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.

Depth effect on the prokaryotic community assemblage associated with sponges from different rocky reefs

“…As reported by Hardoim et al (2021) , prokaryotic communities associated with A. caissara and A. fulva were very similar among these two species and dominated by Chloroflexi, Proteobacteria, Crenarchaeota, and Acidobacteria. In contrast, in this study, Chloroflexi was only represented with a high relative abundance in 2-m Aplysina sp samples and Crenarchaeota did not represent an important component in any of the samples.…”

“…In contrast, in this study, Chloroflexi was only represented with a high relative abundance in 2-m Aplysina sp samples and Crenarchaeota did not represent an important component in any of the samples. However, these same authors ( Hardoim et al, 2021 ) mentioned that community composition was largely different for Aplysina species. For instance, the most abundant phyla encountered in A. fulva, A. cauliformis, A. archeri, A. cavenicola , and A. aerophoba sampled in seven distinct sites were assigned to Proteobacteria, Chloroflexi, unclassified bacteria, Acidobacteria, and Actinobacteria ( Thomas et al, 2016 ), or A. fulva collected in Brazil with the community dominated by Cyanobacteria, Proteobacteria, and Chloroflexi ( Hardoim et al, 2009 ), which coincides with the phyla with the highest relative abundance in the 2-m Aplysina sp samples collected at Punta Arena BCS.…”

Tracing RNA viruses associated with Nudibranchia gastropods

“…Differently from environmental metagenomics, the study of organism-associated biomes (holobiomes) can provide an overview of organism–organism associations ( Hardoim et al, 2021 ) together with a snapshot of local viromes, as shown for the human virome ( Garmaeva et al, 2019 ; Koonin, Dolja & Krupovic, 2021 ). Perhaps this approach is suffering less from limitations relating to proper host assignation, although additional challenges should be considered.…”

Interações entre eucariontes unicelulares e Porifera: função fisiológica e aplicações biotecnológicas de Labyrinthulomycetes associados

“…Also, only Rodriguez-Marconi and collaborators included seawater samples in their experimental design. The approaches used in these studies directly impacts the understanding of the microeukaryotic community associated with these sponges, making comparisons difficult (Hardoim et al 2021). On the other side, these investigations have gathered further evidence that, just as occurs in the bacterial and archaeal communities, the protists associated with sponges can also possess host specificity.…”

“…Interestingly, in the sponge Acanthostylotella cornuta it was observed a high relative abundance of Metamonada, basal heterotrophic eukaryotes that are usually grazers of bacterial communities, but with parasitic representatives . In a more recent study (Hardoim et al 2021), again the question of microeukaryome specificity was raised. Although the previous studies are not directly comparable given methodological divergences, the investigation of the microeukaryotic community of three sympatric species from South America indicates that the hosts directly act on the selection of microorganisms.…”