Gene content, phage cycle regulation model and prophage inactivation disclosed by prophage genomics in the Helicobacter pylori Genome Project

Vale F.F. Roberts R.J. Kobayashi I. Camargo M.C. Rabkin C.S. Wang D. Hicks B. Zhu B. Yeager M. Hutchinson A. Teshome K. Jones K. Luo W. Goldstein A.M. Hu N. Taylor P.R. Song M. Gutiérrez-Escobar A.J. Yu K. Abnet C.C. Chanock S.J. Romero-Gallo J. Krishna U. Peek R.M., Jr Piazuelo M.B. Wilson K.T. Loh J.T. Cover T.L. Raaf N. Aftab H. Akada J. Matsumoto T. Yamaoka Y. Haesebrouck F. Bartelli T.F. Nunes D.N. Pelosof A. Sztokfisz C.Z. Dias-Neto E. Assumpção P.P. Tishkov I. Goodman K.J. Geary J. Cromarty T.J. Price N.L. Quilty D. Corvalan A.H. Serrano C.A. Gonzalez R. Riquelme A. García-Cancino A. Parra-Sepúlveda C. Castillo F. Bravo M.M. Pazos A. Bravo L.E. Fox J.G. Ramírez-Mayorga V. Molina-Castro S. Durán-Bermúdez S. Campos-Núñez C. Chaves-Cervantes M. Tshibangu-Kabamba E. Tumba G.D. Tshimpi-Wola A. de Jesus Ngoma-Kisoko P. Ngoyi D.M. Cruz M. Hosking C. Abreu J.J. Varon C. Benejat L. Jehanne Q. Lehours P. Megraud F. Secka O. Link A. Malfertheiner P. Adinortey M.B. Bockarie A.S. Adinortey C.A. Ofori E.G. Sgouras D.N. Martinez-Gonzalez B. Michopoulos S. Georgopoulos S. Hernandez E. Dominguez R.L. Morgan D.R. Harðardóttir H. Gunnarsdóttir A.I. Guðjónsson H. Jónasson J.G. Björnsson E.S. Ballal M. Shetty V. Miftahussurur M. Sugihartono T. Alfaray R.I. Waskito L.A. Fauzia K.A. Syam A.F. Maulahela H. Malekzadeh R. Sotoudeh M. Peretz A. Azrad M. On A. De Re V. Zanussi S. Cannizzaro R. Canzonieri V. Shimura T. Tokunaga K. Osaki T. Kamiya S. Jadallah K. Matalka I. Sagynbekuly I.N. Moldobaeva M.S. Rakhat A. Choi I.J. Kim J.G. Kim N. Leja M. Vangravs R. Šķenders Ģ. Rūdule A. Kikuste I. Vanags A. Rudzīte D. Kupcinskas J. Skieceviciene J. Jonaitis L. Kiudelis G. Jonaitis P. Kiudelis V. Varkalaite G. Vadivelu J. Loke M.F. Vellasamy K.M. Herrera-Goepfert R. Alonso-Larraga J.O. Yee T.T. Htet K. Matsuhisa T. Shrestha P.K. Ansari S. Abiodun O. Jemilohun C. Akande K.O. Olu-Abiodun O. Magaji F.A. Omotoso A. Okonkwo U. Osuagwu C.C. Owoseni O.O. Castaneda C. Castillo M. Velapatino B. Gilman R.H. Krzyżek P. Gościniak G. Pawełka D. Korona-Glowniak I. Cichoz-Lach H. Oleastro M. Figueiredo C. Machado J.C. Ferreira R.M. Bordin D.S. Livzan M.A. Tsukanov V.V. Tan P. Yeoh K.G. Zhu F. Ally R. Haas R. Fischer W. Montes M. Fernández-Reyes M. Tamayo E. Lizasoain J. Bujanda L. Lario S. Ramírez-Lázaro M.J. Calvet X. Brunet-Mas E. Domper-Arnal M.J. García-Mateo S. Abad-Baroja D. Delgado-Guillena P. Moreira L. Botargues J. Pérez-Martínez I. Barreiro-Alonso E. Flores V. Gisbert J.P. Muro E.A. Linares P. Alcoba L. Martin V. Fleitas-Kanonnikoff T. Altayeb H.N. Engstrand L. Enroth H. Keller P.M. Wagner K. Pohl D. Lee Y.