Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential

Abstract

SUMMARY Marine sponges often contain diverse and abundant microbial communities, including bacteria, archaea, microalgae, and fungi. In some cases, these microbial associates comprise as much as 40% of the sponge volume and can contribute significantly to host metabolism (e.g., via photosynthesis or nitrogen fixation). We review in detail the diversity of microbes associated with sponges, including extensive 16S rRNA-based phylogenetic analyses which support the previously suggested existence of a sponge-specific microbiota. These analyses provide a suitable vantage point from which to consider the potential evolutionary and ecological ramifications of these widespread, sponge-specific microorganisms. Subsequently, we examine the ecology of sponge-microbe associations, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution. The ecological and evolutionary importance of sponge-microbe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in at least some cases, the compounds are of microbial rather than sponge origin. We review the status of this important field, outlining the various approaches (e.g., cultivation, cell separation, and metagenomics) which have been employed to access the chemical wealth of sponge-microbe associations.

Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis

“…Metabolism and stress response The characteristics described above facilitate the persistence of a distinct bacterial community in C. concentrica, allowing for the maintenance of specific sponge-bacteria functional relationships. Sponge-associated bacteria have long been speculated to have evolved metabolic dependencies on their host or specific metabolic properties suitable for their environment (reviewed in Taylor et al, 2007b). Four observations from our analyses support this:…”

“…In contrast, the community of C. concentrica was dominated by distinct phylogenetic clusters within the g-proteobacteria, Phyllobacteriaceae, Sphingomondales, Neisseriales and Nitrospiracae, among others (Figure 1). In particular, the a-and g-proteobacterial groups are related to bacteria found in other sponges, as previously reported (Taylor et al, 2005(Taylor et al, , 2007b, whereas phyla such as Acidobacteria and Chloroflexi described to be present in some sponge species are absent in C. concentrica. A total of 34 sequences (0.95% of all sequences) were common to both the C. concentrica and the planktonic community.…”

“…The considerable bacterial biomass associated with sponges, the existence of sub-populations of bacterial cells in different host compartments with proposed symbiotic host-bacteria interactions and the early discovery of the sponge-bacteria ecosystem as a source of novel bioactives and natural product chemistry have driven many efforts to identify and improve our understanding of spongeassociated microorganisms (Taylor et al, 2007b;Vogel, 2008). Moreover, recent phylogenetic studies suggest that marine sponges harbour specific, stable microbial communities that are distinct in composition from those of the surrounding seawater (Taylor et al, 2007b). The existence of such distinct communities is remarkable given that the sponge's bacterial community is constantly exposed to large amounts of filtered, planktonic bacteria (Vogel, 1977).…”

Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea

“…In recent years, advances in molecular techniques, such as 16S rRNA gene-based clone library, fluorescence in situ hybridization, denaturing gradient gel electrophoresis and terminal restriction fragment length polymorphism (T-RFLP), provide a culture-independent means to improve resolution on revealing the microbial diversity and to make a more accurate phylogenetic affiliation assessment for microbes in a complex community such as sponges. Using these techniques, 20 bacterial and 2 archaeal phyla were discovered in sponges from different geographic locations up to 2008 (Taylor et al, 2007;Webster et al, 2008;Zhu et al, 2008). In addition, sponges from geographically separated regions shared high similarity in their bacterial communities, and sequence clusters specific for sponges absent from the surrounding sea water were identified (Friedrich et al, 2001;Hentschel et al, 2002).…”

“…For the assignment of reads to previously described sponge-specific clusters, 16S rRNA sequences were first extracted from an ARB database containing the sponge-specific cluster sequences (Taylor et al, 2007). V5 and V6 regions of the recruited cluster sequences were split by recognizing the U789F and U1068R primers, and then aligned with the tag pyrosequence reads using MUSCLE (Edgar, 2004).…”