Dataset Information

Uncovering the hidden marine sponge microbiome by applying a multi-primer approach.

ABSTRACT: Marine sponges (phylum Porifera) are hosts to microorganisms that make up to 40-60% of the mesohyl volume. The challenge is to characterise this microbial diversity more comprehensively. To accomplish this, a new method was for the first time proposed to obtain sequence coverage of all the variable regions of the 16S rRNA gene to analyze the amplicon-based microbiomes of four representative sponge species belonging to different orders. The five primer sets targeting nine variable regions of the 16S rRNA gene revealed a significant increase in microbiome coverage of 29.5% of phylum level OTUs and 35.5% class level OTUs compared to the community revealed by the commonly used V4 region-specific primer set alone. Among the resulting OTUs, 52.6% and 61.3% were unaffiliated, including candidate OTUs, at the phylum and class levels, respectively, which demonstrated a substantially superior performance in uncovering taxonomic 'blind spots'. Overall, a more complete sponge microbiome profile was achieved by this multi-primer approach, given the significant improvement of microbial taxonomic coverage and the enhanced capacity to uncover novel microbial taxa. This multi-primer approach represents a fundamental and practical change from the conventional single primer set amplicon-based microbiome approach, and can be broadly applicable to other microbiome studies.

SUBMITTER: Yang Q

PROVIDER: S-EPMC6470215 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Uncovering the hidden marine sponge microbiome by applying a multi-primer approach.

Yang Qi Q Franco Christopher M M CMM Zhang Wei W

Scientific reports 20190417 1

Marine sponges (phylum Porifera) are hosts to microorganisms that make up to 40-60% of the mesohyl volume. The challenge is to characterise this microbial diversity more comprehensively. To accomplish this, a new method was for the first time proposed to obtain sequence coverage of all the variable regions of the 16S rRNA gene to analyze the amplicon-based microbiomes of four representative sponge species belonging to different orders. The five primer sets targeting nine variable regions of the ...[more]

PMID: 30996336

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Project description:BackgroundPoriferans (sponges) are highly adaptable organisms that can thrive in diverse marine and freshwater environments due, in part, to their close associations with internal microbial communities. This sponge microbiome can be acquired from the surrounding environment (horizontal acquisition) or obtained from the parents during the reproductive process through a variety of mechanisms (vertical transfer), typically resulting in the presence of symbiotic microbes throughout all stages of sponge development. How and to what extent the different components of the microbiome are transferred to the developmental stages remain poorly understood. Here, we investigated the microbiome composition of a common, low-microbial-abundance, Atlantic-Mediterranean sponge, Crambe crambe, throughout its ontogeny, including adult individuals, brooded larvae, lecithotrophic free-swimming larvae, newly settled juveniles still lacking osculum, and juveniles with a functional osculum for filter feeding.ResultsUsing 16S rRNA gene analysis, we detected distinct microbiome compositions in each ontogenetic stage, with variations in composition, relative abundance, and diversity of microbial species. However, a particular dominant symbiont, Candidatus Beroebacter blanensis, previously described as the main symbiont of C. crambe, consistently occurred throughout all stages, an omnipresence that suggests vertical transmission from parents to offspring. This symbiont fluctuated in relative abundance across developmental stages, with pronounced prevalence in lecithotrophic stages. A major shift in microbial composition occurred as new settlers completed osculum formation and acquired filter-feeding capacity. Candidatus Beroebacter blanensis decreased significatively at this point. Microbial diversity peaked in filter-feeding stages, contrasting with the lower diversity of lecithotrophic stages. Furthermore, individual specific transmission patterns were detected, with greater microbial similarity between larvae and their respective parents compared to non-parental conspecifics.ConclusionsThese findings suggest a putative vertical transmission of the dominant symbiont, which could provide some metabolic advantage to non-filtering developmental stages of C. crambe. The increase in microbiome diversity with the onset of filter-feeding stages likely reflects enhanced interaction with environmental microbes, facilitating horizontal transmission. Conversely, lower microbiome diversity in lecithotrophic stages, prior to filter feeding, suggests incomplete symbiont transfer or potential symbiont digestion. This research provides novel information on the dynamics of the microbiome through sponge ontogeny, on the strategies for symbiont acquisition at each ontogenetic stage, and on the potential importance of symbionts during larval development.

Dataset Information

Uncovering the hidden marine sponge microbiome by applying a multi-primer approach.

Publications

Uncovering the hidden marine sponge microbiome by applying a multi-primer approach.

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