-C. Liou J.-M. Wu M.-S. Kocazeybek B. Sarıbas S. Tasçı İ. Demiryas S. Kepil N. Quiel L. Villagra M. Norton M. Johnson D. Huang R.J. Hwang J.H. Szymczak W. Rajagopalan S. Asare E. Jacobs W.R., Jr. In H. Bollag R. Lopez A. Kruse E.J. White J. Graham D.Y. Lane C. Gao Y. Gold B.D. Cruz-Correa M. González-Pons M. Rodriguez L.M. Tuan V.P. Dung H.D.Q. Binh T.T. Trang T.T.H. Van Khien V. Chen X. Zhao Y. Raley C. Kessing B. Tran B. Katsura Y. Gonzalez-Hormazabal P. Didelot X. Sheppard S. Tarazona-Santos E. Zamudio R. Mariño-Ramírez L. Backert S. Naumann M. Smet A. Berg D.E. Chiner-Oms Á. Comas I. Martínez-Martínez F.J. Yahara K. Blaser M.J. Vincze T. Morgan R.D. Dekker J.P. Torres J. Noureen M. Cherry J.L. Osada N. Fukuyo M. Arita M. Sandoval-Motta S. Agostini R.B. Ghirotto S. Muñoz-Ramírez Z.Y. Torres R.C. Falush D. Thorell K. Uchiyama I.
2024 Taylor and Francis Ltd.

Gut Microbes
2024 #16 Issue 1

Prophages can have major clinical implications through their ability to change pathogenic bacterial traits. There is limited understanding of the prophage role in ecological, evolutionary, adaptive processes and pathogenicity of Helicobacter pylori, a widespread bacterium causally associated with gastric cancer. Inferring the exact prophage genomic location and completeness requires complete genomes. The international Helicobacter pylori Genome Project (HpGP) dataset comprises 1011 H. pylori complete clinical genomes enriched with epigenetic data. We thoroughly evaluated the H. pylori prophage genomic content in the HpGP dataset. We investigated population evolutionary dynamics through phylogenetic and pangenome analyses. Additionally, we identified genome rearrangements and assessed the impact of prophage presence on bacterial gene disruption and methylome. We found that 29.5% (298) of the HpGP genomes contain prophages, of which only 32.2% (96) were complete, minimizing the burden of prophage carriage. The prevalence of H. pylori prophage sequences was variable by geography and ancestry, but not by disease status of the human host. Prophage insertion occasionally results in gene disruption that can change the global bacterial epigenome. Gene function prediction allowed the development of the first model for lysogenic-lytic cycle regulation in H. pylori. We have disclosed new prophage inactivation mechanisms that appear to occur by genome rearrangement, merger with other mobile elements, and pseudogene accumulation. Our analysis provides a comprehensive framework for H. pylori prophage biological and genomics, offering insights into lysogeny regulation and bacterial adaptation to prophages.

