microbeMASST: a taxonomically informed mass spectrometry search tool for microbial metabolomics data

Simone Zuffa; Robin Schmid; Anelize Bauermeister; Paulo Wender P Gomes; Andres M Caraballo-Rodriguez; Yasin El Abiead; Allegra T Aron; Emily C Gentry; Jasmine Zemlin; Michael J Meehan; Nicole E Avalon; Robert H Cichewicz; Ekaterina Buzun; Marvic Carrillo Terrazas; Chia-Yun Hsu; Renee Oles; Adriana Vasquez Ayala; Jiaqi Zhao; Hiutung Chu; Mirte C M Kuijpers; Sara L Jackrel; Fidele Tugizimana; Lerato Pertunia Nephali; Ian A Dubery; Ntakadzeni Edwin Madala; Eduarda Antunes Moreira; Leticia Veras Costa-Lotufo; Norberto Peporine Lopes; Paula Rezende-Teixeira; Paula C Jimenez; Bipin Rimal; Andrew D Patterson; Matthew F Traxler; Rita de Cassia Pessotti; Daniel Alvarado-Villalobos; Giselle Tamayo-Castillo; Priscila Chaverri; Efrain Escudero-Leyva; Luis-Manuel Quiros-Guerrero; Alexandre Jean Bory; Juliette Joubert; Adriano Rutz; Jean-Luc Wolfender; Pierre-Marie Allard; Andreas Sichert; Sammy Pontrelli; Benjamin S Pullman; Nuno Bandeira; William H Gerwick; Katia Gindro; Josep Massana-Codina; Berenike C Wagner; Karl Forchhammer; Daniel Petras; Nicole Aiosa; Neha Garg; Manuel Liebeke; Patric Bourceau; Kyo Bin Kang; Henna Gadhavi; Luiz Pedro Sorio de Carvalho; Mariana Silva Dos Santos; Alicia Isabel Pérez-Lorente; Carlos Molina-Santiago; Diego Romero; Raimo Franke; Mark Brönstrup; Arturo Vera Ponce de León; Phillip Byron Pope; Sabina Leanti La Rosa; Giorgia La Barbera; Henrik M Roager; Martin Frederik Laursen; Fabian Hammerle; Bianka Siewert; Ursula Peintner; Cuauhtemoc Licona-Cassani; Lorena Rodriguez-Orduña; Evelyn Rampler; Felina Hildebrand; Gunda Koellensperger; Harald Schoeny; Katharina Hohenwallner; Lisa Panzenboeck; Rachel Gregor; Ellis Charles O'Neill; Eve Tallulah Roxborough; Jane Odoi; Nicole J Bale; Su Ding; Jaap S Sinninghe Damsté; Xue Li Guan; Jerry J Cui; Kou-San Ju; Denise Brentan Silva; Fernanda Motta Ribeiro Silva; Gilvan Ferreira da Silva; Hector H F Koolen; Carlismari Grundmann; Jason A Clement; Hosein Mohimani; Kirk Broders; Kerry L McPhail; Sidnee E Ober-Singleton; Christopher M Rath; Daniel McDonald; Rob Knight; Mingxun Wang; Pieter C Dorrestein

doi:10.1038/s41564-023-01575-9

microbeMASST: a taxonomically informed mass spectrometry search tool for microbial metabolomics data

Nat Microbiol. 2024 Feb;9(2):336-345. doi: 10.1038/s41564-023-01575-9. Epub 2024 Feb 5.

Authors

Simone Zuffa^#^{1

2}, Robin Schmid^#^{1

2}, Anelize Bauermeister^#^{1

2

3}, Paulo Wender P Gomes^{1

2}, Andres M Caraballo-Rodriguez^{1

2}, Yasin El Abiead^{1

2}, Allegra T Aron⁴, Emily C Gentry⁵, Jasmine Zemlin^{1

6}, Michael J Meehan¹, Nicole E Avalon⁷, Robert H Cichewicz⁸, Ekaterina Buzun⁹, Marvic Carrillo Terrazas⁹, Chia-Yun Hsu⁹, Renee Oles⁹, Adriana Vasquez Ayala⁹, Jiaqi Zhao⁹, Hiutung Chu^{9

