute of Marine Science, Perth, Australia

7 Department of Biology, University of Mississippi, University, MS, USA

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BMC Genomics 2014, 15:376  doi:10.1186/1471-2164-15-376

Published: 16 May 2014

Abstract

Background

We have a limited understanding of genomic interactions that occur among partners for many symbioses. One of the most important symbioses in tropical reef habitats involves Symbiodinium. Most work examining Symbiodinium-host interactions involves cnidarian partners. To fully and broadly understand the conditions that permit Symbiodinium to procure intracellular residency, we must explore hosts from different taxa to help uncover universal cellular and genetic strategies for invading and persisting in host cells. Here, we present data from gene expression analyses involving the bioeroding sponge Cliona varians that harbors Clade G Symbiodinium.

Results

Patterns of differential gene expression from distinct symbiont states (“normal”, “reinfected”, and “aposymbiotic”) of the sponge host are presented based on two comparative approaches (transcriptome sequencing and suppressive subtractive hybridization (SSH)). Transcriptomic profiles were different when reinfected tissue was compared to normal and aposymbiotic tissue. We characterized a set of 40 genes drawn from a pool of differentially expressed genes in “reinfected” tissue compared to “aposymbiotic” tissue via SSH. As proof of concept, we determined whether some of the differentially expressed genes identified above could be monitored in sponges grown under ecologically realistic field conditions. We allowed aposymbiotic sponge tissue to become re-populated by natural pools of Symbiodinium in shallow water flats in the Florida Keys, and we analyzed gene expression profiles for two genes found to be increased in expression in “reinfected” tissue in both the transcriptome and via SSH. These experiments highlighted the experimental tractability of C. varians to explore with precision the genetic events that occur upon establishment of the symbiosis. We briefly discuss lab- and field-based experimental approaches that promise to offer insights into the co-opted genetic networks that may modulate uptake and regulation of Symbiondinium populations in hospite.

Conclusions

This work provides a sponge transcriptome, and a database of putative genes and genetic pathways that may be involved in Symbiodinium interactions. The relative patterns of gene expression observed in these experiments will need to be evaluated on a gene-by-gene basis in controlled and natural re-infection experiments. We argue that sponges offer particularly useful characteristics for discerning essential dimensions of the Symbiodinium niche.

Keywords:
Symbiosis; Genetic integration; Porifera; Transcriptome; Zooxanthellae