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We are interested in the evolution and diversity of viral lifestyles.

Viruses are the epitome of parasitism. Viral life cycle alternates between a metabolically inactive entity responsible for transmission, the virion, and a metabolically active entity responsible for genome replication, transcription, translation and virion generation, the virocell. A virus must infect a cellular host so that the ensemble becomes a virocell. The interactions between viruses and hosts from the very beginning of cellular life itself have generated an enormous diversity of viral life cycles and several gradients of virus-host interactions: from acute to chronic, latent or silent; from lethal to benign or asymptomatic; from extremely to slightly productive. We aim at understanding the origin and evolution of viral lifestyle diversity by means of experimental and bioinformatic approaches.

Our model are DNA-based viruses, mostly papillomaviruses. Papillomaviruses (PVs) are part and parcel of the skin microbiota in all mammals, and ancestral PVs already infected the ancestral bony vertebrates. The vast majority of PV  infections in humans as well as in other animals are asymptomatic and virtually all individuals get infected very early in life. Yet, some PVs can trigger benign proliferations and cause warts in humans and in many other animals, transmitted by simple contact or by sexual route. Further, a handful of closely related PVs are responsible for ca. 5% of all human cancers, essentially in anogenital and oropharyngeal sites. Despite intense research, many questions remain open regarding the evolutionary connection between PV infections and cancer.

Our ultimate aim is to better understand why only certain PVs are associated to cancer, while the majority of PVs cause asymptomatic infections.


Our website: virostyle.cnrs.fr


Group members

'MiVEGEC' publications by members of the group since 2005:

| 2005 | | 2008 | | 2010 | | 2011 | | 2012 | | 2013 | | 2015 | | 2016 | | 2017 | | 2018 | | 2019 | | 2020 |


Ansaldi M, Boulanger P, Brives C, Debarbieux L, Dufour N, Froissart R, Gandon S, Le Henaff C, Petit MA, Rocha E, Torres-Barcelo C (2020) A century of research on bacteriophages. Virologie 24: 9-22 doi

Ansaldi M, Boulanger P, Brives C, Debarbieux L, Dufour N, Froissart R, Gandon S, Le Henaff C, Petit MA, Rocha E, Torres-Barcelo C (2020) Antibacterial applications of bacteriophages. Virologie 24: 23-36 doi

Antunez-Sanchez J, Naish M, Ramirez-Prado JS, Ohno S, Huang Y, Dawson A, Opassathian K, Manza-Mianza D, Ariel F, Raynaud C, Wibowo A, Daron J, Ueda M, Latrasse D, Slotkin RK, Weigel D, Benhamed M, Gutierrez-Marcos J (2020) A new role for histone demethylases in the maintenance of plant genome integrity. Elife 9: e58533 doi

Borveto F, Bravos IG, Willemsen A (2020) Papillomaviruses infecting cetaceans exhibit signs of genome adaptation following a recombination event. Virus Evolution 6: veaa038 doi

Fellay J, Pedergnana V (2020) Exploring the interactions between the human and viral genomes. Human Genetics 139: 777-781 doi

Happel AU, Kullin B, Gamieldien H, Wentzel N, Zauchenberger CZ, Jaspan HB, Dabee S, Barnabas SL, Jaumdally SZ, Dietrich J, Gray G, Bekker LG, Froissart R, Passmore JAS (2020) Exploring potential of vaginal Lactobacillus isolates from South African women for enhancing treatment for bacterial vaginosis. PLoS Pathogens 16: e1008559 doi

Innes H, Buch S, Hutchinson S, Guha IN, Morling JR, Barnes E, Irving W, Forrest E, Pedergnana V, Goldberg D, Aspinall E, Barclay S, Hayes PC, Dillon J, Nischalke HD, Lutz P, Spengler U, Fischer J, Berg T, Brosch M, Eyer F, Datz C, Mueller S, Peccerella T, Deltenre P, Marot A, Soyka M, McQuillin A, Morgan MY, Hampe J, Stickel F (2020) Genome-wide association study for alcohol-related cirrhosis identifies risk loci in MARC1 and HNRNPUL1.Gastroenterology 159: 1276-1289 doi

