Fecal matter; Gut metabolomics; Human stool; Lipidomics; Metabolomics; Multiplatform analysis; Reference materials; Humans; Chromatography, Liquid/methods; Magnetic Resonance Spectroscopy/methods; Gastrointestinal Microbiome; Reference Standards; Metabolome; Reproducibility of Results; Feces/chemistry; Metabolomics/methods; Gas Chromatography-Mass Spectrometry/methods; Chromatography, Liquid; Feces; Gas Chromatography-Mass Spectrometry; Magnetic Resonance Spectroscopy; Endocrinology, Diabetes and Metabolism; Biochemistry; Clinical Biochemistry
Abstract :
[en] [en] INTRODUCTION: Human metabolomics has made significant strides in understanding metabolic changes and their implications for human health, with promising applications in diagnostics and treatment, particularly regarding the gut microbiome. However, progress is hampered by issues with data comparability and reproducibility across studies, limiting the translation of these discoveries into practical applications.
OBJECTIVES: This study aims to evaluate the fit-for-purpose of a suite of human stool samples as potential candidate reference materials (RMs) and assess the state of the field regarding harmonizing gut metabolomics measurements.
METHODS: An interlaboratory study was conducted with 18 participating institutions. The study allowed for the use of preferred analytical techniques, including liquid chromatography-mass spectrometry (LC-MS), gas chromatography-mass spectrometry (GC-MS), and nuclear magnetic resonance (NMR).
RESULTS: Different laboratories used various methods and analytical platforms to identify the metabolites present in human stool RM samples. The study found a 40% to 70% recurrence in the reported top 20 most abundant metabolites across the four materials. In the full annotation list, the percentage of metabolites reported multiple times after nomenclature standardization was 36% (LC-MS), 58% (GC-MS) and 76% (NMR). Out of 9,300 unique metabolites, only 37 were reported across all three measurement techniques.
CONCLUSION: This collaborative exercise emphasized the broad chemical survey possible with multi-technique approaches. Community engagement is essential for the evaluation and characterization of common materials designed to facilitate comparability and ensure data quality underscoring the value of determining current practices, challenges, and progress of a field through interlaboratory studies.
Disciplines :
Chemistry
Author, co-author :
Cruz, Abraham Kuri ; Chemical Sciences Division, National Institute of Standards and Technology (NIST), 100 Bureau Dr.,, Gaithersburg, MD, 20899, USA
Alves, Marina Amaral ; Turku Bioscience Centre, University of Turku and Åbo Akademi University, Tykistökatu 6, 20520, Turku, Finland ; Walter Mors Institute of Research On Natural Products, Federal University of Rio de Janeiro, Rio de Janeiro, 21941-599, Brazil
Andresson, Thorkell ; Division of Cancer Protection, National Institutes of Health, National Cancer Institute, 9000 Rockville Pike, , Bethesda, MD, 20892, USA
Bayless, Amanda L ; Chemical Sciences Division, National Institute of Standards and Technology (NIST), 331 Fort Johnson Rd, Charleston, SC, 29412, USA
Bloodsworth, Kent J; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Bowden, John A; University of Florida, Gainesville, FL, 32611, USA
Bullock, Kevin; Broad Institute of MIT and Harvard, Merkin Building, 415 Main St., Cambridge, MA, 02142, USA
Burnet, Meagan C; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Neto, Fausto Carnevale ; Northwest Metabolomics Research Center, University of Washington, Seattle, Gerberding Hall G80, Box 351202, Seattle, WA, 98195, USA
