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Downloaded from Journals.Physiology.Org/Journal/Ajpgi at Univ of California Davis (169.237.106.105) on July 21, 2020 UC Davis UC Davis Previously Published Works Title Xenometabolite signatures in the UC Davis type 2 diabetes mellitus rat model revealed using a metabolomics platform enriched with microbe-derived metabolites. Permalink https://escholarship.org/uc/item/9k12s743 Journal American journal of physiology. Gastrointestinal and liver physiology, 319(2) ISSN 0193-1857 Authors Mercer, Kelly E Yeruva, Laxmi Pack, Lindsay et al. Publication Date 2020-08-01 DOI 10.1152/ajpgi.00105.2020 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Am J Physiol Gastrointest Liver Physiol 319: G157–G169, 2020. First published June 8, 2020; doi:10.1152/ajpgi.00105.2020. RESEARCH ARTICLE Microbiome and Host Interactions Xenometabolite signatures in the UC Davis type 2 diabetes mellitus rat model revealed using a metabolomics platform enriched with microbe-derived metabolites Kelly E. Mercer,1,2 Laxmi Yeruva,1,2,3 Lindsay Pack,1 James L. Graham,4,5 Kimber L. Stanhope,4,5 Sree V. Chintapalli,1,2 Umesh D. Wankhade,1,2 Kartik Shankar,6 Peter J. Havel,4,5 Sean H. Adams,1,2 and X Brian D. Piccolo1,2 1Arkansas Children’s Nutrition Center, Little Rock, Arkansas; 2Department of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas; 3Arkansas Children’s Research Institute, Little Rock, Arkansas; 4Department of Nutrition, University of California of California, Davis, California; 5Department of Molecular Biosciences, School of Veterinary Medicine, University of California, Davis, California; and 6Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, Colorado Submitted 6 April 2020; accepted in final form 4 June 2020 Mercer KE, Yeruva L, Pack L, Graham JL, Stanhope KL, metabolomics platform for xenometabolites (nonself-originating me- Chintapalli SV, Wankhade UD, Shankar K, Havel PJ, Adams SH, tabolites). This assay has 190 in-house standards with the majority Piccolo BD. Xenometabolite signatures in the UC Davis type 2 enriched for microbe-derived metabolites. As a proof-of-principle, we diabetes mellitus rat model revealed using a metabolomics platform used the XenoScan to discriminate genetic differences from cecal enriched with microbe-derived metabolites. Am J Physiol Gastrointest samples associated with different rat lineages, in addition to charac- Liver Physiol 319: G157–G169, 2020. First published June 8, 2020; terizing diabetes progression in rat model of type 2 diabetes. Com- doi:10.1152/ajpgi.00105.2020.—The gut microbiome has the poten- plementing microbial sequencing data with xenometabolites uncov- tial to create or modify xenometabolites (i.e., nonhost-derived metab- ered novel microbial metabolism in targeted organisms. olites) through de novo synthesis or modification of exogenous and diabetes; metabolomics; microbiota; xenometabolites endogenous compounds. While there are isolated examples of xeno- metabolites influencing host health and disease, wide-scale character- ization of these metabolites remains limited. We developed a metabo- lomics platform (“XenoScan”) using liquid chromatography-mass INTRODUCTION spectrometry to characterize a range of known and suspected xeno- metabolites and their derivatives. This assay currently applies authen- A great deal of research has focused on the role of the gut tic standards for 190 molecules, enriched for metabolites of microbial microbiome in modulating host physiology and health, includ- origin. As a proof-of-principle, we characterized the cecal content ing associations between specific intestinal microbe popula- xenometabolomics profile in adult male lean Sprague-Dawley (LSD) tions and metabolites with the function of gastrointestinal tract and University of California, Davis type 2 diabetes mellitus (UCD- and systemic immune systems (37, 55), liver function and T2DM) rats at different stages of diabetes. These results were corre- steatosis (10), amino acid metabolism (27), gut hormone re- lated to specific bacterial species generated via shotgun metagenomic lease (11), brain development and behavior (13a), kidney sequencing. UCD-T2DM rats had a unique xenometabolite profile function (28), and other physiological systems. Some of the compared with LSD rats, regardless of diabetes status, suggesting that at least some of the variation is associated with host genetics. strongest evidence that specific bacteria or groups of bacteria Furthermore, modeling approaches revealed that several xenometabo- impact physiological function stems from fecal/cecal content lites discriminated UCD-T2DM rats at early stages of diabetes versus transfer studies, in which donor obesity phenotypes were those at 3 mo postdiabetes onset. Several xenometabolite hubs corre- transferred to recipients (47, 