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Persistence of a Core Microbiome Through the Ontogeny of a Multi-Host Parasite.

ABSTRACT: Animal microbiomes influence their development, behavior and interactions with other organisms. Parasitic metazoans also harbor microbial communities; although they are likely to modulate host-parasite interactions, little is known about parasite microbiomes. The persistence of microbial communities throughout the life of a parasite is particularly challenging for helminths with complex life cycles. These parasites undergo major morphological changes during their life, and parasitize host species that are immunologically, physiologically, and phylogenetically very different. Here, using 16S amplicon sequencing, we characterize the microbiome of the trematode Coitocaecum parvum across four of its life stages: sporocysts, metacercariae and adults inhabiting (respectively) snails, crustaceans and fish, as well as free-living cercariae. Our results demonstrate that, at each life stage, the parasite possesses a phylogenetically diverse microbiome, distinct from that of its hosts or the external environment. The parasite's microbiome comprises bacterial taxa specific to each life stage in different hosts, as well as a small core set of taxa that persists across the parasite's whole life. The apparent existence of an ontogenetically and vertically transmitted core microbiome is supported by the findings that the diversity and taxonomic composition of the microbiome does not vary significantly among life stages, and that the main source of microbial taxa at any life stage is the previous life stage. Our results suggest that microbes are an integrated component of the trematode, possibly shaping its phenotype and host-parasite interactions.

SUBMITTER: Jorge F

PROVIDER: S-EPMC7248275 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Persistence of a Core Microbiome Through the Ontogeny of a Multi-Host Parasite.

Jorge Fátima F Dheilly Nolwenn M NM Poulin Robert R

Frontiers in microbiology 20200519

Animal microbiomes influence their development, behavior and interactions with other organisms. Parasitic metazoans also harbor microbial communities; although they are likely to modulate host-parasite interactions, little is known about parasite microbiomes. The persistence of microbial communities throughout the life of a parasite is particularly challenging for helminths with complex life cycles. These parasites undergo major morphological changes during their life, and parasitize host specie ...[more]

PMID: 32508779

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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

Persistence of a Core Microbiome Through the Ontogeny of a Multi-Host Parasite.

Publications

Persistence of a Core Microbiome Through the Ontogeny of a Multi-Host Parasite.

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