Manhanzva MT, Abrahams AG, Gamieldien H, Froissart R, Jaspan H, Jaumdally SZ, Barnabas SL, Dabee S, Bekker LG, Gray G, Passmore JAS, Masson L (2020) Inflammatory and antimicrobial properties differ between vaginal Lactobacillusisolates from South African women with non-optimal versus optimal microbiota. Scientific Reports 10: 6196 doi

Monjane AL, Dellicour S, Hartnady P, Oyeniran KA, Owor BE, Bezuidenhout M, Linderme D, Syed RA, Donaldson L, Murray S, Rybicki EP, Kvarnheden A, Yazdkhasti E, Lefeuvre P, Froissart R, Roumagnac P, Shepherd DN, Harkins GW, Suchard MA, Lemey P, Varsani A, Martin DP (2020) Symptom evolution following the emergence of maize streak virus. Elife 9: e51984 doi

Murall CL, Reyne B, Selinger C, Bernat C, Boue V, Grasset S, Groc S, Rahmoun M, Bender N, Bonneau M, Foulongne V, Graf C, Picot E, Picot MC, Tribout V, Waterboer T, Bravo IG, Reynes J, Segondy M, Boulle N, Alizon S (2020) HPV cervical infections and serological status in vaccinated and unvaccinated women. Vaccine 38: 8167-8174 doi

Prudhomme J, De Meeus T, Toty C, Cassan C, Rahola N, Vergnes B, Charrel R, Alten B, Sereno D, Bañuls AL (2020) Altitude and hillside orientation shapes the population structure of the Leishmania infantum vector Phlebotomus ariasi. Scientific Reports 10: 14443 doi

Vasudevan AAJ, Balakrishnan K, Gertzen CGW, Borveto F, Zhang ZL, Sangwiman A, Held U, Kustermann C, Banerjee S, Schumann GG, Haussinger D, Bravo IG, Gohlke H, Munk C (2020) Loop 1 of APOBEC3C regulates its antiviral activity against HIV-1. Journal of Molecular Biology 432: 6200-6227 doi

Vu NS, Tran SH, Tran PV, Tran TC, Tran DN, Dang AD, Nguyen YT, Vu LT, Ngo PK, Nguyen HV, Cassan C, Nguyen CV, Rahola N, Bañuls AL (2020) Diversity and ecology of sand flies (Diptera: Psychodidae), potential vectors of Leishmania in the Quang Ninh province, Vietnam. Journal of Medical Entomology 57: 259-265 doi

Willemsen A, van den Boom A, Dietz J, Dagalp SB, Dogan F, Bravo IG, Ehrhardt A, Ehrke-Schulz E (2020) Genomic and phylogenetic characterization of ChPV2, a novel goat PV closely related to the Xi-PV1 species infecting bovines. Virology Journal 17: 167 doi


Alizon S, Bravo IG, Farrell PJ, Roberts S (2019) Towards a multi-level and a multi-disciplinary approach to DNA oncovirus virulence. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 20190041 doi

Ansari MA, Aranday-Cortes E, Ip CLC, Filipe AD, Lau SH, Bamford C, Bonsall D, Trebes A, Piazza P, Sreenu V, Cowton VM, Ball J, Barnes E, Burgess G, Cooke G, Dillon J, Foster G, Gore C, Guha N, Halford R, Holmes C, Hudson E, Hutchinson S, Irving W, Khakoo S, Klenerman P, Martin N, Mbisa T, McKeating J, McLauchlan J, Miners A, Murray A, Shaw P, Simmonds P, Smith S, Spencer C, Thomson E, Troke P, Vickerman P, Zitzmann N, Bowden R, Patel AH, Foster GR, Irving WL, Agarwal K, Thomson EC, Spencer CCA, Pedergnana V, Consortium Stop-HCV (2019) Interferon lambda 4 impacts the genetic diversity of hepatitis C virus. Elife 8: e42463 doi

Bedhomme S, Amoros-Moya D, Valero L, Bonifaci N, Pujana MA, Bravo IG (2019) Evolutionary changes after translational challenges imposed by horizontal gene transfer. Genome Biology and Evolution 11: 814-831 doi