10}, Mirte C M Kuijpers¹¹, Sara L Jackrel¹¹, Fidele Tugizimana^{12

13}, Lerato Pertunia Nephali¹², Ian A Dubery¹², Ntakadzeni Edwin Madala¹⁴, Eduarda Antunes Moreira¹⁵, Leticia Veras Costa-Lotufo³, Norberto Peporine Lopes¹⁵, Paula Rezende-Teixeira³, Paula C Jimenez¹⁶, Bipin Rimal¹⁷, Andrew D Patterson¹⁷, Matthew F Traxler¹⁸, Rita de Cassia Pessotti¹⁸, Daniel Alvarado-Villalobos¹⁹, Giselle Tamayo-Castillo^{19

20}, Priscila Chaverri^{21

22

23}, Efrain Escudero-Leyva²⁴, Luis-Manuel Quiros-Guerrero^{25

26}, Alexandre Jean Bory^{25

26}, Juliette Joubert^{25

26}, Adriano Rutz^{25

26

27}, Jean-Luc Wolfender^{25

26}, Pierre-Marie Allard^{25

26

28}, Andreas Sichert²⁷, Sammy Pontrelli²⁷, Benjamin S Pullman²⁹, Nuno Bandeira^{1

29}, William H Gerwick^{1

7}, Katia Gindro³⁰, Josep Massana-Codina³⁰, Berenike C Wagner³¹, Karl Forchhammer³¹, Daniel Petras³², Nicole Aiosa³³, Neha Garg^{33

34}, Manuel Liebeke^{35

36}, Patric Bourceau³⁵, Kyo Bin Kang³⁷, Henna Gadhavi^{38

39}, Luiz Pedro Sorio de Carvalho^{38

40}, Mariana Silva Dos Santos⁴¹, Alicia Isabel Pérez-Lorente⁴², Carlos Molina-Santiago⁴², Diego Romero⁴², Raimo Franke⁴³, Mark Brönstrup^{43

44}, Arturo Vera Ponce de León⁴⁵, Phillip Byron Pope^{45

46}, Sabina Leanti La Rosa^{45

46}, Giorgia La Barbera⁴⁷, Henrik M Roager⁴⁷, Martin Frederik Laursen⁴⁸, Fabian Hammerle⁴⁹, Bianka Siewert⁴⁹, Ursula Peintner⁵⁰, Cuauhtemoc Licona-Cassani⁵¹, Lorena Rodriguez-Orduña⁵¹, Evelyn Rampler⁵², Felina Hildebrand^{52

53}, Gunda Koellensperger^{52

54}, Harald Schoeny⁵², Katharina Hohenwallner^{52

53}, Lisa Panzenboeck^{52

53}, Rachel Gregor⁵⁵, Ellis Charles O'Neill⁵⁶, Eve Tallulah Roxborough⁵⁶, Jane Odoi⁵⁷, Nicole J Bale⁵⁸, Su Ding⁵⁸, Jaap S Sinninghe Damsté⁵⁸, Xue Li Guan⁵⁹, Jerry J Cui⁶⁰, Kou-San Ju^{60

61

62

63}, Denise Brentan Silva⁶⁴, Fernanda Motta Ribeiro Silva⁶⁴, Gilvan Ferreira da Silva⁶⁵, Hector H F Koolen⁶⁶, Carlismari Grundmann⁶⁷, Jason A Clement⁶⁸, Hosein Mohimani⁶⁹, Kirk Broders⁷⁰, Kerry L McPhail⁷¹, Sidnee E Ober-Singleton⁷², Christopher M Rath⁷³, Daniel McDonald⁷⁴, Rob Knight^{29

