Prokaryotic, Fungal, and Unicellular Eukaryotic Core Communities Across Three Sympatric Marine Sponges From the Southwestern Atlantic Coast Are Dominated Largely by Deterministic Assemblage Processes

Abstract

Marine sponges are known to harbor a diverse and complex microbiota; however, a vast majority of surveys have been investigating the prokaryotic communities in the north hemisphere and Australia. In addition, the mechanisms of microbial community assembly are poorly understood in this pivotal player of the ecosystem. Thus, this survey addressed the holobiome of the sponge species in the São Paulo region (Brazil) for the first time and investigated the contribution of neutral and niche processes of prokaryotic, fungal, and unicellular eukaryotic assemblage in three sympatric species Aplysina caissara, Aplysina fulva, and Tedania ignis along with environmental samples. The compositions of the holobiome associated with the sponges and detected in environmental samples were strikingly different. Remarkably, between 47 and 88% of the assigned operational taxonomic units (OTUs) were specifically associated with sponge species. Moreover, around 77, 69, and 53% of the unclassified OTUs from prokaryotic, fungal, and unicellular eukaryotic communities, respectively, showed less than 97% similarity with well-known databases, suggesting that sponges from the southwestern Atlantic coast are an important source of microbial novelty. These values are even higher, around 80 and 61% of the unclassified OTUs, when excluding low abundance samples from fungal and unicellular eukaryotic datasets, respectively. Host species were the major driver shaping the sponge-associated microbial community. Deterministic processes were primarily responsible for the assembly of microbial communities in all sponge species, while neutral processes of prokaryotic and fungal community assembly were also detected in the sympatric A. caissara and T. ignis replicates, respectively. Most of the species-rich sponge-associated lineages from this region are also found in the Northern seas and many of them might play essential roles in the symbioses, such as biosynthesis of secondary metabolites that exhibit antimicrobial and antiviral activities, as well as provide protection against host predation. Overall, in this study the microbiota was assembled by interactions with the host sponge in a deterministic-based manner; closely related sponge species shared a strong phylogenetic signal in their associated prokaryotic and fungal community traits and Brazilian sponges were a reservoir of novel microbial species.