Bourret J, Alizon S, Bravo IG (2019) COUSIN (COdon Usage Similarity INdex): A normalized measure of codon usage preferences. Genome Biology and Evolution 11: 3523-3528 doi

Chetwin E, Manhanzva MT, Abrahams AG, Froissart R, Gamieldien H, Jaspan H, Jaumdally SZ, Barnabas SL, Dabee S, Happel AU, Bowers D, Davids L, Passmore JAS, Masson L (2019) Antimicrobial and inflammatory properties of South African clinical Lactobacillus isolates and vaginal probiotics. Scientific Reports 9: 1917 doi

Francois S, Mutuel D, Duncan AB, Rodrigues LR, Danzelle C, Lefèvre S, Santos I, Frayssinet M, Fernandez E, Filloux D, Roumagnac P, Froissart R, Ogliastro M (2019) A new prevalent densovirus discovered in Acari. Insight from metagenomics in viral communities associated with two-spotted mite (Tetranychus urticae) populations. Viruses 11: 233 doi

Froissart R, Brives C, Breyton C, Le Marrec C (2019) "French phage network" annual conference 2018 fourth meeting report. Viruses 11: 470 doi

Houlihan CF, Baisley K, Bravo IG, Pavon MA, Changalucha J, Kapiga S, De Sanjose S, Ross DA, Hayes RJ, Watson-Jones D (2019) Human papillomavirus DNA detected in fingertip, oral and bathroom samples from unvaccinated adolescent girls in Tanzania. Sexually Transmitted Infections 95: 374-379 doi

Murall CL, Rahmoun M, Selinger C, Baldellou M, Bernat C, Bonneau M, Boue V, Buisson M, Christophe G, D'Auria G, De Taroni F, Foulongne V, Froissart R, Graf C, Grasset S, Groc S, Hirtz C, Jaussent A, Lajoie J, Lorcy F, Picot E, Picot MC, Ravel J, Reynes J, Rousset T, Seddiki A, Teirlinck M, Tribout V, Tuaillon E, Waterboer T, Jacobs N, Bravo IG, Segondy M, Boulle N, Alizon S (2019) Natural history, dynamics, and ecology of human papillomaviruses in genital infections of young women: protocol of the PAPCLEAR cohort study. BMJ Open 9: e025129 doi

Pedergnana V, Irving WL, Barnes E, McLauchlan J, Spencer CCA, Consortium Stop-Hcv (2019) Impact of IFNL4 genetic variants on sustained virologic response and viremia in hepatitis C virus genotype 3 patients. Journal of Interferon and Cytokine Research 39: 642-649 doi

Pimenoff VN, Tous S, Benavente Y, Alemany L, Quint W, Bosch FX, Bravo IG, de Sanjose S (2019) Distinct geographic clustering of oncogenic human papillomaviruses multiple infections in cervical cancers: results from a worldwide cross-sectional study. International Journal of Cancer 144: 2478-2488 doi

Siala M, Cassan C, Smaoui S, Kammoun S, Marouane C, Godreuil S, Hachicha S, Mhiri E, Slim L, Gamara D, Messadi-Akrout F, Bañuls AL (2019) A first insight into genetic diversity of Mycobacterium bovis isolated from extrapulmonary tuberculosis patients in South Tunisia assessed by spoligotyping and MIRU VNTR. PLoS Neglected Tropical Diseases 13: e0007707 doi

Willemsen A, Bravo IG (2019) Origin and evolution of papillomavirus (onco)genes and genomes. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 20180303 doi

Willemsen A, Felez-Sanchez M, Bravo IG (2019) Genome plasticity in papillomaviruses and de novo emergence of E5 oncogenes. Genome Biology and Evolution 11: 1586-1601 doi

Willemsen A, Zwart MP (2019) On the stability of sequences inserted into viral genomes. Virus Evolution 5: vez045 doi


Bagdassarian E, Doceul V, Pellerin M, Demange A, Meyer L, Jouvenet N, Pavio N (2018) The amino-terminal region of hepatitis E virus ORF1 containing a methyltransferase (Met) and a papain-like cysteine protease (PCP) domain counteracts type I interferon response. Viruses 10: 726 doi