genome rearrangement , H. pylori , HpGP , mobile elements , phage cycle , prophage

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BioISI – Instituto de Biossistemas e Ciências Integrativas, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Research Institute for Medicines (iMed-ULisboa), Faculty of Pharmacy, Universidade de Lisboa, Lisbon, Portugal
New England Biolabs, Ipswich, MA, United States
Research Center for Micro-Nano Technology, Hosei University, Tokyo, Japan
Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan
Institute of Medical Science, University of Tokyo, Tokyo, Japan
Laboratory of Genome Informatics, National Institute for Basic Biology, Aichi, Okazaki, Japan
Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, United States
Pathogen Genome Bioinformatics and Computational Biology, Research Institute for Medicines, Faculty of Pharmacy, Universidade de Lisboa, Lisboa, Portugal
Instituto de Biosistemas e Ciências Integrativas, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal
Cancer Genomics Research Laboratory, Frederick National Laboratory for Cancer Research, Frederick, MD, United States
Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, United States
Veterans Affairs Tennessee Valley Healthcare System, Nashville, TN, United States
Department of Natural and Life Sciences, Faculty of Sciences, University of Algiers 1 Benyoucef Benkhedda, Algiers, Algeria
Department of Gastroenterology, Dhaka Medical College and Hospital, Dhaka, Bangladesh
Department of Environmental and Preventive Medicine, Oita University Faculty of Medicine, Yufu, Japan
Department of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium
A.C.Camargo Cancer Center, São Paulo, São Paulo, Brazil
Núcleo de Pesquisas em Oncologia, Universidade Federal do Pará, Pará, Belém, Brazil
Medical University of Sofia, Sofia, Bulgaria
Faculty of Medicine and Dentistry, Department of Medicine, University of Alberta, Edmonton, AB, Canada
Department of Biomedical and Molecular Sciences, Queen’s University, Kingston, ON, Canada
Department of Hematology and Oncology, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
Department of Pediatric Gastroenterology and Nutrition, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
Department of Gastroenterology, Faculty of Medicine, Pontificia Universidad Católica de Chile; and Center for Cancer Prevention and Control (CECAN), Santiago, Chile
Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción, Chile
Hospital Hanga Roa, Easter Island, Chile
Grupo de Investigación en Biología del Cáncer, Instituto Nacional de Cancerología, DC, Bogotá, Colombia
Departamento de Biología, Universidad de Nariño, Nariño, Pasto, Colombia
Escuela de Medicina, Universidad del Valle, Valle, Cali, Colombia
Division of Comparative Medicine, Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, United States
Instituto de Investigaciones en Salud, Universidad de Costa Rica, San Jose, Costa Rica
Laboratorio de Patología General y Gastrointestinal (LABGIPAT), San Jose, Costa Rica
Servicio de Gastroenterología y Endoscopía Digestiva, Hospital Clínica Bíblica, San Jose, Costa Rica
Faculty of Medicine, Osaka Metropolitan University, Osaka, Japan
Faculty of Medicine, University of Mbuji-Mayi, Mbuji Mayi, Kasai-Oriental, Democratic Republic Congo
Faculty of Medicine, University of Kinshasa, Kinshasa, Democratic Republic Congo
Department of Parasitology, National Institute of Biomedical Research, Kinshasa, Democratic Republic Congo
Instituto de Microbiología y Parasitología, IMPA, Universidad Autónoma de Santo Domingo, UASD, Santo Domingo, Dominican Republic
Dominican-Japanese Digestive Disease Center, Dr Luis E. Aybar Health and Hygiene City, Santo Domingo, Dominican Republic
Bordeaux Institute of Oncology, BRIC U1312, INSERM, Bordeaux, and National Reference Center for Campylobacters & Helicobacters, CHU de Bordeaux, Bordeaux, France
Medical Research Council Unit, The Gambia at the London School of Hygiene & Tropical Medicine, Banjul, Gambia
Department of Gastroenterology, Hepatology and Infectious Diseases, Otto-von-Guericke University Magdeburg, Magdeburg, Germany
