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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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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