Diversity, structure and convergent evolution of the global sponge microbiome

Abstract

Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Here we present a global Porifera microbiome survey, set out to establish the ecological and evolutionary drivers of these host–microbe interactions. We show that sponges are a reservoir of exceptional microbial diversity and major contributors to the total microbial diversity of the world's oceans. Little commonality in species composition or structure is evident across the phylum, although symbiont communities are characterized by specialists and generalists rather than opportunists. Core sponge microbiomes are stable and characterized by generalist symbionts exhibiting amensal and/or commensal interactions. Symbionts that are phylogenetically unique to sponges do not disproportionally contribute to the core microbiome, and host phylogeny impacts complexity rather than composition of the symbiont community. Our findings support a model of independent assembly and evolution in symbiont communities across the entire host phylum, with convergent forces resulting in analogous community organization and interactions.

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

“…We recovered a total of 169 OTUs for the combined sponge samples, and just 72 OTUs in adults alone, which is toward the lower end of the range (50-3820) currently known from adult marine sponge microbiomes (Thomas et al, 2016). We do note, however, that our study had relatively low sequencing depth, which could have compromised the recovery of rarer OTUs.…”

“…These observations raise question about the relative importance of animal hosts and the core symbionts themselves in regulating the assembly and maintenance of the total microbiome through the host life cycle, and in homeostasis of host functionality (Thomas et al, 2016). In an ontogenetic context, numerous studies have demonstrated vertical inheritance of putatively core symbionts during development of embryos and larvae, based on evidence from electron microscopy (see for example Ereskovsky et al, 2005;Oren et al, 2005;Maldonado, 2007;Schmitt et al, 2008) or sequencing of prokaryotic 16S rRNA gene amplicons (see for example Oren et al, 2005;Enticknap et al, 2006;Schmitt et al, 2007Schmitt et al, , 2008Sharp et al, 2007;Steger et al, 2008;Lee et al, 2009;Webster et al, 2010;Gloeckner et al, 2012).…”

“…Marine sponges are well-known for harboring phylogenetically-diverse bacterial communities as adults, often with a high degree of host-symbiont fidelity (Webster et al, , 2010Hentschel et al, 2002Hentschel et al, , 2003Hentschel et al, , 2012Taylor et al, 2004Taylor et al, , 2007Taylor et al, , 2013; Thomas et al, 2016). They provide compelling examples of how an animal's ecology comprises not only its external environment, but also its internally-housed microbes.…”

“…In particular, the bacterial symbionts that coexist with sponges provide their hosts with an extended multitude of metabolic functions that include nitrogen and phosphorous cycling, sulfur oxidation, carbon fixation, conversion of dissolved organic matter, and the production of secondary metabolites that serve the sponge in defense against predation (Taylor et al, 2007;Fan et al, 2012;Hentschel et al, 2012;de Goeij et al, 2013;Wilson et al, 2014;Zhang et al, 2015). The nature of bacterial community-specificity has been explored for multiple sponge species across a variety of phylogenetic, spatial, and temporal scales, revealing that adult sponge microbiomes generally are dominated by core symbionts that comprise a mix of both specialists and generalists (Webster et al, , 2010Schmitt et al, 2011;Erwin et al, 2012Erwin et al, , 2015Simister et al, 2012;Blanquer et al, 2013;Taylor et al, 2013;Easson and Thacker, 2014;Burgsdorf et al, 2015a;Thomas et al, 2016).…”

Draft Genomes Shed Light on the Dual Bacterial Symbiosis that Dominates the Microbiome of the Coral Reef Sponge Amphimedon queenslandica

“…The persistent presence of dominant bacterial phylotypes in several species of sponge indicates that many specific hostmicrobe associations are stable over time, likely facilitated by vertical inheritance (Taylor et al, 2007b;Erwin et al, 2012;Hentschel et al, 2012;Thomas et al, 2016). In non-sponge host-symbiont systems, the temporal stability of associations involving two or more unrelated bacterial symbionts (Takiya et al, 2006;Wu et al, 2006;Dubilier et al, 2008;Zimmermann et al, 2014) has been postulated to involve the use of different energy sources to reduce competition between the bacterial species (Duperron et al, 2006;Kleiner et al, 2012b).…”