74

75}, Mingxun Wang⁷⁶, Pieter C Dorrestein^{77

78}

Affiliations

¹ Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, San Diego, CA, USA.
² Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, San Diego, CA, USA.
³ Department of Pharmacology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.
⁴ Department of Chemistry and Biochemistry, University of Denver, Denver, CO, USA.
⁵ Department of Chemistry, Virginia Tech, Blacksburg, VA, USA.
⁶ Center for Microbiome Innovation, University of California San Diego, San Diego, CA, USA.
⁷ Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA.
⁸ Department of Chemistry and Biochemistry, College of Arts and Sciences, University of Oklahoma, Norman, OK, USA.
⁹ Department of Pathology, School of Medicine, University of California San Diego, San Diego, CA, USA.
¹⁰ Center for Mucosal Immunology, Allergy, and Vaccines (cMAV), Chiba University-University of California San Diego, San Diego, CA, USA.
¹¹ Department of Ecology, Behavior and Evolution, School of Biological Sciences, University of California San Diego, San Diego, CA, USA.
¹² Department of Biochemistry, Faculty of Science, University of Johannesburg, Johannesburg, South Africa.
¹³ International Research and Development, Omnia Nutriology, Omnia Group (Pty) Ltd, Johannesburg, South Africa.
¹⁴ Department of Biochemistry and Microbiology, Faculty of Sciences, Agriculture and Engineering, University of Venda, Thohoyandou, South Africa.
¹⁵ Department of BioMolecular Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo, Brazil.
¹⁶ Department of Marine Science, Institute of Marine Science, Federal University of São Paulo, Santos, Brazil.
¹⁷ Department of Veterinary and Biomedical Sciences, Pennsylvania State University, University Park, PA, USA.
¹⁸ Plant and Microbial Biology, College of Natural Resources, University of California Berkeley, Berkeley, CA, USA.
¹⁹ Metabolomics and Chemical Profiling, Centro de Investigaciones en Productos Naturales (CIPRONA), Universidad de Costa Rica, San José, Costa Rica.
²⁰ Escuela de Química, Universidad de Costa Rica, San José, Costa Rica.
²¹ Microbial Biotechnology, Centro de Investigaciones en Productos Naturales (CIPRONA) and Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica.
²² Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica.
²³ Department of Natural Sciences, Bowie State University, Bowie, MD, USA.
²⁴ Microbial Biotechnology, Centro de Investigaciones en Productos Naturales (CIPRONA), Universidad de Costa Rica, San José, Costa Rica.
²⁵ School of Pharmaceutical Sciences, University of Geneva, Geneva, Switzerland.
²⁶ Institute of Pharmaceutical Sciences of Western Switzerland, University of Geneva, Geneva, Switzerland.
²⁷ Institute of Molecular Systems Biology, ETH Zurich, Zurich, Switzerland.
²⁸ Department of Biology, University of Fribourg, Fribourg, Switzerland.
²⁹ Department of Computer Science and Engineering, University of California San Diego, San Diego, CA, USA.
³⁰ Plant Protection, Mycology group, Agroscope, Nyon, Switzerland.
³¹ Department of Microbiology and Organismic Interactions, Interfaculty Institute of Microbiology and Infection Medicine, University of Tuebingen, Tuebingen, Germany.
³² Cluster of Excellence 'Controlling Microbes to Fight Infections' (CMFI), University of Tuebingen, Tuebingen, Germany.
³³ School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA, USA.
³⁴ Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, GA, USA.
³⁵ Department of Symbiosis, Metabolic Interactions, Max Planck Institute for Marine Microbiology, Bremen, Germany.
³⁶ Department for Metabolomics, Kiel University, Kiel, Germany.
³⁷ Research Institute of Pharmaceutical Sciences, College of Pharmacy, Sookmyung Women's University, Seoul, Korea.
³⁸ Mycobacterial Metabolism and Antibiotic Research Laboratory, The Francis Crick Institute, London, UK.
³⁹ King's College London, London, UK.
⁴⁰ Chemistry Department, The Herbert Wertheim UF Scripps Institute for Biomedical Innovation and Technology, Jupiter, FL, USA.
⁴¹ Metabolomics Science Technology Platform, The Francis Crick Institute, London, UK.
