The Sponge Hologenome

Abstract

A paradigm shift has recently transformed the field of biological science; molecular advances have revealed how fundamentally important microorganisms are to many aspects of a host's phenotype and evolution. In the process, an era of "holobiont" research has emerged to investigate the intricate network of interactions between a host and its symbiotic microbial consortia. Marine sponges are early-diverging metazoa known for hosting dense, specific, and often highly diverse microbial communities. Here we synthesize current thoughts about the environmental and evolutionary forces that influence the diversity, specificity, and distribution of microbial symbionts within the sponge holobiont, explore the physiological pathways that contribute to holobiont function, and describe the molecular mechanisms that underpin the establishment and maintenance of these symbiotic partnerships. The collective genomes of the sponge holobiont form the sponge hologenome, and we highlight how the forces that define a sponge's phenotype in fact act on the genomic interplay between the different components of the holobiont.

FIG 1

(A) Overview of a marine sponge body plan showing a schematic representation of an asconoid sponge. For the more common leuconoid sponge morphology, see the detailed schematic representation in reference . Seawater enters the sponge through tiny pores (ostia) in the surface layer (pinacoderm). Flagellated choanocyte cells are arranged in rings lining the sponge’s aquiferous system and are responsible for moving water through the sponge until it is discharged via the exhalant opening (osculum). Environmental microorganisms are shown as green cells, whereas the dense community of symbiotic microorganisms that exists within the mesohyl is portrayed as red cells. Siliceous spicules provide additional structural support to many sponge species. (B) Multicolor double labeling of oligonucleotide probes for fluorescence in situ hybridization (DOPE-FISH) analysis of the sponge mesohyl using rRNA-targeted probes for specific sponge-associated microorganisms reveals the density of microbial cells. Poribacteria, yellow; Nitrospira, pink; Chloroflexi, cyan; Deltaproteobacteria, light green; Gammaproteobacteria, red; Archaea, blue. Larger dark-green areas are sponge autofluorescence. Photo courtesy of Michael Wagner, Department of Microbial Ecology, University of Vienna. (C) Scanning electron micrograph showing the density of microbial cells surrounding the sponge choanocyte chamber, where individual flagellated choanocyte cells are responsible for drawing water through the sponge and removing bacteria and other particles for subsequent digestion. Photo courtesy of Peta Clode, Centre for Microscopy, Characterisation and Analysis, University of Western Australia.

FIG 2

Working model of how sponge symbiosis has evolved toward microbial communities with distinct phylogeny but common functionality. Differently shaped bacteria represent distinct taxa, while different colors represent functions. As genetic exchange occurs within and between symbiont communities, their functions converge.