Choy, Angelina ; Broad Institute of MIT and Harvard, Merkin Building, 415 Main St., Cambridge, MA, 02142, USA
Clish, Clary B ; Broad Institute of MIT and Harvard, Merkin Building, 415 Main St., Cambridge, MA, 02142, USA
Couvillion, Sneha P ; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Cumeras, Raquel ; West Coast Metabolomics Center, University of California Davis, One Shields Ave., Davis, CA, 95616, USA ; Institut d'Investigació Sanitària Pere Virgili (IISPV), CERCA, 43204, Reus, Spain
Dailey, Lucas; Broad Institute of MIT and Harvard, Merkin Building, 415 Main St., Cambridge, MA, 02142, USA
Dallmann, Guido ; Biocrates Life Sciences AG, Eduard-Bodem-Gasse 8, 6020, Innsbruck, Austria
Davis, W Clay ; Chemical Sciences Division, National Institute of Standards and Technology (NIST), 331 Fort Johnson Rd, Charleston, SC, 29412, USA
Deik, Amy A ; Broad Institute of MIT and Harvard, Merkin Building, 415 Main St., Cambridge, MA, 02142, USA
Dickens, Alex M ; Turku Bioscience Centre, University of Turku and Åbo Akademi University, Tykistökatu 6, 20520, Turku, Finland ; Department of Chemistry, University of Turku, 20014, Turku, Finland
Djukovic, Danijel ; Northwest Metabolomics Research Center, University of Washington, Seattle, Gerberding Hall G80, Box 351202, Seattle, WA, 98195, USA
Dorrestein, Pieter C ; Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, 9500 Gilman Dr., La Jolla, CA, 92093, USA
Eder, Josie G ; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Fiehn, Oliver ; West Coast Metabolomics Center, University of California Davis, One Shields Ave., Davis, CA, 95616, USA
Flores, Roberto ; Division of Program Coordination, Planning and Strategic Initiatives, Office of Nutrition Research, Office of the Director, National Institutes of Health (NIH), 9000 Rockville Pike, Bethesda, MD, 20892, USA
Gika, Helen ; Laboratory of Forensic Medicine and Toxicology, School of Medicine, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece ; Biomic AUTh, Center for Interdisciplinary Research and Innovation (CIRI-AUTH), Balkan Center B1.4, 10th Km Thessaloniki-Thermi Rd., 57001, Thessaloniki, Greece
Hagiwara, Kehau A ; Chemical Sciences Division, National Institute of Standards and Technology (NIST), 331 Fort Johnson Rd, Charleston, SC, 29412, USA
Pham, Tuan Hai ; Biocrates Life Sciences AG, Eduard-Bodem-Gasse 8, 6020, Innsbruck, Austria
Harynuk, James J ; Department of Chemistry, University of Alberta, Edmonton, AB, T6G 2G2, Canada
Aristizabal-Henao, Juan J ; University of Florida, Gainesville, FL, 32611, USA ; BPGbio Inc., 500 Old Connecticut Path, Framingham, MA, 01701, USA
Hoyt, David W ; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Jean-François, Focant ; Organic and Biological Analytical Chemistry Group, MolSys Research Unit, University of Liège, Pl. du Vingt Août 7, 4000, Liège, Belgium
Kråkström, Matilda ; Turku Bioscience Centre, University of Turku and Åbo Akademi University, Tykistökatu 6, 20520, Turku, Finland
Kumar, Amit ; Division of Cancer Protection, National Institutes of Health, National Cancer Institute, 9000 Rockville Pike, , Bethesda, MD, 20892, USA
Kyle, Jennifer E ; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Lamichhane, Santosh ; Turku Bioscience Centre, University of Turku and Åbo Akademi University, Tykistökatu 6, 20520, Turku, Finland
Li, Yuan; UNC Chapel Hill's Nutrition Research Institute, 500 Laureate Way, Kannapolis, NC, 28081, USA
Nam, Seo Lin ; Department of Chemistry, University of Alberta, Edmonton, AB, T6G 2G2, Canada
Mandal, Rupasri; Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2G2, Canada
de la Mata, A Paulina ; Department of Chemistry, University of Alberta, Edmonton, AB, T6G 2G2, Canada
