Diversity, structure and convergent evolution of the global sponge microbiome.

Dirk Erpenbeck,Miguel Lurgi,Ute Hentschel,Carmen Astudillo‐García ,Andia Chaves‐Fonnegra ,Jack A Gilbert ,Rob Knight,Peter J Schupp,Rodrigo Costa,Laura Steindler,Susanna López‐Legentil ,Lucas Moitinho‐Silva ,Gail Ackermann,Cole G Easson ,Nicole S Webster,Torsten Thomas,Patrick M Erwin,Robert Thacker ,José M Montoya ,Julie B Olson,Jose V Lopez ,Michael W Taylor,Johannes R Björk ,Heidi M Luter

doi:10.1038/ncomms11870

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.

Highlights

Sponges are early-diverging metazoa renowned for establishing complex microbial symbioses
We identified five host species (Carteriospongia foliascens, Cliona delitrix, Ircinia oros, Ircinia variabilis and Sarcotragus fasciculatus) that fit this requirement and observed cores ranging in size from 7 to 20 operational taxonomic units (OTUs)
This global microbiome survey of an early-diverging metazoan phylum has revealed that sponges are a reservoir of exceptional microbial diversity and a major contributor to the total microbial diversity found in the world’s oceans

Summary

Introduction

Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Sponges can maintain highly diverse, yet specific symbiont communities, despite the constant influx of seawater microorganisms resulting from their filter-feeding activities[9] These symbioses are known to be at least partially underpinned by metabolic exchange between symbiont and host, including nitrogen cycling, CO2 fixation, secondary metabolite production, and uptake and conversion of dissolved organic matter[10,11,12]. Large-scale efforts, such as the Human Microbiome Project[15] and the Earth Microbiome Project[16], have standardized these technical aspects to reliably and consistently describe patterns of microbial diversity and composition These efforts have generated a large knowledge base for host-associated microbiomes of vertebrates, and especially humans, but equivalent data sets for invertebrates are missing. To define important aspects for the evolution of microbial symbiosis, a deeper understanding of symbiont communities in closely related host species within defined phylogenetic clades (for example, a single phylum) is required

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