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Gut bacterial nutrient preferences quantified in vivo.

ABSTRACT: Great progress has been made in understanding gut microbiomes' products and their effects on health and disease. Less attention, however, has been given to the inputs that gut bacteria consume. Here, we quantitatively examine inputs and outputs of the mouse gut microbiome, using isotope tracing. The main input to microbial carbohydrate fermentation is dietary fiber and to branched-chain fatty acids and aromatic metabolites is dietary protein. In addition, circulating host lactate, 3-hydroxybutyrate, and urea (but not glucose or amino acids) feed the gut microbiome. To determine the nutrient preferences across bacteria, we traced into genus-specific bacterial protein sequences. We found systematic differences in nutrient use: most genera in the phylum Firmicutes prefer dietary protein, Bacteroides dietary fiber, and Akkermansia circulating host lactate. Such preferences correlate with microbiome composition changes in response to dietary modifications. Thus, diet shapes the microbiome by promoting the growth of bacteria that preferentially use the ingested nutrients.

SUBMITTER: Zeng X

PROVIDER: S-EPMC9450212 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Gut bacterial nutrient preferences quantified in vivo.

Zeng Xianfeng X Xing Xi X Gupta Meera M Keber Felix C FC Lopez Jaime G JG Lee Ying-Chiang J YJ Roichman Asael A Wang Lin L Neinast Michael D MD Donia Mohamed S MS Wühr Martin M Jang Cholsoon C Rabinowitz Joshua D JD

Cell 20220901 18

Great progress has been made in understanding gut microbiomes' products and their effects on health and disease. Less attention, however, has been given to the inputs that gut bacteria consume. Here, we quantitatively examine inputs and outputs of the mouse gut microbiome, using isotope tracing. The main input to microbial carbohydrate fermentation is dietary fiber and to branched-chain fatty acids and aromatic metabolites is dietary protein. In addition, circulating host lactate, 3-hydroxybutyr ...[more]

PMID: 36055202

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Project description:A fundamental question in microbial physiology concerns why organisms prefer certain nutrients to others. For example, among different nitrogen sources, ammonium is the preferred nitrogen source, supporting fast growth, whereas alternative nitrogen sources, such as certain amino acids, are considered to be poor nitrogen sources, supporting much slower exponential growth. However, the physiological/regulatory logic behind such nitrogen dietary choices remains elusive. In this study, by engineering Escherichia coli, we switched the dietary preferences toward amino acids, with growth rates equivalent to that of the wild-type strain grown on ammonia. However, when the engineered strain was cultured together with wild-type E. coli, this growth advantage was diminished as a consequence of ammonium leakage from the transport-and-catabolism (TC)-enhanced (TCE) cells, which are preferentially utilized by wild-type bacteria. Our results reveal that the nitrogen regulatory (Ntr) system fine tunes the expression of amino acid transport and catabolism components to match the flux through the ammonia assimilation pathway such that essential nutrients are retained, but, as a consequence, the fast growth rate on amino acids is sacrificed. Bacteria exhibit different growth rates under various nutrient conditions. These environmentally related behaviors reflect the coordination between metabolism and the underlying regulatory networks. In the present study, we investigated the intertwined nitrogen metabolic and nitrogen regulatory systems to understand the growth differences between rich and poor nitrogen sources. Although maximal growth rate is considered to be evolutionarily advantageous for bacteria (as remarked by François Jacob, who said that the "dream" of every cell is to become two cells), we showed that negative-feedback loops in the regulatory system inhibit growth rates on amino acids. We demonstrated that in the absence of regulatory feedback, amino acids are capable of supporting fast growth rates, but this results in ammonia leaking out from cells as "waste," benefiting the growth of competitors. These findings provide important insights into the regulatory logic that controls metabolic flux and ensures nutrient containment but consequently sacrifices growth rate.