Meehan, Michael J; Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, 9500 Gilman Dr., La Jolla, CA, 92093, USA
Meikopoulos, Thomas ; Division of Program Coordination, Planning and Strategic Initiatives, Office of Nutrition Research, Office of the Director, National Institutes of Health (NIH), 9000 Rockville Pike, Bethesda, MD, 20892, USA ; Biomic AUTh, Center for Interdisciplinary Research and Innovation (CIRI-AUTH), Balkan Center B1.4, 10th Km Thessaloniki-Thermi Rd., 57001, Thessaloniki, Greece
Metz, Thomas O ; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Mouskeftara, Thomai ; Laboratory of Forensic Medicine and Toxicology, School of Medicine, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece ; Biomic AUTh, Center for Interdisciplinary Research and Innovation (CIRI-AUTH), Balkan Center B1.4, 10th Km Thessaloniki-Thermi Rd., 57001, Thessaloniki, Greece
Munoz, Nathalie ; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Gowda, G A Nagana ; Northwest Metabolomics Research Center, University of Washington, Seattle, Gerberding Hall G80, Box 351202, Seattle, WA, 98195, USA
Orešic, Matej ; Turku Bioscience Centre, University of Turku and Åbo Akademi University, Tykistökatu 6, 20520, Turku, Finland ; School of Medical Sciences, Faculty of Medicine and Health, Örebro University, 70281, Örebro, Sweden
Panitchpakdi, Morgan ; Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, 9500 Gilman Dr., La Jolla, CA, 92093, USA
Pierre-Hugues, Stefanuto ; Organic and Biological Analytical Chemistry Group, MolSys Research Unit, University of Liège, Pl. du Vingt Août 7, 4000, Liège, Belgium
Raftery, Daniel ; Northwest Metabolomics Research Center, University of Washington, Seattle, Gerberding Hall G80, Box 351202, Seattle, WA, 98195, USA
Rushing, Blake ; UNC Chapel Hill's Nutrition Research Institute, 500 Laureate Way, Kannapolis, NC, 28081, USA
Schock, Tracey ; Chemical Sciences Division, National Institute of Standards and Technology (NIST), 331 Fort Johnson Rd, Charleston, SC, 29412, USA
Seifried, Harold ; Division of Cancer Protection, National Institutes of Health, National Cancer Institute, 9000 Rockville Pike, , Bethesda, MD, 20892, USA
Servetas, Stephanie ; Biosystems and Biomaterials Division, National Institute of Standards and Technology (NIST), 100 Bureau Dr. , Gaithersburg, MD, 20899, USA
Shen, Tong ; West Coast Metabolomics Center, University of California Davis, One Shields Ave., Davis, CA, 95616, USA
Sumner, Susan ; UNC Chapel Hill's Nutrition Research Institute, 500 Laureate Way, Kannapolis, NC, 28081, USA
Carrillo, Kieran S Tarazona ; Department of Chemistry, University of Alberta, Edmonton, AB, T6G 2G2, Canada
Dejong, Thibaut ; Université de Liège - ULiège > Molecular Systems (MolSys)
Trejo, Jesse B; Pacific Northwest National Laboratory, 902 Battelle Blvd., Richland, WA, 99354, USA
Van Meulebroek, Lieven ; Laboratory of Integrative Metabolomics, Department of Translational Physiology, Infectiology and Public Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium
Vanhaecke, Lynn ; Laboratory of Integrative Metabolomics, Department of Translational Physiology, Infectiology and Public Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium
Virgiliou, Christina ; Laboratory of Forensic Medicine and Toxicology, School of Medicine, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece ; Biomic AUTh, Center for Interdisciplinary Research and Innovation (CIRI-AUTH), Balkan Center B1.4, 10th Km Thessaloniki-Thermi Rd., 57001, Thessaloniki, Greece
Weldon, Kelly C ; Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, 9500 Gilman Dr., La Jolla, CA, 92093, USA
Wishart, David S ; Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2G2, Canada
