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On the way to specificity - Microbiome reflects sponge genetic cluster primarily in highly structured populations.

ABSTRACT: Most animals, including sponges (Porifera), have species-specific microbiomes. Which genetic or environmental factors play major roles structuring the microbial community at the intraspecific level in sponges is, however, largely unknown. In this study, we tested whether geographic location or genetic structure of conspecific sponges influences their microbial assembly. For that, we used three sponge species with different rates of gene flow, and collected samples along their entire distribution range (two from the Mediterranean and one from the Southern Ocean) yielding a total of 393 samples. These three sponge species have been previously analysed by microsatellites or single nucleotide polymorphisms, and here we investigate their microbiomes by amplicon sequencing of the microbial 16S rRNA gene. The sponge Petrosia ficiformis, with highly isolated populations (low gene flow), showed a stronger influence of the host genetic distance on the microbial composition than the spatial distance. Host-specificity was therefore detected at the genotypic level, with individuals belonging to the same host genetic cluster harbouring more similar microbiomes than distant ones. On the contrary, the microbiome of Ircinia fasciculata and Dendrilla antarctica - both with weak population structure (high gene flow) - seemed influenced by location rather than by host genetic distance. Our results suggest that in sponge species with high population structure, the host genetic cluster influence the microbial community more than the geographic location.

SUBMITTER: Diez-Vives C

PROVIDER: S-EPMC7756592 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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On the way to specificity - Microbiome reflects sponge genetic cluster primarily in highly structured populations.

Díez-Vives Cristina C Taboada Sergi S Leiva Carlos C Busch Kathrin K Hentschel Ute U Riesgo Ana A

Molecular ecology 20200930 22

Most animals, including sponges (Porifera), have species-specific microbiomes. Which genetic or environmental factors play major roles structuring the microbial community at the intraspecific level in sponges is, however, largely unknown. In this study, we tested whether geographic location or genetic structure of conspecific sponges influences their microbial assembly. For that, we used three sponge species with different rates of gene flow, and collected samples along their entire distribution ...[more]

PMID: 32931063

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Project description:BACKGROUND: Non-random patterns of genetic variation exist among individuals in a population owing to a variety of evolutionary factors. Therefore, populations are structured into genetically distinct subpopulations. As genotypic datasets become ever larger, it is increasingly difficult to correctly estimate the number of subpopulations and assign individuals to them. The computationally efficient non-parametric, chiefly Principal Components Analysis (PCA)-based methods are thus becoming increasingly relied upon for population structure analysis. Current PCA-based methods can accurately detect structure; however, the accuracy in resolving subpopulations and assigning individuals to them is wanting. When subpopulations are closely related to one another, they overlap in PCA space and appear as a conglomerate. This problem is exacerbated when some subpopulations in the dataset are genetically far removed from others. We propose a novel PCA-based framework which addresses this shortcoming. RESULTS: A novel population structure analysis algorithm called iterative pruning PCA (ipPCA) was developed which assigns individuals to subpopulations and infers the total number of subpopulations present. Genotypic data from simulated and real population datasets with different degrees of structure were analyzed. For datasets with simple structures, the subpopulation assignments of individuals made by ipPCA were largely consistent with the STRUCTURE, BAPS and AWclust algorithms. On the other hand, highly structured populations containing many closely related subpopulations could be accurately resolved only by ipPCA, and not by other methods. CONCLUSION: The algorithm is computationally efficient and not constrained by the dataset complexity. This systematic subpopulation assignment approach removes the need for prior population labels, which could be advantageous when cryptic stratification is encountered in datasets containing individuals otherwise assumed to belong to a homogenous population.

Project description:Sponge microbiomes are typically profiled by analyzing the community DNA of whole tissues, which does not distinguish the taxa residing within sponge cells from extracellular microbes. To uncover the endosymbiotic microbiome, we separated the sponge cells to enrich the intracellular microbes. The intracellular bacterial community of sponge Euryspongia arenaria was initially assessed by amplicon sequencing, which indicated that it hosts three unique phyla not found in the extracellular and bulk tissue microbiomes. These three phyla account for 66% of the taxonomically known genera in the intracellular microbiome. The shotgun metagenomic analysis extended the taxonomic coverage to viruses and eukaryotes, revealing the most abundant signature taxa specific to the intracellular microbiome. Functional KEGG pathway annotation demonstrated that the endosymbiotic microbiome hosted the greatest number of unique gene orthologs. The pathway profiles distinguished the intra- and extracellular microbiomes from the tissue and seawater microbiomes. Carbohydrate-active enzyme analysis further discriminated each microbiome based on their representative and dominant enzyme families. One pathway involved in digestion system and family esterase had a consistently higher level in intracellular microbiome and could statistically differentiate the intracellular microbiome from the others, suggesting that triacylglycerol lipases could be the key functional component peculiar to the endosymbionts. The identified higher abundance of lipase-related eggNOG categories further supported the lipid-hydrolyzing metabolism of endosymbiotic microbiota. Pseudomonas members, reported as lipase-producing bacteria, were only in the endosymbiotic microbiome, meanwhile Pseudomonas also showed a greater abundance intracellularly. Our study aided a comprehensive sponge microbiome that demonstrated the taxonomic and functional specificity of endosymbiotic microbiota. IMPORTANCE Sponges host abundant microbial symbionts that can produce an impressive number of novel bioactive metabolites. However, knowledge on intracellular (endosymbiotic) microbiota is scarce. We characterize the composition and function of the endosymbiotic microbiome by separation of sponge cells and enrichment of intracellular microbes. We uncover a noteworthy number of taxa exclusively in the endosymbiotic microbiome. We unlock the unique pathways and enzymes of endosymbiotic taxa. This study achieves a more comprehensive sponge microbial community profile, which demonstrates the structural and functional specificity of the endosymbiotic microbiome. Our findings not only open the possibility to reveal the low abundant and the likely missed microbiota when directly sequencing the sponge bulk tissues, but also warrant future in-depth exploration within single sponge cells.

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On the way to specificity - Microbiome reflects sponge genetic cluster primarily in highly structured populations.

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On the way to specificity - Microbiome reflects sponge genetic cluster primarily in highly structured populations.

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