Department of Biochemistry, School of Biological Sciences, University of Cape Coast, Central Region, Cape Coast, Ghana
Department of Internal Medicine and Therapeutics, School of Medical Sciences, University of Cape Coast, Central Region, Cape Coast, Ghana
Department of Molecular Biology and Biotechnology, School of Biological Sciences, University of Cape Coast, Central Region, Cape Coast, Ghana
Department of Biology Education, Faculty of Science Education, University of Education, Winneba, Ghana
Laboratory of Medical Microbiology, Hellenic Pasteur Institute, Athens, Greece
Department of Gastroenterology, Alexandra Hospital, Athens, Greece
Department of Gastroenterology, Athens Medical, P. Faliron Hospital, Athens, Greece
Facultad de Ciencias Médicas, University of San Carlos of Guatemala, Guatemala City, Guatemala
Departamento de Medicina Interna, Hospital de Occidente, Santa Rosa de Copán, Honduras
School of Medicine, University of Alabama at Birmingham (UAB), Birmingham, AL, United States
Landspítali – The National University Hospital of Iceland, Reykjavík, Iceland
University of Iceland, Reykjavík, Iceland
Department of Microbiology, Kasturba Medical College, Manipal Academy of Higher Education, Karnataka, Manipal, India
Department of Medicine, University of Cambridge, Cambridge, United Kingdom
Universitas Airlangga, Surabaya, East Java, Indonesia
University of Indonesia, Jakarta, Indonesia
Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran
Clinical Microbiology Laboratory and Research Institute, Tzafon Medical Center, affiliated with Azrieli Faculty of Medicine, Bar Ilan University, Poriya, Israel
Azrieli Faculty of Medicine, Bar Ilan University, Safed, Israel
Pediatric Gastroenterology and Nutrition Unit, Tzafon Medical Center, Poriya, Israel
Unit of Immunopathology and Oncological Biomarkers, Centro di Riferimento Oncologico di Aviano, Aviano, Italy
Unit of Oncological Gastroenterology, Centro di Riferimento Oncologico di Aviano (CRO) IRCCS, Italy
Department of Medical, Surgical and Health Sciences, University of Trieste, Italy
Unit of Pathology, Centro di Riferimento Oncologico di Aviano (CRO) IRCCS, Italy
Department of Gastroenterology and Metabolism, Nagoya City University Graduate School of Medical Sciences, Nagoya, Japan
School of Medicine, Kyorin University, Tokyo, Mitaka, Japan
Faculty of Medicine, Jordan University of Science and Technology, Ar-Ramtha, Jordan
Research Institute of Life and Health Sciences, Higher School of Medicine, Kokshetau University named after Sh. Ualikhanov, Kokshetau, Kazakhstan
Central Asian Institute for Medical Research, Astana, Kazakhstan
Asian Pacific Organization for Cancer Prevention, Bishkek, Kyrgyzstan
Kyrgyz State Medical Academy, Bishkek, Kyrgyzstan
Center for Gastric Cancer, National Cancer Center, Goyang, South Korea
Department of Internal Medicine, Chung-Ang University Hospital, Seoul, South Korea
College of Medicine, Seoul National University, Seoul, South Korea
Institute of Clinical and Preventive Medicine, University of Latvia, Riga, Latvia
Digestive Diseases Centre GASTRO, Riga, Latvia
Riga East University Hospital, Riga, Latvia
Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
Department of Medical Microbiology, Faculty of Medicine, Universiti Malaya, Kuala Lumpur, Malaysia
Medical Education Research and Development Unit, Faculty of Medicine, Universiti Malaya, Kuala Lumpur, Malaysia
Departamento de Patología, Instituto Nacional de Cancerología, Mexico City, Mexico
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Defence Services General Hospital, Yangon, Yangon Region, Yangon, Myanmar
Nippon Medical School, Tokyo, Japan
Department of Gastroenterology, Maharajgunj Medical Campus, Tribhuvan University Teaching Hospital, Kathmandu, Nepal
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University Teaching Hospital, University of Jos, Plateau, Jos, Nigeria
University of Calabar Teaching Hospital, Cross River, Calabar, Nigeria
Department of Surgery, University of Nigeria Teaching Hospital, Enugu State, Ituku-Ozalla, Nigeria
Department of Internal Medicine, Federal Medical Center Abeokuta, Ogun State, Abeokuta, Nigeria
