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Influence of bacteria on the maintenance of a yeast during Drosophila melanogaster metamorphosis.

ABSTRACT: Interactions between microorganisms associated with metazoan hosts are emerging as key features of symbiotic systems. Little is known about the role of such interactions on the maintenance of host-microorganism association throughout the host's life cycle. We studied the influence of extracellular bacteria on the maintenance of a wild isolate of the yeast Saccharomyces cerevisiae through metamorphosis of the fly Drosophila melanogaster reared in fruit. Yeasts maintained through metamorphosis only when larvae were associated with extracellular bacteria isolated from D. melanogaster faeces. One of these isolates, an Enterobacteriaceae, favoured yeast maintenance during metamorphosis. Such bacterial influence on host-yeast association may have consequences for the ecology and evolution of insect-yeast-bacteria symbioses in the wild.

SUBMITTER: Guilhot R

PROVIDER: S-EPMC8489055 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Influence of bacteria on the maintenance of a yeast during Drosophila melanogaster metamorphosis.

Guilhot Robin R Rombaut Antoine A Xuéreb Anne A Howell Kate K Fellous Simon S

Animal microbiome 20211003 1

Interactions between microorganisms associated with metazoan hosts are emerging as key features of symbiotic systems. Little is known about the role of such interactions on the maintenance of host-microorganism association throughout the host's life cycle. We studied the influence of extracellular bacteria on the maintenance of a wild isolate of the yeast Saccharomyces cerevisiae through metamorphosis of the fly Drosophila melanogaster reared in fruit. Yeasts maintained through metamorphosis onl ...[more]

PMID: 34602098

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Project description:As organisms age the environment fluctuates, exerting differential selection across ontogeny. In particular, highly seasonal environments expose life stages to often drastically different thermal environments. This developmental variation is particularly striking in organisms with complex life cycles, wherein life history stages also exhibit distinct morphologies, physiologies, and behaviors. Genes acting pleiotropically on thermal responses may produce genetic correlations across ontogeny, constraining the independent evolution of each life stage to their respective thermal environments. To investigate whether developmental genetic correlations constrain the evolution thermal hardiness of the fly Drosophila melanogaster, we applied quantitative genetic analyses to cold hardiness measured in both larvae and adults from isogenic lines of the Drosophila Genetic Reference Panel (DGRP), using survival at stressful low temperatures as the phenotypic metric. Using full genome resequencing data for the DGRP, we also implemented genome-wide association (GWA) analysis using Bayesian Sparse Linear Mixed Models (BSLMMs) to estimate associations between naturally segregating variation and cold hardiness for both larvae and adults. Quantitative genetic analyses revealed no significant genetic correlation for cold hardiness between life stages, suggesting complete genetic decoupling of thermal hardiness across the metamorphic boundary. Both quantitative genetic and GWA analyses suggested that polygenic variation underlies cold hardiness in both stages, and that associated loci largely affected one stage or the other, but not both. However, reciprocal enrichment tests and correlations between BSLMM parameters for each life stage support some shared physiological mechanisms that may reflect common cellular thermal response pathways. Overall, these results suggest no developmental genetic constraints on cold hardiness across metamorphosis in D. melanogaster, an important consideration in evolutionary models of responses to changing climates. Genetic correlations for environmental sensitivity across ontogeny remains largely unexplored in other organisms, thus assessing the generality of genetic decoupling will require further quantitative or population genetic analysis in additional species.

Project description:Animal-associated microorganisms (microbiota) dramatically influence the nutritional and physiological traits of their hosts. To expand our understanding of such influences, we predicted bacterial genes that influence a quantitative animal trait by a comparative genomic approach, and we extended these predictions via mutant analysis. We focused on Drosophila melanogaster starvation resistance (SR). We first confirmed that D. melanogaster SR responds to the microbiota by demonstrating that bacterium-free flies have greater SR than flies bearing a standard 5-species microbial community, and we extended this analysis by revealing the species-specific influences of 38 genome-sequenced bacterial species on D. melanogaster SR. A subsequent metagenome-wide association analysis predicted bacterial genes with potential influence on D. melanogaster SR, among which were significant enrichments in bacterial genes for the metabolism of sulfur-containing amino acids and B vitamins. Dietary supplementation experiments established that the addition of methionine, but not B vitamins, to the diets significantly lowered D. melanogaster SR in a way that was additive, but not interactive, with the microbiota. A direct role for bacterial methionine metabolism genes in D. melanogaster SR was subsequently confirmed by analysis of flies that were reared individually with distinct methionine cycle Escherichia coli mutants. The correlated responses of D. melanogaster SR to bacterial methionine metabolism mutants and dietary modification are consistent with the established finding that bacteria can influence fly phenotypes through dietary modification, although we do not provide explicit evidence of this conclusion. Taken together, this work reveals that D. melanogaster SR is a microbiota-responsive trait, and specific bacterial genes underlie these influences.IMPORTANCE Extending descriptive studies of animal-associated microorganisms (microbiota) to define causal mechanistic bases for their influence on animal traits is an emerging imperative. In this study, we reveal that D. melanogaster starvation resistance (SR), a model quantitative trait in animal genetics, responds to the presence and identity of the microbiota. Using a predictive analysis, we reveal that the amino acid methionine has a key influence on D. melanogaster SR and show that bacterial methionine metabolism mutants alter normal patterns of SR in flies bearing the bacteria. Our data further suggest that these effects are additive, and we propose the untested hypothesis that, similar to bacterial effects on fruit fly triacylglyceride deposition, the bacterial influence may be through dietary modification. Together, these findings expand our understanding of the bacterial genetic basis for influence on a nutritionally relevant trait of a model animal host.

Dataset Information

Influence of bacteria on the maintenance of a yeast during Drosophila melanogaster metamorphosis.

Publications

Influence of bacteria on the maintenance of a yeast during Drosophila melanogaster metamorphosis.

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