Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster

Dobson, A.; Chaston, John M.; Newell, Peter D.; Donahue, Leanne R.; Hermann, Sara L.; Sannino, David R.; Westmiller, Stephanie; Wong, Adam C. N.; Clark, Andrew G.; Lazzaro, Brian P.; Douglas, Angela E.

doi:10.1038/ncomms7312

Cited by 89 publications

(91 citation statements)

References 51 publications

(55 reference statements)

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“…To quantify nutritional indices, triplicate samples of five flies each were homogenized in 125 l TET buffer (10 mM Tris [pH 8], 1 mM EDTA, 0.1% Triton X-100) with 1.4-mm ceramic beads (MP Biomedicals) in a FastPrep-24 instrument (MP Biomedicals) for 30 s. Twenty microliters of homogenate was frozen at Ϫ80°C, and 40 l was heat treated at 72°C for 15 min prior to freezing at Ϫ80°C. As described previously (12), commercial kits were used to assay protein content (catalog no. 500-0111; Bio-Rad) in directly frozen samples, and glucose and glycogen (catalog no.…”

Section: Methodsmentioning

confidence: 99%

“…Drosophila mutants (see Table S2B in the supplemental material) corresponding to genes containing or near GWA-identified SNPs and background stocks were obtained from the Bloomington Drosophila Stock Center and used directly in subsequent assays, following the experimental design of our previous work and others (12,(29)(30)(31). Gnotobiotic flies were raised with the five-species microbiota, as in the GWA, and A. tropicalis abundance and nutritional indices were determined.…”

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

“…The nutritional consequence of the microbiota is known to vary with the abundance and composition of the microorganisms (7,(10)(11)(12)(13). For example, comparison of nutritional phenotypes in Drosophila melanogaster raised with or without gut bacteria revealed that the microbiome can influence penetrance of host mutations (12). To the extent that the abundance and composition of the microbiota are determined by host genotype, the impact of animal genetic variation on nutrition may be mediated via effects on the microbiota, and host genotype-independent differences in the microbiota among individual animals may also make an appreciable contribution to the nutritional phenotype of animals (10).…”

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confidence: 99%

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Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

Chaston

Dobson

Newell

et al. 2016

Appl Environ Microbiol

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124

131

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A wealth of studies has demonstrated that resident microorganisms (microbiota) influence the pattern of nutrient allocation to animal protein and energy stores, but it is unclear how the effects of the microbiota interact with other determinants of animal nutrition, including animal genetic factors and diet. Here, we demonstrate that members of the gut microbiota in Drosophila melanogaster mediate the effect of certain animal genetic determinants on an important nutritional trait, triglyceride (lipid) content. Parallel analysis of the taxonomic composition of the associated bacterial community and host nutritional indices (glucose, glycogen, triglyceride, and protein contents) in multiple Drosophila genotypes revealed significant associations between the abundance of certain microbial taxa, especially Acetobacteraceae and Xanthamonadaceae, and host nutritional phenotype. By a genome-wide association study of Drosophila lines colonized with a defined microbiota, multiple host genes were statistically associated with the abundance of one bacterium, Acetobacter tropicalis. Experiments using mutant Drosophila validated the genetic association evidence and reveal that host genetic control of microbiota abundance affects the nutritional status of the flies. These data indicate that the abundance of the resident microbiota is influenced by host genotype, with consequent effects on nutrient allocation patterns, demonstrating that host genetic control of the microbiome contributes to the genotype-phenotype relationship of the animal host.T he recognition that animals are routinely colonized by dense and often diverse communities of microorganisms is driving a major reassessment of fundamental aspects of animal biology (1). Notably, there is accumulating evidence that resident microorganisms influence the nutritional status of animals in multiple ways, including competition for ingested nutrients, providing supplementary nutrients (e.g., vitamins, short-chain fatty acids, essential amino acids), and by modulating the nutrient signaling circuits that regulate nutrient allocation (2-5). These discoveries demonstrate the inadequacy of traditional explanations of animal nutrition in terms of nutritional inputs (amount and composition of food ingested) and outputs (animal nutritional demand for activity, growth, reproduction, etc.) and highlight our ignorance of how microbial effects on animal nutrition interact with other factors, especially animal genotype (6-10).The focus of this study is the impact of interactions between the gut microbiota and host genotype on animal nutrition. The nutritional consequence of the microbiota is known to vary with the abundance and composition of the microorganisms (7, 10-13). For example, comparison of nutritional phenotypes in Drosophila melanogaster raised with or without gut bacteria revealed that the microbiome can influence penetrance of host mutations (12). To the extent that the abundance and composition of the microbiota are determined by host genotype, the impact of animal genetic ...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

Chaston

Dobson

Newell

et al. 2016

Appl Environ Microbiol

Self Cite

124

131

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“…Accordingly, there could be genetic or maternal factors that affect the extent to which an individual is sensitive to temperature and bacteria. Strong genetic variation in responses to microbiota has been observed in Drosophila nutrition-related traits (Dobson et al, 2015). The outcomes observed here resemble environmental canalization (Flatt, 2005), with bacteria in some way contributing to the homeostatic mechanism that stabilizes the phenotypic outcome under the elevated temperature condition.…”

Section: Discussionmentioning

confidence: 52%

Temperature-dependent benefits of bacterial exposure in embryonic development of Daphnia magna resting eggs

Mushegian

Burcklen

Schär

et al. 2016

Journal of Experimental Biology

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The environments in which animals develop and evolve are profoundly shaped by bacteria, which affect animals both indirectly through their role in biogeochemical processes and directly through antagonistic or beneficial interactions. The outcomes of these activities can differ according to environmental context. In a series of laboratory experiments with diapausing eggs of the water flea Daphnia magna, we manipulated two environmental parameters, temperature and presence of bacteria, and examined their effect on development. At elevated temperatures (≥26°C), resting eggs developing without live bacteria had reduced hatching success and correspondingly higher rates of severe morphological abnormalities compared with eggs with bacteria in their environment. The beneficial effect of bacteria was strongly reduced at 20°C. Neither temperature nor the presence of bacteria affected directly developing parthenogenetic eggs. The mechanistic basis of this effect of bacteria on development is unclear, but these results highlight the complex interplay of biotic and abiotic factors influencing animal development after diapause.

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Diet, Gut Microbes and Host Mate Choice

2018

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All organisms live in close association with microbes. However, not all such associations are meaningful in an evolutionary context. Current debate concerns whether hosts and microbes are best described as communities of individuals or as holobionts (selective units of hosts plus their microbes). Recent reports that assortative mating of hosts by diet can be mediated by commensal gut microbes have attracted interest as a potential route to host reproductive isolation (RI). Here, the authors discuss logical problems with this line of argument. The authors briefly review how microbes can affect host mating preferences and evaluate recent findings from fruitflies. Endosymbionts can potentially influence host RI given stable and recurrent co‐association of hosts and microbes over evolutionary time. However, observations of co‐occurrence of microbes and hosts are ripe for misinterpretation and such associations will rarely represent a meaningful holobiont. A framework in which hosts and their microbes are independent evolutionary units provides the only satisfactory explanation for the observed range of effects and associations.

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Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster

Cited by 89 publications

References 51 publications

Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

Temperature-dependent benefits of bacterial exposure in embryonic development of Daphnia magna resting eggs

Diet, Gut Microbes and Host Mate Choice

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