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Universidad Peruana Cayetano Heredia, Lima, Peru
Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, United States
Department of Microbiology, Wroclaw Medical University, Wrocław, Poland
Department of Surgery Teaching, Wroclaw Medical University, Wrocław, Poland
Department of Pharmaceutical Microbiology, Medical University of Lublin, Lublin, Poland
Department of Gastroenterology with Endoscopic Unit, Medical University of Lublin, Lublin, Poland
Instituto Nacional de Saúde Dr. Ricardo Jorge, Lisboa, Portugal
Instituto de Patologia e Imunologia Molecular da Universidade do Porto, Porto, Portugal
Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal
Faculdade de Medicina da Universidade do Porto, Porto, Portugal
Department of Pancreatic, Biliary and Upper Digestive Tract Disorders, A. S. Loginov Moscow Clinical Scientific Center, Moscow, Russian Federation
Department of General Medical Practice and Family Medicine, Tver State Medical University, Moscow, Russian Federation
Department of Propaedeutic of Internal diseases and Gastroenterology, Russian University of Medicine, Moscow, Russian Federation
Department of Faculty Therapy and Gastroenterology, Omsk State Medical University, Omsk, Russian Federation
Scientific Research Institute of Medical Problems of the North, Federal Research Centre “Krasnoyarsk Science Centre” of the Siberian Branch of Russian Academy of Science, Krasnoyarsk, Russian Federation
Cancer Science Institute of Singapore, National University of Singapore, Singapore, Singapore
Cancer and Stem Cell Biology Program, Duke NUS Medical School, Singapore, Singapore
Genome Institute of Singapore, Agency for Science, Technology and Research, Singapore, Singapore
Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
Department of Gastroenterology and Hepatology, National University Health System, Singapore, Singapore
Chris Hani Baragwanath Academic Hospital, Johannesburg, South Africa
University of the Witwatersrand, Johannesburg, South Africa
Max von Pettenkofer Institute of Hygiene and Medical Microbiology, Faculty of Medicine, LMU Munich, Munich, Germany
Department of Microbiology, Hospital Universitario Donostia-Instituto de Investigacion Sanitaria Biogipuzkoa, San Sebastian, Spain
Department of Gastroenterology, Bioodonostia Health Research Institute – Donostia University Hospital, Universidad del País Vasco (UPV/EHU), Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), San Sebastian, Spain
Digestive Diseases Unit, Parc Taulí Hospital Universitari., Institut d’Investigació i Innovació Parc Taulí (I3PT- CERCA), Universitat Autònoma de Barcelona, Barcelona, Spain
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas, Instituto de Salud Carlos III, Madrid, Spain
Lozano Blesa University Clinic Hospital, Zaragoza, Spain
Aragon Health Research Institute, Zaragoza, Spain
Miguel Servet University Hospital, Zaragoza, Spain
Hospital General de Granollers, Barcelona, Spain
Gastroenterology Department, Hospital Clínic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona, Barcelona, Spain
Hospital Universitari de Bellvitge, L’Hospitalet de Llobregat, Barcelona, Spain
Department of Gastroenterology, Hospital Universitario Central de Asturias, Asturias, Oviedo, Spain
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Farmacology Group, Instituto de Investigación Sanitaria del Principado de Asturias, Asturias, Oviedo, Spain
Instituto Universitario de Oncología del Principado de Asturias, Asturias, Oviedo, Spain
Hospital General Universitario Gregorio Marañón, Madrid, Spain
Gastroenterology Unit, Hospital Universitario de La Princesa, Instituto de Investigación Sanitaria Princesa, Madrid, Spain
Universidad Autónoma de Madrid, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas, Madrid, Spain
Gastroenterology Department, Hospital Universitario de Navarra, Navarra, Pamplona, Spain
Hospital de Leon, Leon, Spain
Institut of Biomedicine, University of León, Consortium for Biomedical Research in Epidemiology and Public Health, Leon, Spain
Instituto de Investigación Sanitaria INCLIVA, Hospital Clínico Universitario de Valencia, Valencia, Spain
