Microbiome-by-ethanol interactions impact Drosophila melanogaster fitness, physiology, and behavior

Chandler, James Angus; Innocent, Lina Victoria; Martinez, Daniel Jonathan; Huang, Isaac Li; Yang, Jane L; Ludington, William B.

doi:10.1016/j.isci.2022.104000

Cited by 9 publications

(5 citation statements)

References 116 publications

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“…S4 ]. One of the crop’s most highly expressed genes, Alcohol dehydrogenase ( Adh ), plays a protective role when adults feed on fermenting fruit ( 53 ). In the human esophagus, alcohol dehydrogenase 7 is highly expressed and differentially up-regulated compared to other tissues ( 44 ), suggesting a conserved foregut function.…”

Section: Resultsmentioning

confidence: 99%

Cellular and molecular organization of the Drosophila foregut

Zhu,

Ludington,

Spradling

2024

Proc. Natl. Acad. Sci. U.S.A.

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The animal foregut is the first tissue to encounter ingested food, bacteria, and viruses. We characterized the adult Drosophila foregut using transcriptomics to better understand how it triages consumed items for digestion or immune response and manages resources. Cell types were assigned and validated using GFP-tagged and Gal4 reporter lines. Foregut-associated neuroendocrine cells play a major integrative role by coordinating gut activity with nutrition, the microbiome, and circadian cycles; some express clock genes. Multiple epithelial cell types comprise the proventriculus, the central foregut organ that secretes the peritrophic matrix (PM) lining the gut. Analyzing cell types synthesizing individual PM layers revealed abundant mucin production close to enterocytes, similar to the mammalian intestinal mucosa. The esophagus and salivary gland express secreted proteins likely to line the esophageal surface, some of which may generate a foregut commensal niche housing specific gut microbiome species. Overall, our results imply that the foregut coordinates dietary sensing, hormonal regulation, and immunity in a manner that has been conserved during animal evolution.

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Section: Resultsmentioning

confidence: 99%

Cellular and molecular organization of the Drosophila foregut

Zhu,

Ludington,

Spradling

2024

Proc. Natl. Acad. Sci. U.S.A.

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“…Host-microbe associations are prevalent throughout the Metazoa. While many of these associations are transient, non-specific and of little consequence to the host, many others are stable, with a high degree of specificity for both the host and microbe, and these typically have a valuable contribution to the fitness of both host and microbe [86][87][88]. Understanding how these specific relationships form in development and over evolutionary time is of importance to animal health and the ecological health of our planet.…”

Section: Discussionmentioning

confidence: 99%

The importance of host physical niches for the stability of gut microbiome composition

Ludington

2024

Phil. Trans. R. Soc. B

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Gut bacteria are prevalent throughout the Metazoa and form complex microbial communities associated with food breakdown, nutrient provision and disease prevention. How hosts acquire and maintain a consistent bacterial flora remains mysterious even in the best-studied animals, including humans, mice, fishes, squid, bugs, worms and flies. This essay visits the evidence that hosts have co-evolved relationships with specific bacteria and that some of these relationships are supported by specialized physical niches that select, sequester and maintain microbial symbionts. Genetics approaches could uncover the mechanisms for recruiting and maintaining the stable and consistent members of the microbiome. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’.

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“…The commonly-used preservative nipagin (methylparaben) affects the density of Acetobacter (18), which may alter growth in fly food, and thereby modify physiological impact. Also nipagin is dissolved in ethanol, which interacts with variation in the microbiota (19). Acid preservatives are also used, which may modulate fly function though effects on the microbiota (e.g.…”

Section: Observationmentioning

confidence: 99%

Outcome ofDrosophilamicrobiota manipulation depends on dietary preservative formula and batch variation in dietary yeast

Sannino

Dobson

2023

Preprint

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Gut microbiota are fundamentally important for healthy function in their animal hosts. The flyDrosophila melanogasteris a powerful system for understanding the underlying host/microbe interactions, with modulation of the microbiota inducing phenotypic changes that are conserved across animal taxa. The context-dependence of these responses has not been explored systematically, which may confound repeatability. Here we show that the microbiota's impact on fly triacylglyceride (TAG) levels - a commonly-measured metabolic index - depends on factors in fly media that are rarely considered or controlled, and are not standardized among laboratories: media preservative formula, yeast batch, and the interactive effect of their combinatorial variation. In studies of conventional, axenic and gnotobiotic flies, we found that microbial impacts were apparent only on specific yeast-by-preservative conditions, with TAG levels determined by a tripartite interaction of the three experimental factors. When comparing axenic and conventional flies, we found that preservatives rather than microbiota status was the main driver of variance in host TAG, and certain yeast-preservative combinations reversed microbiota effects on TAG levels. Further, comparisons between TAG levels of axenic flies and those associated withAcetobacter pomorumorLevilactobacillus brevisdetermined that preservatives, microbiota status, and their interaction were the major drivers of TAG variation. Our results suggest that the microbiota shapes the host TAG response in a manner dependent on the combination of the dietary factors of preservative formulation and yeast batch, with implications for repeatability, interpretation, and optimal experimental standards.

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Microbiome-by-ethanol interactions impact Drosophila melanogaster fitness, physiology, and behavior

Cited by 9 publications

References 116 publications

Cellular and molecular organization of the Drosophila foregut

Cellular and molecular organization of the Drosophila foregut

The importance of host physical niches for the stability of gut microbiome composition

Outcome ofDrosophilamicrobiota manipulation depends on dietary preservative formula and batch variation in dietary yeast

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