Viral ecogenomics across the Porifera

Cecília Pascelli,Timothy Ravasi,Emmanuelle Botté,Marija Kupresanin,Thomas Rattei,Patrick W Laffy,Miguel Lurgi,Nicole S Webster

doi:10.1186/s40168-020-00919-5

Abstract

BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea.ResultsViromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts.ConclusionsOur results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts.3fNQJtcyRuwttbnAh9LNMAVideo

Highlights

Marine sponges are an ecologically important component of the benthos, providing habitat for a diverse array of macro and microorganisms and mediating biogeochemical fluxes by filtering organic matter and facilitating the consumption and release of Pascelli et al Microbiome (2020) 8:144 sponges revealed enrichment of several microbial phyla including the Proteobacteria, Actinobacteria, Chloroflexi, Nitrospirae and Cyanobacteria, with Thaumarchaeota being the primary sponge-associated archaeal taxa [12]
auxiliary metabolic genes (AMGs) consist of a variety of host-derived genes with broad functional diversity that can contribute to the metabolism of their cellular hosts via processes including photosynthesis, nucleotide metabolism and nutrient cycling [25,26,27]
Bacteriophage groups dominated the sponge viromes, contigs taxonomically assigned to members of viral families that typically infect eukaryotes were prevalent, including representatives of the nucleocytoplasmic large DNA viruses (NCLDV)

Summary

Introduction

Marine sponges (phylum Porifera) are an ecologically important component of the benthos, providing habitat for a diverse array of macro and microorganisms and mediating biogeochemical fluxes by filtering organic matter and facilitating the consumption and release of Pascelli et al Microbiome (2020) 8:144 sponges revealed enrichment of several microbial phyla including the Proteobacteria (classes Alpha- and Gammaproteobacteria), Actinobacteria, Chloroflexi, Nitrospirae and Cyanobacteria, with Thaumarchaeota being the primary sponge-associated archaeal taxa [12]. The microbiome of cosmopolitan sponges, such as Carteriospongia foliascens and Xestospongia testudinaria, often shows biogeographic distinctions, likely responding to environmental variations [13, 14]. Sponges and their complex communities of microbial symbionts are a typical example of a ‘meta-organism’ or ‘holobiont’ [15, 16]. Despite the critical role of viruses in marine ecosystems, we are only just beginning to describe their diversity and contributions to host ecology This is important considering the recently recognised role of phages in manipulating their bacterial hosts due to alteration of host metabolism or hostmicrobial interactions via auxiliary metabolic genes (AMGs) or accessory genes.

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