Zhang, Lu; Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2G2, Canada
Zheng, Jiamin; Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2G2, Canada
Da Silva, Sandra ; Biosystems and Biomaterials Division, National Institute of Standards and Technology (NIST), 100 Bureau Dr. , Gaithersburg, MD, 20899, USA. sandra.dasilva@nist.gov
The authors thank The BioCollective for the collection of frozen pooled human whole stool samples, the Biosystems and Biomaterials and Chemical Sciences Divisions at NIST for conducting an ILS and all the institutions that participated in this study. The authors also thank IAFNS. This work was supported partially by the Institute for the Advancement of Food and Nutrition Sciences (IAFNS) (through an ILSI North America Gut Microbiome Committee grant). IAFNS is a nonprofit science organization that pools funding from industry and advances science through in-kind and financial contributions from private and public sector members. IAFNS had no role in the design, analysis, interpretation, or presentation of the data and results. Metabolomics and lipidomics measurements at PNNL were performed in the Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the U.S. Department of Energy Office of Biological and Environmental Research and located on the campus of PNNL in Richland, Washington. PNNL is a multiprogram national laboratory operated by Battelle for the DOE under Contract DE-AC05-76RLO 1830.P.C.D. would like to acknowledge support from NIH U19 AG063744, and support for the collaborative microbial metabolite center to P.C.D (1U24DK133658). Mass spectrometry-based metabolomics and lipidomics data generated at PNNL were supported by National Center for Complementary and Integrative Health grant R01 AT010271 (T.O.M.) and National Institute of Environmental Health Sciences grant U2CES030170 (T.O.M.). K.T., S.L.N., A.P.D.l.M., and J.J.H. would like to thank MITACS, DNA Genotek, Inc., and The Natural Sciences and Engineering Research Council of Canada (NSERC) for support. The support of The Canada Foundation for Innovation (CFI), Genome Canada, and Genome Alberta to The Metabolomics Innovation Center (TMIC) is also acknowledged. Metabolomics assays performed at the University of Alberta and The Metabolomics Innovation Centre (TMIC) were funded, in part, by Genome Canada and the Canada Foundation for Innovation. R.C. acknowledges that \"This project received funding from the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie Grant Agreement No. (798038)\u201D. B.R.R. and S. S. would like to declare that this study was supported by the NIEHS through the Human Health Exposure Analysis Resource (HHEAR) program through grant 5U2CES030857 and by NCI through the Metabolomics and Clinical Assay Center of the Nutrition for Precision Health (NPH) program through grant 5U24CA268153.
Alseekh, S., Aharoni, A., Brotman, Y., Contrepois, K., D’Auria, J., Ewald, J., C. Ewald, J., Fraser, P. D., Giavalisco, P., Hall, R. D., Heinemann, M., Link, H., Luo, J., Neumann, S., Nielsen, J., Perez de Souza, L., Saito, K., Sauer, U., Schroeder, F. C., Fernie, A. R. (2021). Mass spectrometry-based metabolomics: A guide for annotation, quantification and best reporting practices. In Nature methods (Vol. 18, Issue 7, pp. 747–756). Nature Research. https://doi.org/10.1038/s41592-021-01197-1
J.J. Aristizabal-Henao D.J. Lemas E.K. Griffin K.A. Costa C. Camacho J.A. Bowden Metabolomic profiling of biological reference materials using a multiplatform high-resolution mass spectrometric approach Journal of the American Society for Mass Spectrometry 2021 32 9 2481 2489 10.1021/jasms.1c00194 34388338
