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Drosophila and Commensal Bacteria Synergistically Compete with Opportunistic Pathogens at Bulk and Single-Cell Resolutions [scRNA-seq]

ABSTRACT: A challenging task to reveal health and disease-associated microbiome signatures is to disentangle regulatory networks of microbes among themselves and with their host. Using the integrated Drosophila-commensal-pathogen model system, we here reported that Drosophila and commensal bacterium L. plantarum cooperated to compete with the opportunistic pathogen S. marcescens. At first, we found that Drosophila larvae and L. plantarum efficiently antagonized S. marcescens in the coexisting niche by suppressing population size and altering metabolism. Drosophila and L. plantarum synergistically enforced the transcriptional reprogramming of S. marcescens, including lipopolysaccharide synthesis, peptidoglycan synthesis, and cationic antimicrobial peptide (CAMP) resistance. More importantly, bacterial single-cell RNA sequencing reveals that larvae and L. plantarum modulated carbon utilization and resistance heterogeneity of S. marcescens. On the other hand, L. plantarum adjusted the transcriptional reprogramming in adaption to the alliance with larvae for colonization resistance to S. marcescen. Altogether, our findings provide amenable insight into the host–microbe–microbe interplays at both bulk and single-cell resolutions, advancing fundamental concepts of interactome and precise manipulation of bacterial communities.

ORGANISM(S): Lactiplantibacillus plantarum Serratia marcescens

PROVIDER: GSE251782 | GEO | 2024/10/01

REPOSITORIES: GEO

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Project description:Genome scale metabolic model of Drosophila gut microbe Acetobacter fabarum Abstract - An important goal for many nutrition-based microbiome studies is to identify the metabolic function of microbes in complex microbial communities and their impact on host physiology. This research can be confounded by poorly understood effects of community composition and host diet on the metabolic traits of individual taxa. Here, we investigated these multiway interactions by constructing and analyzing metabolic models comprising every combination of five bacterial members of the Drosophila gut microbiome (from single taxa to the five-member community of Acetobacter and Lactobacillus species) under three nutrient regimes. We show that the metabolic function of Drosophila gut bacteria is dynamic, influenced by community composition, and responsive to dietary modulation. Furthermore, we show that ecological interactions such as competition and mutualism identified from the growth patterns of gut bacteria are underlain by a diversity of metabolic interactions, and show that the bacteria tend to compete for amino acids and B vitamins more frequently than for carbon sources. Our results reveal that, in addition to fermentation products such as acetate, intermediates of the tricarboxylic acid (TCA) cycle, including 2-oxoglutarate and succinate, are produced at high flux and cross-fed between bacterial taxa, suggesting important roles for TCA cycle intermediates in modulating Drosophila gut microbe interactions and the potential to influence host traits. These metabolic models provide specific predictions of the patterns of ecological and metabolic interactions among gut bacteria under different nutrient regimes, with potentially important consequences for overall community metabolic function and nutritional interactions with the host.IMPORTANCE Drosophila is an important model for microbiome research partly because of the low complexity of its mostly culturable gut microbiota. Our current understanding of how Drosophila interacts with its gut microbes and how these interactions influence host traits derives almost entirely from empirical studies that focus on individual microbial taxa or classes of metabolites. These studies have failed to capture fully the complexity of metabolic interactions that occur between host and microbe. To overcome this limitation, we reconstructed and analyzed 31 metabolic models for every combination of the five principal bacterial taxa in the gut microbiome of Drosophila This revealed that metabolic interactions between Drosophila gut bacterial taxa are highly dynamic and influenced by cooccurring bacteria and nutrient availability. Our results generate testable hypotheses about among-microbe ecological interactions in the Drosophila gut and the diversity of metabolites available to influence host traits.

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Drosophila and Commensal Bacteria Synergistically Compete with Opportunistic Pathogens at Bulk and Single-Cell Resolutions [scRNA-seq]

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