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

Vale FF, Roberts RJ, Kobayashi I, Camargo MC, Rabkin CS, Wang D, Hicks B, Zhu B, Yeager M, Hutchinson A, Teshome K, Jones K, Luo W, Goldstein AM, Hu N, Taylor PR, Song M, Gutiérrez-Escobar AJ, Yu K, Abnet CC, Chanock SJ, Romero-Gallo J, Krishna U, Peek RM, Piazuelo MB, Wilson KT, Loh JT, Cover TL, Raaf N, Aftab H, Akada J, Matsumoto T, Yamaoka Y, Haesebrouck F, Bartelli TF, Nunes DN, Pelosof A, Sztokfisz CZ, Dias-Neto E, Assumpção PP, Tishkov I, Goodman KJ, Geary J, Cromarty TJ, Price NL, Quilty D, Corvalan AH, Serrano CA, Gonzalez R, Riquelme A, García-Cancino A, Parra-Sepúlveda C, Castillo F, Bravo MM, Pazos A, Bravo LE, Fox JG, Ramírez-Mayorga V, Molina-Castro S, Durán-Bermúdez S, Campos-Núñez C, Chaves-Cervantes M, Tshibangu-Kabamba E, Tumba GD, Tshimpi-Wola A, de Jesus Ngoma-Kisoko P, Ngoyi DM, Cruz M, Hosking C, Abreu JJ, Varon C, Benejat L, Jehanne Q, Lehours P, Megraud F, Secka O, Link A, Malfertheiner P, Adinortey MB, Bockarie AS, Adinortey CA, Ofori EG, Sgouras DN, Martinez-Gonzalez B, Michopoulos S, Georgopoulos S, Hernandez E, Dominguez RL, Morgan DR, Harðardóttir H, Gunnarsdóttir AI, Guðjónsson H, Jónasson JG, Björnsson ES, Ballal M, Shetty V, Miftahussurur M, Sugihartono T, Alfaray RI, Waskito LA, Fauzia KA, Syam AF, 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 IN, Moldobaeva MS, Rakhat A, Choi IJ, Kim JG, 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 MF, Vellasamy KM, Herrera-Goepfert R, Alonso-Larraga JO, Yee TT, Htet K, Matsuhisa T, Shrestha PK, Ansari S, Abiodun O, Jemilohun C, Akande KO, Olu-Abiodun O, Magaji FA, Omotoso A, Okonkwo U, Osuagwu CC, Owoseni OO, Castaneda C, Castillo M, Velapatino B, Gilman RH, Krzyżek P, Gościniak G, Pawełka D, Korona-Glowniak I, Cichoz-Lach H, Oleastro M, Figueiredo C, Machado JC, Ferreira RM, Bordin DS, Livzan MA, Tsukanov VV, Tan P, Yeoh KG, Zhu F, Ally R, Haas R, Fischer W, Montes M, Fernández-Reyes M, Tamayo E, Lizasoain J, Bujanda L, Lario S, Ramírez-Lázaro MJ, Calvet X, Brunet-Mas E, Domper-Arnal MJ, García-Mateo S, Abad-Baroja D, Delgado-Guillena P, Moreira L, Botargues J, Pérez-Martínez I, Barreiro-Alonso E, Flores V, Gisbert JP, Muro EA, Linares P, Alcoba L, Martin V, Fleitas-Kanonnikoff T, Altayeb HN, Engstrand L, Enroth H, Keller PM, Wagner K, Pohl D, Lee YC, Liou JM, Wu MS, Kocazeybek B, Sarıbas S, Tasçı İ, Demiryas S, Kepil N, Quiel L, Villagra M, Norton M, Johnson D, Huang RJ, Hwang JH, Szymczak W, Rajagopalan S, Asare E, Jacobs WR, In H, Bollag R, Lopez A, Kruse EJ, White J, Graham DY, Lane C, Gao Y, Gold BD, Cruz-Correa M, González-Pons M, Rodriguez LM, Tuan VP, Dung HDQ, Binh TT, Trang TTH, 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 DE, Chiner-Oms Á, Comas I, Martínez-Martínez FJ, Yahara K, Blaser MJ, Vincze T, Morgan RD, Dekker JP, Torres J, Noureen M, Cherry JL, Osada N, Fukuyo M, Arita M, Sandoval-Motta S, Agostini RB, Ghirotto S, Muñoz-Ramírez ZY, Torres RC, Falush D, Thorell K, Uchiyama I (2024)

Publication Type: Journal article

Publication year: 2024

Journal

Book Volume: 16

Article Number: 2379440

Journal Issue: 1

DOI: 10.1080/19490976.2024.2379440

Abstract

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.