G. Bang J.H. Park C. Park K.J. Kim J.K. Kim S.Y. Lee J.Y. Kim Y.H. Park High-resolution metabolomics-based biomarker discovery using exhaled breath condensate from patients with lung cancer Journal of Analytical Science and Technology 2022 10.1186/s40543-022-00347-0
Z.A. Barandouzi J. Lee M. del Carmen Rosas J. Chen W.A. Henderson A.R. Starkweather X.S. Cong Associations of neurotransmitters and the gut microbiome with emotional distress in mixed type of irritable bowel syndrome Scientific Reports 2022 10.1038/s41598-022-05756-0 35102266 8803858
Bayless, A., Da Silva, S., Davis, W. C., Kuri Cruz, A., Piotrowski, P., Schock, T., & Servetas, S. (2023). Multi’omic characterization of human whole stool RGTMs. NIST Internal Report (IR) 8451. https://doi.org/10.6028/NIST.IR.8451
J. Brunmair M. Gotsmy L. Niederstaetter B. Neuditschko A. Bileck A. Slany M.L. Feuerstein C. Langbauer L. Janker J. Zanghellini S.M. Meier-Menches C. Gerner Finger sweat analysis enables short interval metabolic biomonitoring in humans Nature Communications 2021 10.1038/s41467-021-26245-4 34645808 8514494
R. Cumeras T. Shen L. Valdiviez Z. Tippins B.D. Haffner O. Fiehn Differences in the stool metabolome between vegans and omnivores: Analyzing the NIST stool reference material Metabolites 2023 10.3390/metabo13080921 38132849 10744506
Cunningham, A. L., Stephens, J. W., Harris, D. A. (2021). Gut microbiota influence in type 2 diabetes mellitus (T2DM). In Gut pathogens (Vol. 13, Issue 1). BioMed Central Ltd. https://doi.org/10.1186/s13099-021-00446-0
F. De Filippis L. Paparo R. Nocerino G. Della Gatta L. Carucci R. Russo E. Pasolli D. Ercolini R. Berni Canani Specific gut microbiome signatures and the associated pro-inflamatory functions are linked to pediatric allergy and acquisition of immune tolerance Nature Communications 2021 10.1038/s41467-021-26266-z 34645820 8514477
M.L.A. De Leoz D.L. Duewer A. Fung L. Liu H.K. Yau O. Potter G.O. Staples K. Furuki R. Frenkel Y. Hu Z. Sosic P. Zhang F. Altmann C. Grunwald-Grube C. Shao J. Zaia W. Evers S. Pengelley D. Suckau S.E. Stein NIST interlaboratory study on glycosylation analysis of monoclonal antibodies: Comparison of results from diverse analytical methods Molecular and Cellular Proteomics 2020 19 1 11 30 10.1074/mcp.RA119.001677 31591262
M. De Spiegeleer M. De Graeve S. Huysman A. Vanderbeke L. Van Meulebroek L. Vanhaecke Impact of storage conditions on the human stool metabolome and lipidome: Preserving the most accurate fingerprint Analytica Chimica Acta 2020 1108 79 88 10.1016/j.aca.2020.02.046 32222247
O. Deda A.C. Chatziioannou S. Fasoula D. Palachanis Ν. Raikos G.A. Theodoridis H.G. Gika Sample preparation optimization in fecal metabolic profiling Journal of Chromatography b: Analytical Technologies in the Biomedical and Life Sciences 2017 1047 115 123 10.1016/j.jchromb.2016.06.047 27423778
Elpa, D. P., Chiu, H. Y., Wu, S. P., Urban, P. L. (2021). Skin metabolomics. In Trends in endocrinology and metabolism (Vol. 32, Issue 2, pp. 66–75). Elsevier. https://doi.org/10.1016/j.tem.2020.11.009
K.M. Erlandson J. Liu R. Johnson S. Dillon C.M. Jankowski M. Kroehl C.E. Robertson D.N. Frank Y. Tuncil J. Higgins B. Hamaker C.C. Wilson An exercise intervention alters stool microbiota and metabolites among older, sedentary adults Therapeutic Advances in Infectious Disease 2021 10.1177/20499361211027067 34262758 8246564
Fahy, E., Subramaniam, S. (2020). RefMet: A reference nomenclature for metabolomics. In Nature methods (Vol. 17, Issue 12, pp. 1173–1174). Nature Research. https://doi.org/10.1038/s41592-020-01009-y
O. Fiehn Metabolomics by gas chromatography-mass spectrometry: Combined targeted and untargeted profiling Current Protocols in Molecular Biology 2016 10.1002/0471142727.mb3004s114 27038389 4829120
