Dataset Information

Impacts of a novel defensive symbiosis on the nematode host microbiome.

ABSTRACT:

Background

Bacteria adapted to live within animals can protect their hosts against harmful infections. Beyond antagonism with pathogens, a 'defensive' bacterial symbiont could engage in additional interactions with other colonizing micro-organisms. A single bacterium might thus have cascading ecological impacts on the whole microbiome that are rarely investigated. Here, we assess the role of a defensive symbiont as a driver of host-associated microbiota composition by using a bacterial species (Enterococcus faecalis) that was previously experimentally adapted to a nematode host model (Caenorhabditis elegans).

Results

An analysis of 16S rRNA data from C. elegans exposed to E. faecalis and subsequently reared in soil, reveal that symbiont adaptation to host environment or its protective potential had minimal impact on microbiota diversity. Whilst the abundance of Pseudomonas was higher in the microbiota of hosts with protective E.faecalis (and another protective species tested), a few other genera - including Serratia and Salinispora - were less abundant in hosts colonized by all E. faecalis strains. In addition, the protective effect of E. faecalis against virulent Staphylococcus aureus pathogens was maintained despite multi-species interactions within the microbiota.

Conclusions

Our results reveal the degree to which a new, evolving symbiont can colonise and maintain pathogen-resistance with minimal disruption to host microbiota diversity.

SUBMITTER: Dahan D

PROVIDER: S-EPMC7296725 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Publications

Impacts of a novel defensive symbiosis on the nematode host microbiome.

Dahan Dylan D Preston Gail M GM Sealey Jordan J King Kayla C KC

BMC microbiology 20200615 1

<h4>Background</h4>Bacteria adapted to live within animals can protect their hosts against harmful infections. Beyond antagonism with pathogens, a 'defensive' bacterial symbiont could engage in additional interactions with other colonizing micro-organisms. A single bacterium might thus have cascading ecological impacts on the whole microbiome that are rarely investigated. Here, we assess the role of a defensive symbiont as a driver of host-associated microbiota composition by using a bacterial s ...[more]

PMID: 32539750

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Project description:The symbiosis between cnidarians and dinoflagellates underpins the success of reef-building corals in otherwise nutrient-poor habitats. Alterations to symbiotic state can perturb metabolic homeostasis and thus alter the release of biogenic volatile organic compounds (BVOCs). While BVOCs can play important roles in metabolic regulation and signalling, how the symbiotic state affects BVOC output remains unexplored. We therefore characterised the suite of BVOCs that comprise the volatilome of the sea anemone Exaiptasia diaphana ('Aiptasia') when aposymbiotic and in symbiosis with either its native dinoflagellate symbiont Breviolum minutum or the non-native symbiont Durusdinium trenchii. In parallel, the bacterial community structure in these different symbiotic states was fully characterised to resolve the holobiont microbiome. Based on rRNA analyses, 147 unique amplicon sequence variants (ASVs) were observed across symbiotic states. Furthermore, the microbiomes were distinct across the different symbiotic states: bacteria in the family Vibrionaceae were the most abundant in aposymbiotic anemones; those in the family Crocinitomicaceae were the most abundant in anemones symbiotic with D. trenchii; and anemones symbiotic with B. minutum had the highest proportion of low-abundance ASVs. Across these different holobionts, 142 BVOCs were detected and classified into 17 groups based on their chemical structure, with BVOCs containing multiple functional groups being the most abundant. Isoprene was detected in higher abundance when anemones hosted their native symbiont, and dimethyl sulphide was detected in higher abundance in the volatilome of both Aiptasia-Symbiodiniaceae combinations relative to aposymbiotic anemones. The volatilomes of aposymbiotic anemones and anemones symbiotic with B. minutum were distinct, while the volatilome of anemones symbiotic with D. trenchii overlapped both of the others. Collectively, our results are consistent with previous reports that D. trenchii produces a metabolically sub-optimal symbiosis with Aiptasia, and add to our understanding of how symbiotic cnidarians, including corals, may respond to climate change should they acquire novel dinoflagellate partners.

Project description:BackgroundHost-microbe associations underlie many key processes of host development, immunity, and life history. Yet, none of the current research on the central model species Caenorhabditis elegans considers the worm's natural microbiome. Instead, almost all laboratories exclusively use the canonical strain N2 and derived mutants, maintained through routine bleach sterilization in monoxenic cultures with an E. coli strain as food. Here, we characterize for the first time the native microbiome of C. elegans and assess its influence on nematode life history characteristics.ResultsNematodes sampled directly from their native habitats carry a species-rich bacterial community, dominated by Proteobacteria such as Enterobacteriaceae and members of the genera Pseudomonas, Stenotrophomonas, Ochrobactrum, and Sphingomonas. The C. elegans microbiome is distinct from that of the worm's natural environment and the congeneric species C. remanei. Exposure to a derived experimental microbiome revealed that bacterial composition is influenced by host developmental stage and genotype. These experiments also showed that the microbes enhance host fitness under standard and also stressful conditions (e.g., high temperature and either low or high osmolarity). Taking advantage of the nematode's transparency, we further demonstrate that several Proteobacteria are able to enter the C. elegans gut and that an Ochrobactrum isolate even seems to be able to persist in the intestines under stressful conditions. Moreover, three Pseudomonas isolates produce an anti-fungal effect in vitro which we show can contribute to the worm's defense against fungal pathogens in vivo.ConclusionThis first systematic analysis of the nematode's native microbiome reveals a species-rich bacterial community to be associated with C. elegans, which is likely of central importance for our understanding of the worm's biology. The information acquired and the microbial isolates now available for experimental work establishes C. elegans as a tractable model for the in-depth dissection of host-microbiome interactions.

Dataset Information

Impacts of a novel defensive symbiosis on the nematode host microbiome.

Background

Results

Conclusions

Publications

Impacts of a novel defensive symbiosis on the nematode host microbiome.

Similar Datasets

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