Phylogenetic diversity, functional convergence, and stress response of the symbiotic system between sponges and microorganisms

All living multicellular organisms contain associated microorganisms, which often make substantial symbiotic contributions to host physiology, behaviors and evolution. Marine sponges host dense and highly diverse communities of symbiotic microorganisms. These symbionts are assembled in stable and host-specific community structures and are often inherited through the sponges generations. Previous investigations have provided a good understanding of the phylogenetic diversity of microbial symbionts in marine sponges. However the functional features that underpin their symbiotic interactions are largely unknown.This thesis uses sponges as models to address fundamental concepts of microbial symbiosis, including community diversity and assembly, metabolic interactions with the host and other symbionts, as well as symbiosis stability under perturbations. State-of-the-art techniques including 16S rRNA gene pyro-tag-sequencing, metagenomics and metaproteomics were applied. Specifically, a pipeline was developed to reconstruct full-length ribosomal rRNA genes from pyrosequencing metagenomic shotgun data. This work showed that a substantial proportion of microbial diversity has been typically missed by the PCR-based approaches. Detailed metagenomic analyses then identified the functional core in symbiont communities from taxonomically distinct sponge species. The result indicated that common functions were provided by distinct but functionally equivalent symbionts and enzymes in different sponge hosts. Moreover, the abundant elements involved in horizontal gene transfer suggested their key roles in distributing core functions between co-evolutionary symbionts and in facilitating functional convergence on the community scale. To investigate the expression profile of sponge symbionts, metaproteogenomic analysis was conducted on the sponge Cymbastela concentrica. The analysis detected abundant protein expression for the functions of substrate transport, aerobic and anaerobic metabolisms, stress response, and host-symbiont interactions. To study the stability and dynamics of the sponge holobiont during perturbation, the sponge Rhopaloeides odorabile was examined under controlled thermal stress. Dramatic changes in community structure, functional composition and gene expression were observed along with the host stress response suggesting that a decline in symbiotic interactions was likely to be the key factor in the loss of holobiont function.These discoveries combined with a theoretical framework advanced our knowledge in sponge microbiology and provided new insights into the ecology and evolution of microbial symbiosis