⁴² Department of Microbiology, Instituto de Hortofruticultura Subtropical y Mediterránea 'La Mayora', Universidad de Málaga-Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Bulevar Louis Pasteur (Campus Universitario de Teatinos), Malaga, Spain.
⁴³ Department of Chemical Biology, Helmholtz Centre for Infection Research, Braunschweig, Germany.
⁴⁴ German Center for Infection Research (DZIF), Site Hannover-Braunschweig, Braunschweig, Germany.
⁴⁵ Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.
⁴⁶ Faculty of Biosciences, Norwegian University of Life Sciences, Ås, Norway.
⁴⁷ Department of Nutrition, Exercise and Sports, University of Copenhagen, Frederiksberg, Denmark.
⁴⁸ National Food Institute, Technical University of Denmark, Lyngby, Denmark.
⁴⁹ Department of Pharmacognosy, Institute of Pharmacy, University of Innsbruck, Innsbruck, Austria.
⁵⁰ Department of Microbiology, University of Innsbruck, Innsbruck, Austria.
⁵¹ Escuela de Ingeniería y Ciencias, Centro de Biotecnología FEMSA, Tecnologico de Monterrey, Monterrey, Mexico.
⁵² Department of Analytical Chemistry, Faculty of Chemistry, University of Vienna, Vienna, Austria.
⁵³ Vienna Doctoral School in Chemistry (DoSChem), Faculty of Chemistry, University of Vienna, Vienna, Austria.
⁵⁴ Vienna Metabolomics Center (VIME), University of Vienna, Vienna, Austria.
⁵⁵ Department of Civil and Environmental Engineering, School of Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁵⁶ School of Chemistry, University of Nottingham, Nottingham, UK.
⁵⁷ Faculty of Engineering, University of Nottingham, Nottingham, UK.
⁵⁸ Department of Marine Microbiology and Biogeochemistry, Netherlands Institute for Sea Research (NIOZ), t Horntje (Texel), the Netherlands.
⁵⁹ Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.
⁶⁰ Department of Microbiology, College of Arts and Sciences, The Ohio State University, Columbus, OH, USA.
⁶¹ Division of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, The Ohio State University, Columbus, OH, USA.
⁶² Center for Applied Plant Sciences, The Ohio State University, Columbus, OH, USA.
⁶³ Infectious Diseases Institute, The Ohio State University, Columbus, OH, USA.
⁶⁴ Faculty of Pharmaceutical Sciences, Food and Nutrition, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil.
⁶⁵ Embrapa Amazônia Ocidental, Manaus, Brazil.
⁶⁶ Escola Superior de Ciências da Saúde, Universidade do Estado do Amazonas, Manaus, Brazil.
⁶⁷ Department of Pharmaceutical Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil.
⁶⁸ Baruch S. Blumberg Institute, Doylestown, PA, USA.
⁶⁹ Computational Biology Department, School of Computer Science, Carnegie Mellon University, Pittsburgh, PA, USA.
⁷⁰ USDA, Agricultural Research Service, National Center for Agricultural Utilization Research, Mycotoxin Prevention and Applied Microbiology Research Unit, Peoria, IL, USA.
⁷¹ Department of Pharmaceutical Sciences, College of Pharmacy, Oregon State University, Corvallis, OR, USA.
⁷² Department of Physics, Study of Heavy-Element-Biomaterials, University of Oregon, Eugene, OR, USA.
⁷³ , Emeryville, CA, USA.
⁷⁴ Department of Pediatrics, University of California San Diego, San Diego, CA, USA.
⁷⁵ Department of Bioengineering, University of California San Diego, San Diego, CA, USA.
⁷⁶ Department of Computer Science and Engineering, University of California Riverside, Riverside, CA, USA.
⁷⁷ Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, San Diego, CA, USA. pdorrestein@health.ucsd.edu.
⁷⁸ Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, San Diego, CA, USA. pdorrestein@health.ucsd.edu.

^# Contributed equally.

Abstract

microbeMASST, a taxonomically informed mass spectrometry (MS) search tool, tackles limited microbial metabolite annotation in untargeted metabolomics experiments. Leveraging a curated database of >60,000 microbial monocultures, users can search known and unknown MS/MS spectra and link them to their respective microbial producers via MS/MS fragmentation patterns. Identification of microbe-derived metabolites and relative producers without a priori knowledge will vastly enhance the understanding of microorganisms' role in ecology and human health.

MeSH terms

Databases, Factual
Humans
Metabolomics* / methods
Tandem Mass Spectrometry*

Abstract

MeSH terms

Grants and funding