O. Fiehn D. Robertson J. Griffin M. vab der Werf B. Nikolau N. Morrison L.W. Sumner R. Goodacre N.W. Hardy C. Taylor J. Fostel B. Kristal R. Kaddurah-Daouk P. Mendes B. van Ommen J.C. Lindon S.A. Sansone The metabolomics standards initiative (MSI) Metabolomics 2007 3 3 175 178 10.1007/s11306-007-0070-6
Gardner, A., Carpenter, G., So, P. W. (2020). Salivary metabolomics: From diagnostic biomarker discovery to investigating biological function. In Metabolites (Vol. 10, Issue 2). MDPI AG. https://doi.org/10.3390/metabo10020047
J.M. Gauglitz K.A. West W. Bittremieux C.L. Williams K.C. Weldon M. Panitchpakdi F. Di Ottavio C.M. Aceves E. Brown N.C. Sikora A.K. Jarmusch C. Martino A. Tripathi M.J. Meehan K. Dorrestein J.P. Shaffer R. Coras F. Vargas L.D.R. Goldasich P.C. Dorrestein Enhancing untargeted metabolomics using metadata-based source annotation Nature Biotechnology 2022 40 12 1774 1779 10.1038/s41587-022-01368-1 35798960 10277029
J. Gray B. Guo R. Bearden J. Manka A fast, fully validated GC-MS method using a simplified pretreatment for the quantification of short and branched chain fatty acids in human stool Journal of Mass Spectrometry 2022 10.1002/jms.4817 35266592
Journey E. N. K., Ortega-Santos, C. P., Bruening, M., & Whisner, C. M Changes in weight status and the intestinal microbiota among College Freshman, aged 18 Years Journal of Adolescent Health 2020 66 2 166 171 10.1016/j.jadohealth.2019.06.005
Kirwan, J. A., Gika, H., Beger, R. D., Bearden, D., Dunn, W. B., Goodacre, R., Theodoridis, G., Witting, M., Yu, L. R., Wilson, I. D. (2022). Quality assurance and quality control reporting in untargeted metabolic phenotyping: mQACC recommendations for analytical quality management. In Metabolomics (Vol. 18, Issue 9). Springer. https://doi.org/10.1007/s11306-022-01926-3
H.C. Köfeler T.O. Eichmann R. Ahrends J.A. Bowden N. Danne-Rasche E.A. Dennis M. Fedorova W.J. Griffiths X. Han J. Hartler M. Holčapek R. Jirásko J.P. Koelmel C.S. Ejsing G. Liebisch Z. Ni V.B. O’Donnell O. Quehenberger D. Schwudke A. Shevchenko M. Wakelam M.R. Wenk D. Wolrab K. Ekroos Quality control requirements for the correct annotation of lipidomics data Nature Communications 2021 12 4771 10.1038/s41467-021-24984-y 34362906 8346590
Kondoh, H., Kameda, M., & Yanagida, M. (2021). Whole blood metabolomics in aging research. In International journal of molecular sciences (Vol. 22, Issue 1, pp. K., 1–13). MDPI AG. https://doi.org/10.3390/ijms22010175
J. Langenau K. Oluwagbemigun C. Brachem W. Lieb R. Di Giuseppe A. Artati G. Kastenmüller L. Weinhold M. Schmid U. Nöthlings Blood metabolomic profiling confirms and identifies biomarkers of food intake Metabolites 2020 10 11 1 17 10.3390/metabo10110468
Lippa, K. A., Aristizabal-Henao, J. J., Beger, R. D., Bowden, J. A., Broeckling, C., Beecher, C., Clay Davis, W., Dunn, W. B., Flores, R., Goodacre, R., Gouveia, G. J., Harms, A. C., Hartung, T., Jones, C. M., Lewis, M. R., Ntai, I., Percy, A. J., Raftery, D., Schock, T. B., Ubhi, B. K. (2022). Reference materials for MS-based untargeted metabolomics and lipidomics: a review by the metabolomics quality assurance and quality control consortium (mQACC). In Metabolomics (Vol. 18, Issue 4). Springer. https://doi.org/10.1007/s11306-021-01848-6
McDonald, J. G., Ejsing, C. S., Kopczynski, D., Holčapek, M., Aoki, J., Arita, M., Arita, M., Baker, E. S., Bertrand-Michel, J., Bowden, J. A., Brügger, B., Ellis, S. R., Fedorova, M., Griffiths, W. J., Han, X., Hartler, J., Hoffmann, N., Koelmel, J. P., Köfeler, H. C., Ekroos, K. (2022). Introducing the Lipidomics Minimal Reporting Checklist. In Nature Metabolism (Vol. 4, Issue 9, pp. 1086–1088). Nature Research. https://doi.org/10.1038/s42255-022-00628-3