Cassan C, Diagne CA, Tatard C, Gauthier P, Dalecky A, Ba K, Kane M, Niang Y, Diallo M, Sow A, Brouat C, Bañuls AL (2018) Leishmania major and Trypanosoma lewisi infection in invasive and native rodents in Senegal. PLoS Neglected Tropical Diseases 12: e0006615 doi

Francois S, Filloux D, Frayssinet M, Roumagnac P, Martin DP, Ogliastro M, Froissart R (2018) Increase in taxonomic assignment efficiency of viral reads in metagenomic studies. Virus Research 244: 230-234 doi

Gallet R, Froissart R, Ravigne V (2018) Experimental demonstration of the impact of hard and soft selection regimes on polymorphism maintenance in spatially heterogeneous environments. Evolution 72: 1677-1688 doi   reprint

Happel AU, Barnabas SL, Froissart R, Passmore JS (2018) Weighing in on the risks and benefits of probiotic use in HIV-infected and immunocompromised populations. Beneficial Microbes 9: 239-246 doi

Mena M, Taberna M, Tous S, Marquez S, Clavero O, Quiros B, Lloveras B, Alejo M, Leon X, Quer M, Bague S, Mesia R, Nogues J, Goma M, Aguila A, Bonfill T, Blazquez C, Guix M, Hijano R, Torres M, Holzinger D, Pawlita M, Pavon MA, Bravo IG, de Sanjose S, Bosch FX, Alemany L (2018) Double positivity for HPV-DNA/p16(ink4a) is the biomarker with strongest diagnostic accuracy and prognostic value for human papillomavirus related oropharyngeal cancer patients. Oral Oncology 78: 137-144 doi

Mengual-Chuliá B, Wibbelt G, Gottschling M, Bravo IG (2018) Two novel, distantly related papillomaviruses isolated from healthy skin of the Timor deer (Rusa timorensis). Microbiology Resource Announcements 6: e00505-18 doi

Mengual-Chuliá B, Wittstatt U, Olias P, Bravo IG (2018) Genome sequences of two novel papillomaviruses isolated from healthy skin of Pudu puda and Cervus elaphus deer. Microbiology Resource Announcements 6: e00298-18 doi

Taberna M, Torres M, Alejo M, Mena M, Tous S, Marquez S, Pavon MA, Leon X, Garcia J, Guix M, Hijano R, Bonfill T, Aguila A, Lozano A, Mesia R, Alemany L, Bravo IG (2018) The use of HPV16-E5, EGFR, and pEGFR as prognostic biomarkers for oropharyngeal cancer patients. Frontiers in Oncology 8: 589 doi

Willemsen A, Carrasco JL, Elena SF, Zwart MP (2018) Going, going, gone: predicting the fate of genomic insertions in plant RNA viruses. Heredity 121: 499-509 doi


Alizon S, Murall CL, Bravo IG (2017) Why human papillomavirus acute infections matter. Viruses 9: 293 doi

Bedhomme S, Pantoja DP, Bravo IG (2017) Plasmid and clonal interference during post horizontal gene transfer evolution. Molecular Ecology 26: 1832-1847 doi

Happel AU, Jaumdally SZ, Pidwell T, Cornelius T, Jaspan HB, Froissart R, Barnabas SL, Passmore JAS (2017) Probiotics for vaginal health in South Africa: what is on retailers' shelves? BMC Womens Health 17: 7 doi

Murall CL, Abbate JL, Touzel MP, Allen-Vercoe E, Alizon S, Froissart R, McCann K (2017) Invasions of host-associated microbiome networks. In, Networks of Invasion: Empirical Evidence and Case Studies. Advances in Ecological Research. 57: 201-281 doi

Nicolás-Párraga S, Alemany L, de Sanjosé S, Bosch FX, Bravo IG, RIS HPV TT and HPV VVAP study groups (2017) Differential HPV16 variant distribution in squamous cell carcinoma, adenocarcinoma and adenosquamous cell carcinoma. International Journal of Cancer 140: 2092-2100 doi