Project description:UNLABELLED:A major challenge facing bacterial intestinal pathogens is competition for nutrient sources with the host microbiota.Vibrio cholerae is an intestinal pathogen that causes cholera, which affects millions each year; however, our knowledge of its nutritional requirements in the intestinal milieu is limited. In this study, we demonstrated that V. cholerae can grow efficiently on intestinal mucus and its component sialic acids and that a tripartite ATP-independent periplasmic SiaPQM strain, transporter-deficient mutant NC1777, was attenuated for colonization using a streptomycin-pretreated adult mouse model. In in vivo competition assays, NC1777 was significantly outcompeted for up to 3 days postinfection. NC1777 was also significantly outcompeted in in vitro competition assays in M9 minimal medium supplemented with intestinal mucus, indicating that sialic acid uptake is essential for fitness. Phylogenetic analyses demonstrated that the ability to utilize sialic acid was distributed among 452 bacterial species from eight phyla. The majority of species belonged to four phyla, Actinobacteria (members of Actinobacillus, Corynebacterium, Mycoplasma, and Streptomyces), Bacteroidetes (mainly Bacteroides, Capnocytophaga, and Prevotella), Firmicutes (members of Streptococcus, Staphylococcus, Clostridium, and Lactobacillus), and Proteobacteria (including Escherichia, Shigella, Salmonella, Citrobacter, Haemophilus, Klebsiella, Pasteurella, Photobacterium, Vibrio, and Yersinia species), mostly commensals and/or pathogens. Overall, our data demonstrate that the ability to take up host-derived sugars and sialic acid specifically allows V. cholerae a competitive advantage in intestinal colonization and that this is a trait that is sporadic in its occurrence and phylogenetic distribution and ancestral in some genera but horizontally acquired in others. IMPORTANCE:Sialic acids are nine carbon amino sugars that are abundant on all mucous surfaces. The deadly human pathogen Vibrio cholerae contains the genes required for scavenging, transport, and catabolism of sialic acid. We determined that the V. cholerae SiaPQM transporter is essential for sialic acid transport and that this trait allows the bacterium to outcompete noncatabolizers in vivo. We also showed that the ability to take up and catabolize sialic acid is prevalent among both commensals and pathogens that colonize the oral cavity and the respiratory, intestinal, and urogenital tracts. Phylogenetic analysis determined that the sialic acid catabolism phenotype is ancestral in some genera such as Yersinia, Streptococcus, and Staphylococcus and is acquired by horizontal gene transfer in others such as Vibrio, Aeromonas, and Klebsiella. The data demonstrate that this trait has evolved multiple times in different lineages, indicating the importance of specialized metabolism to niche expansion.

Project description:BackgroundThe 20-70% participation of diabetes patients in lifestyle interventions (LSI) worldwide seems to be rather sub-optimal, in spite of all intents of such interventions to delay further progress of the disease. Positive effects through LSI are expected in particular for patients who suffer less from diabetes-related limitations or other chronic diseases. Seeing that diabetes prevalence and with it mortality are increasing, LSI have become an inherent part of diabetes treatment standards. Various qualitative studies have been carried out to identify participation barriers for LSI. However, these have not resulted in more detailed knowledge about the relative importance of factors with an inhibiting impact on participation. Since it cannot be assumed that all of the influencing factors have equivalent values, it is necessary to investigate their individual importance with regard to a positive or negative decision about participating. There are no systematic reviews on patient preferences for LSI programs in diabetes prevention. As a result, the main objectives of this systematic review are to (i) identify existing patient preference elicitation studies related to LSI for diabetic patients, (ii) summarize the methods applied and findings, and (iii) appraise the reporting and methodological quality of such studies.MethodsWe will perform systematic literature searches to identify suitable studies from 14 electronic databases. Retrieved study records will be included based on predefined eligibility criteria as defined in this protocol. We will run abstract and full-text screenings and then extract data from all selected studies by filling in a predefined data extraction spreadsheet. We will undertake a descriptive, narrative synthesis of findings to address the study objectives, since no pooling for quantified preferences is for methodological reasons implementable. We will pay special attention to aspects of methodological quality of preference elicitation by applying established evaluation criteria of the ISPOR and some own developed criteria for different elicitation techniques. All critical stages within the screening, data extraction, and synthesis processes will be conducted by two pairs of authors. This protocol adheres to PRISMA and PRISMA-P standards.DiscussionThe proposed systematic review will provide an overview of the methods used and current practice in the elicitation and quantification of patients' preferences for diabetes prevention lifestyle interventions. Furthermore, the methodological quality of the identified studies will be appraised as well.Systematic review registrationPROSPERO CRD42018086988.

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Gut bacterial nutrient preferences quantified in vivo.

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Gut bacterial nutrient preferences quantified in vivo.

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