Monda, V., Villano, I., Messina, A., Valenzano, A., Esposito, T., Moscatelli, F., Viggiano, A., Cibelli, G., Chieffi, S., Monda, M., & Messina, G. (2017). Exercise modifies the gut microbiota with positive health effects. In Oxidative Medicine and Cellular Longevity (Vol. 2017). Hindawi Limited. https://doi.org/10.1155/2017/3831972
S. Moosmang M. Pitscheider S. Sturm C. Seger H. Tilg M. Halabalaki H. Stuppner Metabolomic analysis—addressing NMR and LC-MS related problems in human feces sample preparation Clinica Chimica Acta 2019 489 169 176 10.1016/j.cca.2017.10.029
R. Moreau J. Clària F. Aguilar F. Fenaille J.J. Lozano C. Junot B. Colsch P. Caraceni J. Trebicka M. Pavesi C. Alessandria F. Nevens F. Saliba T.M. Welzel A. Albillos T. Gustot J. Fernández C. Moreno M. Baldassarre P. Angeli Blood metabolomics uncovers inflammation-associated mitochondrial dysfunction as a potential mechanism underlying ACLF Journal of Hepatology 2020 72 4 688 701 10.1016/j.jhep.2019.11.009 31778751
S.L. Nam K. Tarazona Carrillo A.P. de la Mata J.J. Harynuk Untargeted metabolomic profiling of aqueous and lyophilized pooled human feces from two diet cohorts using two-dimensional gas chromatography coupled with time-of-flight mass spectrometry Metabolites 2023 10.3390/metabo13070828 37999255 10673153
Neuman, H., & Koren, O. (2016). The gut microbiome. In Encyclopedia of cell biology (Vol. 2, pp. 799–808). Elsevier. https://doi.org/10.1016/B978-0-12-394447-4.20083-7
Pantazi, A. C., Mihai, C. M., Balasa, A. L., Chisnoiu, T., Lupu, A., Frecus, C. E., Mihai, L., Ungureanu, A., Kassim, M. A. K., Andrusca, A., Nicolae, M., Cuzic, V., Lupu, V. V., & Cambrea, S. C. (2023). Relationship between gut microbiota and allergies in children: A literature review. In Nutrients (Vol. 15, Issue 11). MDPI.https://doi.org/10.3390/nu15112529
Parekh, P. J., Balart, L. A., & Johnson, D. A. (2015). The influence of the gut microbiome on obesity, metabolic syndrome and gastrointestinal disease. In Clinical and translational gastroenterology (Vol. 6, Issue 6). Nature Publishing Group.https://doi.org/10.1038/ctg.2015.16
K.T. Peter A.L. Phillips A.M. Knolhoff P.R. Gardinali C.A. Manzano K.E. Miller M. Pristner L. Sabourin M.W. Sumarah B. Warth J.R. Sobus Nontargeted analysis study reporting tool: A framework to improve research transparency and reproducibility Analytical Chemistry 2021 93 41 13870 13879 10.1021/acs.analchem.1c02621 34618419 9408805
K.O. Poulsen F. Meng E. Lanfranchi J.F. Young C. Stanton C.A. Ryan A.L. Kelly U.K. Sundekilde Dynamic changes in the human milk metabolome over 25 weeks of lactation Frontiers in Nutrition 2022 10.3389/fnut.2022.917659 36386902 9665408
M. Prochazkova E. Budinska M. Kuzma H. Pelantova J. Hradecky M. Heczkova N. Daskova M. Bratova I. Modos P. Videnska P. Splichalova S.A. Sowah M. Kralova M. Henikova E. Selinger K. Klima K. Chalupsky R. Sedlacek R. Landberg M. Cahova Vegan diet is associated with favorable effects on the metabolic performance of intestinal microbiota: A cross-sectional multi-omics study Frontiers in Nutrition 2022 10.3389/fnut.2021.783302 35071294 8777108
D. Radjabzadeh J.A. Bosch A.G. Uitterlinden A.H. Zwinderman M.A. Ikram J.B.J. van Meurs A.I. Luik M. Nieuwdorp A. Lok C.M. van Duijn R. Kraaij N. Amin Gut microbiome-wide association study of depressive symptoms Nature Communications 2022 10.1038/s41467-022-34502-3 36473853 9726982
Rodríguez-Morató, J., Pozo, Ó. J., & Marcos, J. (2018). Targeting human urinary metabolome by LC–MS/MS: A review. In Bioanalysis (Vol. 10, Issue 7, pp. 489–516). Future Medicine Ltd. https://doi.org/10.4155/bio-2017-0285