Pimenoff VN, de Oliveira CM, Bravo IG (2017) Transmission between archaic and modern human ancestors during the evolution of the oncogenic human papillomavirus 16. Molecular Biology and Evolution 34: 4-19 doi

Pontremoli C, Forni D, Cagliani R, Pozzoli U, Riva S, Bravo IG, Clerici M, Sironi M (2017) Evolutionary analysis of old world arenaviruses reveals a major adaptive contribution of the viral polymerase. Molecular Ecology 26: 5173-5188 doi

Torres-Barcelo C, Kaltz O, Froissart R, Gandon S, Ginet N, Ansaldi M (2017) "French phage network"-second meeting report. Viruses 9: 87 doi

Willemsen A, Zwart MP, Ambros S, Carrasco JL, Elena SF (2017) 2b or not 2b: Experimental evolution of functional exogenous sequences in a plant RNA virus. Genome Biology and Evolution 9: 297-310 doi

Willemsen A, Zwart MP, Elena SF (2017) High virulence does not necessarily impede viral adaptation to a new host: a case study using a plant RNA virus. BMC Evolutionary Biology 17: 25 doi

Zhang ZL, Gu QY, Montero MD, Bravo IG, Marques-Bonet T, Haussinger D, Munk C (2017) Stably expressed APOBEC3H forms a barrier for cross-species transmission of simian immunodeficiency virus of chimpanzee to humans. PLoS Pathogens 13: e1006746 doi


Alten B, Maia C, Afonso MO, Campino L, Jimenez M, Gonzalez E, Molina R, Bañuls AL, Prudhomme J, Vergnes B, Toty C, Cassan C, Rahola N, Thierry M, Sereno D, Bongiorno G, Bianchi R, Khoury C, Tsirigotakis N, Dokianakis E, Antoniou M, Christodoulou V, Mazeris A, Karakus M, Ozbel Y, Arserim SK, Kasap OE, Gunay F, Oguz G, Kaynas S, Tsertsvadze N, Tskhvaradze L, Giorgobiani E, Gramiccia M, Volf P, Gradoni L (2016) Seasonal dynamics of phlebotomine sand fly species proven vectors of Mediterranean leishmaniasis caused by Leishmania infantum. PLoS Neglected Tropical Diseases 10: e0004458 doi

Cassan C, Dione MM, Dereure J, Diedhiou S, Bucheton B, Hide M, Kako C, Gaye O, Senghor M, Niang AA, Bañuls AL, Faye B (2016) First insights into the genetic diversity and origin of Leishmania infantum in Mont Rolland (Thiès region, Senegal). Microbes and Infection 18: 412-420 doi

Félez-Sánchez M, Vergara M, de Sanjosé S, Castellsague X, Alemany L, Bravo IG, Grp Vvapo Ris Hpv Tt Study (2016) Searching beyond the usual papillomavirus suspects in squamous carcinomas of the vulva, penis and head and neck. Infection, Genetics and Evolution 45: 198-204 doi

François S, Filloux D, Roumagnac P, Bigot D, Gayral P, Martin DP, Froissart R, Ogliastro M (2016) Discovery of parvovirus-related sequences in an unexpected broad range of animals. Scientific Reports 6: 30880 doi

Mengual-Chulá B, Bedhomme S, Lafforgue G, Elena SF, Bravo IG (2016) Assessing parallel gene histories in viral genomes. BMC Evolutionary Biology 16: 32 doi

Nicolás-Párraga S, Gandini C, Pimenoff VN, Alemany L, de Sanjose S, Bosch FX, Bravo IG, Ris Hpv TT, Grp Hpv Vvap Study (2016) HPV16 variants distribution in invasive cancers of the cervix, vulva, vagina, penis, and anus. Cancer Medicine 5: 2909-2919 doi

Prudhomme J, Cassan C, Hide M, Toty C, Rahola N, Vergnes B, Dujardin JP, Alten B, Sereno D, Bañuls AL (2016) Ecology and morphological variations in wings of Phlebotomus ariasi (Diptera: Psychodidae) in the region of Roquedur (Gard, France): a geometric morphometrics approach. Parasites & Vectors 9: 578 doi

