Abstract

BackgroundWe 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.ResultsPatterns 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.ConclusionsThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-376) contains supplementary material, which is available to authorized users.

Highlights

  • We have a limited understanding of genomic interactions that occur among partners for many symbioses

  • Creation of “aposymbiotic” and “reinfected” tissue Cliona varians forma varians associates with dense populations of Clade G Symbiodinium [38,46]. These sponges can be divorced from their resident symbionts by removing the pinacodermal region of the sponge, which is the site of highest Symbiodinium density (Additional file 1: Figure S1)

  • This is, the first that provides insights into the genetic pathways that appear to be important in poriferan: Symbiodinium partnerships

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Summary

Introduction

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. It is a truism that most if not all species on the planet serve as habitat for one or more microbial symbiont [1] These associations can have ecological outcomes that are beneficial (e.g., mutualisms) or deleterious (e.g., parasitisms), and as such are among the most important biological interactions on the planet given that they affect everything from general ecosystem health to human disease. We understand less about the benefits the symbionts receive from the association, though most hypotheses argue that Symbiodinium benefit from intracellular residency by gaining access to nutrients that are limiting outside the host The partnership is arguably the most important ecological interaction that occurs in shallow tropical habitats worldwide because Symbiodinium spp. energetically subsidize the entire ecosystem and power calcification processes [14] that generate the topographic complexity of these systems

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