R.M. Salek C. Steinbeck M.R. Viant R. Goodacre W.B. Dunn The role of reporting standards for metabolite annotation and identification in metabolomic studies GigaScience 2013 10.1186/2047-217X-2-13 24131531 3853013
Y. Simón-Manso M.S. Lowenthal L.E. Kilpatrick M.L. Sampson K.H. Telu P.A. Rudnick W.G. Mallard D.W. Bearden T.B. Schock D.V. Tchekhovskoi N. Blonder X. Yan Y. Liang Y. Zheng W.E. Wallace P. Neta K.W. Phinney A.T. Remaley S.E. Stein Metabolite profiling of a NIST standard reference material for human plasma (SRM 1950): GC-MS, LC-MS, NMR, and clinical laboratory analyses, libraries, and web-based resources Analytical Chemistry 2013 85 24 11725 11731 10.1021/ac402503m 24147600
M. Sindelar G.J. Patti Chemical discovery in the era of metabolomics Journal of the American Chemical Society 2020 142 20 9097 9105 10.1021/jacs.9b13198 32275430 7310675
A.M. Stephen J.H. Cummings The microbial contribution to human faecal mass The Pathological Society of Great Britain and Ireland 1980 13 1 45 56
L.W. Sumner A. Amberg D. Barrett M.H. Beale R. Beger C.A. Daykin T.W.M. Fan O. Fiehn R. Goodacre J.L. Griffin T. Hankemeier N. Hardy J. Harnly R. Higashi J. Kopka A.N. Lane J.C. Lindon P. Marriott A.W. Nicholls M.R. Viant Proposed minimum reporting standards for chemical analysis: Chemical analysis working group (CAWG) metabolomics standards initiative (MSI) Metabolomics 2007 3 3 211 221 10.1007/s11306-007-0082-2 24039616 3772505
C. Sun A. Li C. Xu J. Ma H. Wang Z. Jiang J. Hou Comparative analysis of fecal microbiota in vegetarians and omnivores Nutrients 2023 10.3390/nu15102358 38201846 10780998
Y.V. Sun Y.J. Hu Integrative analysis of multi-omics data for discovery and functional studies of complex human diseases Advances Genetics 2016 93 147 190 10.1016/bs.adgen.2015.11.004
D. Vandeputte G. Falony S. Vieira-Silva R.Y. Tito M. Joossens J. Raes Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates Gut 2016 65 1 57 62 10.1136/gutjnl-2015-309618 26069274
M.R. Viant T.M.D. Ebbels R.D. Beger D.R. Ekman D.J.T. Epps H. Kamp P.E.G. Leonards G.D. Loizou J.I. MacRae B. van Ravenzwaay P. Rocca-Serra R.M. Salek T. Walk R.J.M. Weber Use cases, best practice and reporting standards for metabolomics in regulatory toxicology Nature Communications 2019 10.1038/s41467-019-10900-y 31292445 6620295
K. Wang R.S. Mehta W. Ma L.H. Nguyen D.D. Wang A.R. Ghazi Y. Yan L. Al-Shaar Y. Wang D. Hang B.C. Fu S. Ogino E.B. Rimm F.B. Hu R.N. Carmody W.S. Garrett Q. Sun A.T. Chan C. Huttenhower M. Song The gut microbiome modifies the associations of short- and long-term physical activity with body weight changes Microbiome 2023 10.1186/s40168-023-01542-w 38102689 10722806
R. Wawrzyniak A. Kosnowska S. Macioszek R. Bartoszewski M.J. Markuszewski New plasma preparation approach to enrich metabolome coverage in untargeted metabolomics: Plasma protein bound hydrophobic metabolite release with proteinase K Scientific Reports 2018 10.1038/s41598-018-27983-0 29934622 6015025
Wilson, I. D., Theodoridis, G., & Virgiliou, C. (2021). A perspective on the standards describing mass spectrometry-based metabolic phenotyping (metabolomics/metabonomics) studies in publications. In Journal of chromatography B: Analytical technologies in the biomedical and life sciences (Vol. 1164). Elsevier.https://doi.org/10.1016/j.jchromb.2020.122515
S. Xing S. Shen B. Xu X. Li T. Huan BUDDY: Molecular formula discovery via bottom-up MS/MS interrogation Nature Methods 2023 20 6 881 890 10.1038/s41592-023-01850-x 37055660
J. Zierer M.A. Jackson G. Kastenmüller M. Mangino T. Long A. Telenti R.P. Mohney K.S. Small J.T. Bell C.J. Steves A.M. Valdes T.D. Spector C. Menni The fecal metabolome as a functional readout of the gut microbiome Nature Genetics 2018 50 6 790 795 10.1038/s41588-018-0135-7 29808030 6104805