Biochemistry Department, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia
Faculty of Medical laboratory Science, Sudan University of Science and Technology, Khartoum, Sudan
Centre for Translational Microbiome Research, Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Solna, Sweden
University of Skövde, Skövde, Sweden
Institute for Infectious Diseases, University of Bern, Bern, Switzerland
Clinical Bacteriology/Mycology Unit, University Hospital Basel, Basel, Switzerland
Institute of Medical Microbiology, University of Zurich, Zürich, Switzerland
Clinic for Gastroenterology and Hepatology, University Hospital Zurich, Zürich, Switzerland
College of Medicine, National Taiwan University, Taipei City, Taiwan
Medical Microbiology Department, Cerrahpasa Medical Faculty, Istanbul University-Cerrahpasa, İstanbul, Turkey
General Surgery Department, Cerrahpasa Medical Faculty, Istanbul University-Cerrahpasa, İstanbul, Turkey
Medical Pathology Department, Cerrahpasa Medical Faculty, Istanbul University-Cerrahpasa, İstanbul, Turkey
Staten Island University Hospital -Northwell Health, Staten Island, NY, United States
Carson Tahoe Regional Medical Center, Carson City, NV, United States
White River Medical Center, Batesville, AR, United States
Department of Medicine, Stanford University, Stanford, CA, United States
Albert Einstein College of Medicine, Bronx, NY, United States
Rutgers Cancer Institute, New Brunswick, NJ, United States
Georgia Cancer Center’s Biorepository, Augusta University, Augusta, Georgia
Augusta University Medical Center, Augusta, Georgia
Section of Gastroenterology and Hepatology, Department of Medicine, Baylor College of Medicine, Houston, TX, United States
Enteric Diseases Laboratory Branch, Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United States
Gi Care for Kids, LLC, Children’s Center for Digestive Healthcare, LLC, Atlanta, GA, United States
University of Puerto Rico Comprehensive Cancer Center, San Juan, Puerto Rico
University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico
Gastrointestinal and Other Cancers Research Group, Division of Cancer Prevention, National Cancer Institute, Rockville, MD, United States
Department of Endoscopy, Cho Ray Hospital, Ho Chi Minh City, Viet Nam
Department of Hepatogastroenterology, 108 Military Central Hospital, Hanoi, Viet Nam
Sequencing Facility Bioinformatics Group, Bioinformatics and Computational Science Directorate, Frederick National Laboratory for Cancer Research, Frederick, MD, United States
Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick, MD, United States
Center for the Evolutionary Origins of Human Behavior, Kyoto University, Inuyama, Japan
Instituto de Ciencias Biomédicas (ICBM), Facultad de Medicina, Universidad de Chile, Santiago, Chile
School of Life Sciences, University of Warwick, Coventry, United Kingdom
Department of Biology & Biochemistry, University of Bath, Bath, United Kingdom
Departamento de Genética, Ecologia e Evolução, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
National Institute on Minority Health and Health Disparities, Bethesda, MD, United States
Division of Microbiology, Department of Biology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Institute of Experimental Internal Medicine, Otto-von- Guericke-Universität Magdeburg, Magdeburg, Germany
Laboratory of Experimental Medicine and Pediatrics, Faculty of Medicine and Health Sciences, University of Antwerp, Antwerp, Belgium
Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO, United States
Genomics and Health Area, FISABIO – Public Health, Valencia, Spain
CIBER in Epidemiology and Public Health, Madrid, Spain
Tuberculosis Genomics Unit, Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Científicas, Valencia, Spain
Quadram Institute Bioscience, Norwich, United Kingdom
National Institute of Infectious Diseases, Tokyo, Japan
Center for Advanced Biotechnology and Medicine, Rutgers University, New Brunswick, NJ, United States
Bacterial Pathogenesis and Antimicrobial Resistance Unit, National Institute of Allergy and Infectious Diseases, Bethesda, MD, United States