52). Recently, clinical application lated with specific bacterial species in both LSD and UCD-T2DM of this strategy has shown promise, with fecal transfer from rats. For example, indole-3-propionic acid negatively correlated with healthy donors to patients suffering from inflammatory bowel species within the Oscillibacter genus in UCD-T2DM rats considered disease (IBD) helping mitigate IBD-associated symptoms (54). to be prediabetic or recently diagnosed diabetic, in contrast to glu- Most studies of gut microbiome-host interactions have fo- conic acid and trimethylamine, which were positively correlated with cused on correlations between abundances of specific microbes Oscillibacter species. The application of a xenometabolite-enriched and specific (patho)physiological variables, which allows for metabolomics assay in relevant milieus will enable rapid identification hypothesis-generation in terms of the potential bacterial taxa of a wide variety of gut-derived metabolites, their derivatives, and their potential biochemical origins of xenometabolites in relationship that are involved. However, the specific molecular signals to host gastrointestinal microbial ecology. underlying microbe-to-host communication and gut-derived metabolites that reflect shifts in microbial populations, ecol- NEW & NOTEWORTHY We debut a liquid chromatography-mass ogy, and biochemistry remain to be fully elaborated. There is spectrometry (LC/MS) platform called the XenoScan, which is a a massive genetic potential (number of genes and gene vari- ants) for the gut microbiome; when coupled to the large Correspondence: S. H. Adams ([email protected]); B. D. Piccolo biomass of microbes in the gastrointestinal tract, and the ([email protected]). complex molecule mixtures in foods, there is tremendous http://www.ajpgi.org 0193-1857/20 Copyright © 2020 the American Physiological Society G157 Downloaded from journals.physiology.org/journal/ajpgi at Univ of California Davis (169.237.106.105) on July 21, 2020. G158 XENOSCAN: A LC/MS PLATFORM ENRICHED IN XENOMETABOLITES enzymatic and nonenzymatic capacity for generating xenome- mals used in this study has previously been conducted and a major tabolites. This can occur via de novo synthesis, through mi- effect of collection year was observed even though UCD-T2DM rats crobial conversion of exogenous components (e.g., phytonutri- had been maintained at the same animal facility for Ͼ12 yr (45). Thus the current study only reports results from rats collected during 2016. ents, fibers, oligosaccharides, pharmacological agents, etc.), ϭ ϭ and via microbial modification of host-derived molecules (pri- Final sample numbers (n) were as follows: LSD 7, PD 9, RD ϭ 10, and D3M ϭ 5. Since only two animals were available from mary bile acids, urea, etc.). The latter may also be referred to 6-mo diabetic rats (D6M) from 2016, these animals were not included as “cometabolites” since they involve metabolism by both host for analyses herein. and microbe(s). Much work remains to fully categorize xeno- metabolites and their nomenclature, to determine which of Sample Collection these metabolites serve as modulators of mammalian physiol- ogy, and to understand their specific microbial and food- As previously described (45), rats were given a 200 mg/kg ip dose derived origins. of pentobarbital sodium after a 13-h fast. Fully anesthetized rats were exsanguinated via cardiac puncture between ca. 0800 and 1100. Cecal Metabolomics has proven quite valuable to identify molec- tissue was immediately removed after exsanguination and blotted dry. ular biomarkers of microbial metabolism; however, few labo- A hole was punched into the cecal tissue, and a cecal content sample ratories have dedicated authentic standard libraries that encom- was squeezed into a sterile 1.5-mL microcentrifuge tube. Samples pass the wide breadth of metabolites associated with microbial were immediately placed in a Ϫ80°C freezer until analysis. activities. Furthermore, most large-scale metabolomics plat- forms have standard and spectral libraries that generally en- Metagenomic Sequencing compass human and mammalian metabolic pathways, which Total DNA was extracted from cecal content samples (0.1–0.3 g) complicates identification of microbial specific metabolites. To using the DNeasy PowerSoil HTP 96 Kit (Qiagen, Germantown, MD) address this issue, we have developed a metabolomics platform following the manufacturer’s instructions. Sequencing libraries were that enables a greater focus on “nonhost” xenometabolites, generated from extracted DNA samples using Nextera XT reagents xenometabolite derivatives, cometabolites, and related mole- including dual indexes. Libraries were quantitated using Qubit ds- cules, which can be applied to better understand alterations in DNA reagents and pooled
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