Senghor MW, Niang AA, Depaquit J, Ferte H, Faye MN, Elguero E, Gaye O, Alten B, Perktas U, Cassan C, Faye B, Bañuls AL (2016) Transmission of Leishmania infantum in the canine leishmaniasis focus of Mont-Rolland, Senegal: ecological, parasitological and molecular evidence for a possible role of Sergentomyia sand flies. PLoS Neglected Tropical Diseases 10: e0004940 doi

Willemsen A, Zwart MP, Higueras P, Sardanyes J, Elena SF (2016) Predicting the stability of homologous gene duplications in a plant RNA virus. Genome Biology and Evolution 8: 3065-3082 doi

Zhang ZL, Gu QY, Vasudevan AAJ, Hain A, Kloke BP, Hasheminasab S, Mulnaes D, Sato K, Cichutek K, Haussinger D, Bravo IG, Smits SHJ, Gohlke H, Münk C (2016) Determinants of FIV and HIV Vif sensitivity of feline APOBEC3 restriction factors. Retrovirology 13: 46 doi


Prudhomme J, Rahola N, Toty C, Cassan C, Roiz D, Vergnes B, Thierry M, Rioux JA, Alten B, Sereno D, Bañuls AL (2015) Ecology and spatiotemporal dynamics of sandflies in the Mediterranean Languedoc region (Roquedur area, Gard, France). Parasites & Vectors 8: 642 doi


Berngruber TW, Froissart R, Choisy M & Gandon S (2013) Evolution of virulence in emerging epidemics. PLoS Pathogens. 9: e1003209 doi

Doumayrou J, Avellan A, Froissart R & Michalakis Y (2013) An experimental test of the transmission-virulence trade-off in a plant virus. Evolution. 67: 477-486 doi

Doumayrou J, Leblaye S, Froissart R & Michalakis Y (2013) Reduction of leaf area and symptom severity as proxies of disease-induced plant mortality: The example of the Cauliflower mosaic virus infecting two Brassicaceae hosts. Virus Research. 176: 91-100 doi


Multeau C, Froissart R, Perrin A, Castelli I, Casartelli M & Ogliastro M (2012) Four amino acids of an insect densovirus capsid determine midgut tropism and virulence. Journal of Virology. 86: 5937-5941 doi pdf

Vale PF, Choisy M, Froissart R, Sanjuan R & Gandon S (2012) The distribution of mutational fitness effects of phage phi X174 on different hosts. Evolution. 66: 3495-3507 doi


Vuillaume F, Thebaud G, Urbino C, Forfert N, Granier M, Froissart R, Blanc S & Peterschmitt M (2011) Distribution of the phenotypic effects of random homologous recombination between two virus species. PLoS Pathogens. 7: e1002028 doi pdf


Elena SF & Froissart R (2010) New experimental and theoretical approaches towards the understanding of the emergence of viral infections Introduction. Philosophical Transactions of the Royal Society B: Biological Sciences. 365: 1867-1869 pdf

Froissart R, Doumayrou J, Vuillaume F, Alizon S & Michalakis Y (2010) The virulence-transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies. Philosophical Transactions of the Royal Society B: Biological Sciences. 365: 1907-1918 pdf


Monsion B, Froissart R, Michalakis Y & Blanc S (2008) Large bottleneck size in Cauliflower Mosaic Virus populations during host plant colonization. PLoS Pathogens. 4: e1000174 pdf


Froissart R, Roze D, Uzest M, Galibert L, Blanc S & Michalakis Y (2005) Recombination every day: Abundant recombination in a virus during a single multi-cellular host infectiton. PLoS Biology. 3: e89 [- synopsis -] pdf

Montville R, Froissart R, Remold SK, Tenaillon O & Turner PE (2005) Evolution of mutational robustness in an RNA virus PLoS Biology. 3: e381 [- synopsis -] pdf

Plisson C, Uzest M, Drucker M, Froissart R, Dumas C, Conway J, Thomas D, Blanc S & Bron P (2005) Structure of the mature P3-virus particle complex of cauliflower mosaic virus revealed by cryo-electron microscopy Journal of Molecular Biology. 346: 267-277 pdf