Prokaryotic, Fungal, and Unicellular 1 Eukaryotic Core Communities across Three Sympatric Marine Sponges from the Southwestern Atlantic Coast are Dominated largely by Deterministic Assemblage Processes

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 Sao 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 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 was 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 strong phylogenetic signal in their associated prokaryotic and fungal community traits and Brazilian sponges were a reservoir of novel microbial species.

海洋海绵已知其宿主共生有多样且复杂的微生物组；但绝大多数相关调研仅聚焦于北半球及澳大利亚海域海绵的原核生物群落。而作为海洋生态系统中的关键类群，海绵的微生物群落构建机制至今仍未得到充分解析。有鉴于此，本研究首次针对巴西圣保罗海域的海绵物种全微生物组（holobiome）展开系统调研，并以三种同域分布海绵——Aplysina caissara、Aplysina fulva及Tedania ignis为研究对象，结合同期环境样本，探究了原核生物、真菌及单细胞真核生物群落构建的中性过程与生态位过程的相对贡献。海绵共生全微生物组与环境样本的微生物群落组成差异显著。值得注意的是，47%~88%的已注释操作分类单元（Operational Taxonomic Units，OTU）仅与单一海绵物种特异性关联。此外，原核生物、真菌及单细胞真核生物群落中未分类OTU的占比分别约为77%、69%和53%，这些OTU与主流公共数据库中的序列相似性均低于97%，这表明西南大西洋海域的海绵是微生物新物种的重要资源库。若分别剔除真菌与单细胞真核生物数据集内的低丰度样本，上述未分类OTU的占比将进一步提升至约80%与61%。宿主物种是调控海绵共生微生物群落结构的首要驱动因子。所有海绵物种的微生物群落构建均以确定性过程为主导；而在同域分布的A. caissara与T. ignis的生物学重复样本中，分别检测到了原核生物与真菌群落构建的中性过程。本区域海绵共生的多数物种丰富类群也在北半球海域被检出，其中许多类群可能在共生关系中发挥关键功能：例如合成具有抗菌、抗病毒活性的次生代谢产物，以及为宿主提供捕食防御保护。综上，本研究表明海绵微生物组通过与宿主的相互作用以确定性方式完成群落构建；亲缘关系相近的海绵物种，其共生原核生物与真菌群落特征具有显著的系统发育信号；巴西海域海绵亦是微生物新物种的重要储藏库。