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Department of Genetics, SOKENDAI University, Shizuoka, Mishima, Japan
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Department of Molecular Oncology, Chiba University, Chiba, Japan
Bioinformation and DDBJ Center, National Institute of Genetics, Shizuoka, Mishima, Japan
Instituto Nacional de Medicina Genómica, Ciudad de México, Mexico
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Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy
Facultad de Ciencias Químicas, Universidad Autónoma de Chihuahua, Chihuahua, Chihuahua, Mexico
Centre for Microbes Development and Health, Institute Pasteur Shanghai, Shanghai, China
Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
National Institute for Basic Biology, National Institutes of Natural Sciences, Aichi, Japan

BioISI – Instituto de Biossistemas e Ciências Integrativas
Research Institute for Medicines (iMed-ULisboa)
New England Biolabs
Research Center for Micro-Nano Technology
Department of Computational Biology and Medical Sciences
Institute of Medical Science
Laboratory of Genome Informatics
Division of Cancer Epidemiology and Genetics
Pathogen Genome Bioinformatics and Computational Biology
Instituto de Biosistemas e Ciências Integrativas
Cancer Genomics Research Laboratory
Department of Medicine
Veterans Affairs Tennessee Valley Healthcare System
Department of Natural and Life Sciences
Department of Gastroenterology
Department of Environmental and Preventive Medicine
Department of Pathobiology
A.C.Camargo Cancer Center
Núcleo de Pesquisas em Oncologia
Medical University of Sofia
Faculty of Medicine and Dentistry
Department of Biomedical and Molecular Sciences
Department of Hematology and Oncology
Department of Pediatric Gastroenterology and Nutrition
Department of Gastroenterology
Facultad de Ciencias Biológicas
Hospital Hanga Roa
Grupo de Investigación en Biología del Cáncer
Departamento de Biología
Escuela de Medicina
Division of Comparative Medicine
Instituto de Investigaciones en Salud
Laboratorio de Patología General y Gastrointestinal (LABGIPAT)
Servicio de Gastroenterología y Endoscopía Digestiva
Faculty of Medicine
Faculty of Medicine
Faculty of Medicine
Department of Parasitology
Instituto de Microbiología y Parasitología
Dominican-Japanese Digestive Disease Center
Bordeaux Institute of Oncology
Medical Research Council Unit
Department of Gastroenterology
Department of Biochemistry
Department of Internal Medicine and Therapeutics
Department of Molecular Biology and Biotechnology
Department of Biology Education
Laboratory of Medical Microbiology
Department of Gastroenterology
Department of Gastroenterology
Facultad de Ciencias Médicas
Departamento de Medicina Interna
School of Medicine
Landspítali – The National University Hospital of Iceland
University of Iceland
Department of Microbiology
Department of Medicine
Universitas Airlangga
University of Indonesia
Digestive Disease Research Institute
Clinical Microbiology Laboratory and Research Institute
Azrieli Faculty of Medicine
Pediatric Gastroenterology and Nutrition Unit
Unit of Immunopathology and Oncological Biomarkers
Unit of Oncological Gastroenterology
Department of Medical
Unit of Pathology
Department of Gastroenterology and Metabolism
School of Medicine
Faculty of Medicine
Research Institute of Life and Health Sciences
Central Asian Institute for Medical Research
Asian Pacific Organization for Cancer Prevention
Kyrgyz State Medical Academy
Center for Gastric Cancer
Department of Internal Medicine
College of Medicine
Institute of Clinical and Preventive Medicine
Digestive Diseases Centre GASTRO
Riga East University Hospital
Department of Gastroenterology
Department of Medical Microbiology
Medical Education Research and Development Unit
Departamento de Patología
Servicio de Endoscopía
Defence Services General Hospital
Nippon Medical School
Department of Gastroenterology
Division of Health Sciences
Department of Community Medicine
Department of Medicine
Department of Medicine
Department of Nursing
University Teaching Hospital
University of Calabar Teaching Hospital
Department of Surgery