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Involved external institutions

Leidos Biomedical Research Inc. United States (USA) (US) Universidad de Costa Rica Costa Rica (CR) Centre Hospitalier Universitaire de Bordeaux / CHU Bordeaux France (FR) Hellenic Pasteur Institute (HPI) Greece (GR) Alexandra Hospital Greece (GR) Asklepieia Health Cluster Greece (GR) University of San Carlos of Guatemala (USAC) / Universidad de San Carlos de Guatemala Guatemala (GT) University of Alabama at Birmingham (UAB) United States (USA) (US) Landspítali / National University Hospital of Iceland Iceland (IS) National Cancer Institute (NCI) United States (USA) (US) Centro di Riferimento Oncologico (CRO) Italy (IT) Vanderbilt University United States (USA) (US) Hospital Clínico Universitario de Valencia Spain (ES) Universität Bern Switzerland (CH) Istanbul University Cerrahpaşa / İstanbul Üniversitesi Cerrahpaşa (IUC) Turkey (TR) Northwell Health United States (USA) (US) Carson Tahoe Regional Medical Center United States (USA) (US) White River Health United States (USA) (US) National Cancer Center (NCC) / 국립암센터 Korea, Republic of (KR) Cardiovascular Research Foundation United States (USA) (US) Federal Medical Centre, Abeokuta Nigeria (NG) Omsk State Medical University (OSMU) / West Siberian State Medical Institute / Омский государственный медицинский университет Russian Federation (RU) Research Institute of Medical Problems of the North (RAMS) / Научно-исследовательский институт медицинских проблем Севера Russian Federation (RU) Scientific University of the South / Universidad Científica del Sur (UCSUR) Peru (PE) Universidad Peruana Cayetano Heredia Peru (PE) Johns Hopkins University (JHU) United States (USA) (US) National University of Singapore (NUS) Singapore (SG) Wrocław Medical University / Uniwersytet Medyczny we Wrocławiu Poland (PL) London School of Hygiene and Tropical Medicine United Kingdom (GB) Chris Hani Baragwanath Hospital South Africa (ZA) Ludwig-Maximilians-Universität (LMU) Germany (DE) Otto-von-Guericke-Universität Magdeburg Germany (DE) Medical University of Lublin / Uniwersytet Medyczny w Lublinie Poland (PL) National Institute of Genomic Medicine / Instituto Nacional de Medicina Genómica (INMEGEN) Mexico (MX) Università degli Studi di Ferrara Italy (IT) Autonomous University of Chihuahua / Universidad Autónoma de Chihuahua (UACH) Mexico (MX) Institut Pasteur of Shanghai (IPS) / 上海巴斯德研究所 China (CN) University of Gothenburg / Göteborgs universitet Sweden (SE) National Institute for Basic Biology (NIBB) Japan (JP) Lithuanian University of Health Sciences / Lietuvos sveikatos mokslų universitetas (LSMU) Lithuania (LT) University of Malaya (UM) / Universiti Malaya Malaysia (MY) Crescent University Nigeria (NG) Jos University Teaching Hospital (JUTH) Nigeria (NG) University of Calabar (Teaching Hospital) Nigeria (NG) University of Nigeria Nigeria (NG) National Center for Emerging and Zoonotic Infectious Diseases (NCEZID) United States (USA) (US) GI Care for Kids United States (USA) (US) University of Lisbon / Universidade de Lisboa (ULisboa) Portugal (PT) New England Biolabs United States (USA) (US) Hosei University / 法政大学 Japan (JP) Oita University / 大分大学 Japan (JP) Airlangga University / Universitas Airlangga Indonesia (ID) Universiteit Gent (UGent) / Ghent University Belgium (BE) University of Indonesia (UI) / Universitas Indonesia Indonesia (ID) A.C.Camargo Cancer Center Brazil (BR) Tehran University of Medical Sciences (TUMS) / دانشگاه علوم پزشکی تهران Iran, Islamic Republic of (IR) Universidade Federal do Pará (UFPA) Brazil (BR) Medical University Sofia / Медицински университет Bulgaria (BG) University of Alberta Canada (CA) Augusta University United States (USA) (US) Pontificia Universidad Católica de Chile Chile (CL) Stanford University United States (USA) (US) Kyorin University / 杏林大学 Japan (JP) Jordan University of Science and Technology (JUST) / جامعة العلوم والتكنولوجيا الأردنية‎ Jordan (JO) Universidad de Concepcion Chile (CL) Kyrgyz State Medical Academy (KSMA) Kyrgyzstan (KG) University of Latvia Latvia (LV) University of Nariño / Universidad de Nariño (Udenar) Colombia (CO) University of Valle / Universidad del Valle (Univalle) Colombia (CO) Massachusetts Institute of Technology (MIT) United States (USA) (US) Riga East University Hospital Latvia (LV) Osaka Metropolitan University (OMU) Japan (JP) University of Mbuji Mayi (UM) Congo, The Democratic Republic of The (CD) National Health Institute Doutor Ricardo Jorge (INSA) Portugal (PT) Donostia University Hospital / Donostia Unibertsitate Ospitalea Spain (ES) Universidade do Porto Portugal (PT) University of Cape Coast Ghana (GH) GBUZ Moscow Clinical Scientific Center Russian Federation (RU) Bellvitge University Hospital / Hospital Universitari de Bellvitge Spain (ES) University of Education, Winneba Ghana (GH) Hospital Clínico Universitario Lozano Blesa Spain (ES) Hospital Universitario Miguel Servet Spain (ES) Hospital Asil de Granollers Spain (ES) Central University Hospital of Asturias Spain (ES) Hospital General Universitario Gregorio Marañón Spain (ES) Instituto de Investigación Sanitaria Princesa Spain (ES) Hospital Universitario de Navarra Spain (ES) Hospital de León Spain (ES) Universidad de León Spain (ES) King Abdulaziz University (KAU) / جامعة الملك عبد العزيز Saudi Arabia (SA) Karolinska Institute Sweden (SE) University of Skövde / Högskolan i Skövde (HIS) Sweden (SE) University of Zurich / Universität Zürich (UZH) Switzerland (CH) Universitätsspital Zürich (USZ) Switzerland (CH) National Taiwan University (NTU) Taiwan (TW) Nagoya City University / 名古屋市立大学 Japan (JP) Kasturba Medical College (KMC) India (IN) University of Algiers Ben Youssef Ben Khadda / Université d'Alger Ben Youssef Ben Khadda / Université D'Alger 1 Algeria (DZ) Baylor College of Medicine United States (USA) (US) Instituto Nacional de Enfermedades Neoplásicas (INEN) Peru (PE) Queen's University Canada (CA) Kyoto University / 京都大学 Kyōto daigaku Japan (JP) University of Antwerp / Universiteit Antwerpen Belgium (BE) National Institute of Allergy and Infectious Diseases United States (USA) (US) Universitat de Barcelona (UB) / University of Barcelona Spain (ES) Bar-Ilan University Israel (IL) Università degli Studi di Trieste Italy (IT) Dhaka Medical College and Hospital (DMCH) / ঢাকা মেডিকেল কলেজ Bangladesh (BD) Hospital Hanga Roa Chile (CL) Chung-Ang University Hospital (CAUH) / 중앙대학교의료원 Korea, Republic of (KR) Seoul National University (SNU) / 서울대학교 Korea, Republic of (KR) Instituto Nacional De Cancerologia Bogota Colombia (CO) University of Kinshasa / Université de Kinshasa Congo, The Democratic Republic of The (CD) Nippon Medical School Japan (JP) Tribhuvan University Teaching Hospital (TUTH) Nepal (NP) Higher Colleges of Technology United Arab Emirates (AE) Babcock University (BU) / Adventist College of West Africa Nigeria (NG) Autonomous University of Santo Domingo / Universidad Autónoma de Santo Domingo (UASD) Dominican Republic (DO) Universidad de Chile Chile (CL) Biomedical Institute of Valencia / Instituto de Biomedicina de Valencia (IBV) Spain (ES) National Institute of Infectious Diseases, Japan (NIID) Japan (JP) Rutgers, The State University of New Jersey United States (USA) (US) Unidad de Investigación en Enfermedades Infecciosas y Parasitarias Mexico (MX) The Graduate University for Advanced Studies Japan (JP) National Center for Biotechnology Information (NCBI) United States (USA) (US) Hokkaido University (Hokudai) / 北海道大学 Japan (JP) Chiba University / 千葉大学 Japan (JP) National Institute of Genetics (NIG) / 国立遺伝学研究所 Japan (JP) Instituto Nacional de Cancerología Mexico (MX) University of Ibadan Nigeria (NG) University of Puerto Rico (UPR) Puerto Rico (PR) Chợ Rẫy Hospital Viet Nam (VN) University of Bath United Kingdom (GB) Universidade Federal de Minas Gerais (UFMG) Brazil (BR) National Institute on Minority Health and Health Disparities (NIMHD) United States (USA) (US) Washington University in St. Louis United States (USA) (US) 108 Military Central Hospital / Bệnh viện Trung ương Quân đội 108 Viet Nam (VN) Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBER-ESP) Spain (ES)

How to cite

APA:

Vale, F.F., Roberts, R.J., Kobayashi, I., Camargo, M.C., Rabkin, C.S., Wang, D.,... Uchiyama, I. (2024). Gene content, phage cycle regulation model and prophage inactivation disclosed by prophage genomics in the Helicobacter pylori Genome Project. Gut Microbes, 16(1). https://doi.org/10.1080/19490976.2024.2379440

MLA:

Vale, Filipa F., et al. "Gene content, phage cycle regulation model and prophage inactivation disclosed by prophage genomics in the Helicobacter pylori Genome Project." Gut Microbes 16.1 (2024).

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