Department of Internal Medicine
Faculty of Health Sciences
Departamento de investigación
Universidad Peruana Cayetano Heredia
Bloomberg School of Public Health
Department of Microbiology
Department of Surgery Teaching
Department of Pharmaceutical Microbiology
Department of Gastroenterology with Endoscopic Unit
Instituto Nacional de Saúde Dr. Ricardo Jorge
Instituto de Patologia e Imunologia Molecular da Universidade do Porto
Instituto de Investigação e Inovação em Saúde
Faculdade de Medicina da Universidade do Porto
Department of Pancreatic
Department of General Medical Practice and Family Medicine
Department of Propaedeutic of Internal diseases and Gastroenterology
Department of Faculty Therapy and Gastroenterology
Scientific Research Institute of Medical Problems of the North
Cancer Science Institute of Singapore
Cancer and Stem Cell Biology Program
Genome Institute of Singapore
Department of Medicine
Department of Gastroenterology and Hepatology
Chris Hani Baragwanath Academic Hospital
University of the Witwatersrand
Max von Pettenkofer Institute of Hygiene and Medical Microbiology
Department of Microbiology
Department of Gastroenterology
Digestive Diseases Unit
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas
Lozano Blesa University Clinic Hospital
Aragon Health Research Institute
Miguel Servet University Hospital
Hospital General de Granollers
Gastroenterology Department
Hospital Universitari de Bellvitge
Department of Gastroenterology
Diet
Farmacology Group
Instituto Universitario de Oncología del Principado de Asturias
Hospital General Universitario Gregorio Marañón
Gastroenterology Unit
Universidad Autónoma de Madrid
Gastroenterology Department
Hospital de Leon
Institut of Biomedicine
Instituto de Investigación Sanitaria INCLIVA
Biochemistry Department
Faculty of Medical laboratory Science
Centre for Translational Microbiome Research
University of Skövde
Institute for Infectious Diseases
Clinical Bacteriology/Mycology Unit
Institute of Medical Microbiology
Clinic for Gastroenterology and Hepatology
College of Medicine
Medical Microbiology Department
General Surgery Department
Medical Pathology Department
Staten Island University Hospital -Northwell Health
Carson Tahoe Regional Medical Center
White River Medical Center
Department of Medicine
Albert Einstein College of Medicine
Rutgers Cancer Institute
Georgia Cancer Center’s Biorepository
Augusta University Medical Center
Section of Gastroenterology and Hepatology
Enteric Diseases Laboratory Branch
Gi Care for Kids
University of Puerto Rico Comprehensive Cancer Center
University of Puerto Rico Medical Sciences Campus
Gastrointestinal and Other Cancers Research Group
Department of Endoscopy
Department of Hepatogastroenterology
Sequencing Facility Bioinformatics Group
Cancer Research Technology Program
Center for the Evolutionary Origins of Human Behavior
Instituto de Ciencias Biomédicas (ICBM)
School of Life Sciences
Department of Biology & Biochemistry
Departamento de Genética
National Institute on Minority Health and Health Disparities
Division of Microbiology
Institute of Experimental Internal Medicine
Laboratory of Experimental Medicine and Pediatrics
Department of Molecular Microbiology
Genomics and Health Area
CIBER in Epidemiology and Public Health
Tuberculosis Genomics Unit
Quadram Institute Bioscience
National Institute of Infectious Diseases
Center for Advanced Biotechnology and Medicine
Bacterial Pathogenesis and Antimicrobial Resistance Unit
Unidad de Investigación en Enfermedades Infecciosas y Parasitarias
Department of Genetics
National Center for Biotechnology Information
Division of International Epidemiology and Population Studies
Faculty of Information Science and Technology
Department of Molecular Oncology
Bioinformation and DDBJ Center
Instituto Nacional de Medicina Genómica
Consejo Nacional de Ciencia y Tecnologia
Centro de Ciencias de la Complejidad
Department of Life Sciences and Biotechnology
Facultad de Ciencias Químicas
Centre for Microbes Development and Health
Department of Chemistry and Molecular Biology
National Institute for Basic Biology

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