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Determining the Pathogenic Potential of Commensal and Clinical Gardnerella Vaginalis Isolates

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Determining the Pathogenic Potential of Commensal and Clinical Gardnerella Vaginalis Isolates ic s Isolate Pathogen ommensal and Clinical aginalis v oana Isabel Castro 2018 DOUTORAMENTO CIÊNCIAS BIOMÉDICAS Potential of C J Determining the Gardnerella D Joana Isabel Castro. Determining the Pathogenic Potential of Commensal D.ICBAS 2018 and Clinical Gardnerella vaginalis Isolates Determining the Pathogenic Potential of Commensal and Clinical Gardnerella vaginalis Isolates Joana Isabel Reis Castro INSTITUTO DE CIÊNCIAS BIOMÉDICAS ABEL SALAZAR Tese de Candidatura ao grau de Doutor em Ciências Biomédicas submetida ao Instituto de Ciências Biomédicas Abel Salazar da Universidade do Porto. Orientador – Doutor Nuno Cerca Categoria – Investigador Principal Afiliação – Centro de Engenharia Biológica, LIBRO – Laboratório de Investigação em Biofilmes Rosário Oliveira, Universidade do Minho, Campus de Gualtar, 4710-057 Braga, Portugal Coorientador – Doutora Kimberly Kay Jefferson Categoria – Professora Associada Afiliação – Department of Microbiology and Immunology, Virginia Commonwealth University, Richmond, VA, 23298-0678c, USA “The important thing is not to stop questioning. Curiosity has its own reason for existing.” Albert Einstein The work presented in this thesis was funded by the Portuguese Foundation for Science and Technology (FCT) under the scope of the strategic funding of UID/BIO/04469/2013 unit and COMPETE 2020 (POCI-01-0145-FEDER-006684), the project RECI/BBB-EBI/0179/2012 (FCOMP-01-0124-FEDER-027462) and BioTecNorte operation (NORTE-01-0145-FEDER-000004) funded by European Regional Development Fund under the scope of Norte2020 – Programa Operacional Regional do Norte. JC acknowledges the FCT individual grant with reference SFRH/BD/93963/2013. iii iv Acknowledgments Um guerreiro da luz nunca esquece a gratidão. Durante a luta, foi ajudado pelos anjos; as forças celestiais colocaram cada coisa em seu lugar, e permitiram que ele pudesse dar o melhor de si. (…) Sua gratidão, porém, não se limita ao mundo espiritual; ele jamais esquece os amigos, porque o sangue deles se misturou ao seu no campo de batalha. Paulo Coelho, em O Manual do Guerreiro da Luz Ao meu orientador, Doutor Nuno Cerca, pela orientação, partilha de conhecimentos, por todas as oportunidades, pela confiança e amizade ao longo destes anos. I would like to acknowledge my co-supervisor, Doctor Kimberly Jefferson, who kindly welcomed me in her lab at the Virginia Commonwealth University and by the guidance, knowledge transfer and assistance in writing reports, papers and also in the thesis. A todos os meus colegas e amigos do “grupo NC”, pelo bom ambiente de trabalho, pelo apoio e amizade. Um especial agradecimento para a Ângela França, pela colaboração no estudo do transcriptoma da Gardnerella vaginalis (capítulo 5). Gostaria também de agradecer aos antigos membros do “grupo NC”, em especial à Tatiana Cereja, Patrícia Alves e Cármen Sousa, pelo suporte técnico na caracterização fenotípica dos vários isolados de G. vaginalis (capítulo 3) e à Daniela Machado pela colaboração no trabalho dos biofilmes mistos (capítulo 7). Não posso deixar de referir o Centro de Engenharia Biológica (que tem sido uma segunda casa nos últimos anos) e todos os que dele fazem parte. A todos os outros meus amigos e em especial à Célia Fortuna, Lília Marques, Liliana Maia, Madalena Maia, Marino Maciel, Natália Martins, Paulo Silva, e Sara Pimenta pela amizade sincera. Terrie Scherer, I will never forget your kindness and friendship. Não poderia de deixar de fazer um agradecimento especial aos meus Pais, Irmão e Avós por serem o meu porto de abrigo, pelos valores transmitidos, pelos meios que sempre me proporcionaram, pela força e pela coragem que sempre me incutiram para seguir em frente e realizar este sonho. E por fim, a ti, Pedro Silva quero agradecer-te por todos os teus gestos de amor, que se refletiram na infinita paciência, compreensão e apoio moral que sempre me mostraste em todos os momentos. A todos, enfim, reitero o meu apreço e a minha eterna gratidão. v vi Scientific outputs Under the terms of the Decree of Law 74/2006, article 34º, point 1, published in Diário da República, 1ª série, nº60, in 24 of March 2006, altereded by the Decree of Law 11/2013, published in Diário da República, 1ª série, nº151, in 7 of August 2013, that proceeds the 3rd alteration of Decree of Law 74/2006, the author hereby declared that has actively participated in the design and technical execution of the work, interpretation of the results and manuscript preparation of the original articles included in this thesis. Under the terms of the referred Decreto-Lei, the author hereby declared that the following original articles/communications were prepared in the scope of this thesis. Papers in peer reviewed journals Castro J, França A, Bradwell KR, Serrano MG, Jefferson KK, Cerca N (2017). Comparative transcriptomic analysis of Gardnerella vaginalis biofilms versus planktonic cultures using RNA-seq. NPJ Biofilms Microbiomes 3:3 (doi: 10.1038/s41522-017-0012-7). Castro J, Machado D, Cerca N (2016). Escherichia coli and Enterococcus faecalis are able to incorporate and enhance a pre-formed Gardnerella vaginalis biofilm. Pathogens and Disease 74:3 (doi: 10.1093/femspd/ftw007). Castro J, Cerca N (2015). BV and non-BV associated Gardnerella vaginalis establish similar synergistic interactions with other BV-associated microorganisms in dual-species biofilms. Anaerobe 36:56-9 (doi: 10.1016/j.anaerobe.2015.10.008). Castro J, Alves P, Sousa C, Cereija TB, França A, Jefferson KK, Cerca N (2015). Using an in-vitro biofilm model to assess the virulence potential of bacterial vaginosis or non- bacterial vaginosis Gardnerella vaginalis isolates. Scientific Reports 5:11640 (doi: 10.1038/srep11640). Book chapter Castro J, Machado D, Cerca N (2015), “Gardnerella vaginalis gene expression in biofilms” in Impact of biofilms in health: a transcriptomics perspective (Ed. Cerca N) 227-243, Universidade do Minho – DEB, Braga, Portugal, ISBN: 978-989-97478-6-9. Oral presentations Castro J, Cerca N* (2018). The microbiome during bacterial vaginosis: who is cooperating with Gardnerella vaginalis in enhancing crucial gene expression in a dual-species vii biofilm model? IUSTI, 2018 Word + European Congress, 27th – 30th June, Dublin, Ireland (*presenting author). Castro J*, Cerca N (2018). Bacterial cooperation in Bacterial Vaginosis: are social interactions relevant to enhance Gardnerella vaginalis virulence? First Meeting of the PhD in Biomedical Sciences, Instituto de Ciências Biomédicas Abel Salazar, 7th May, Porto, Portugal (*presenting author). Castro J, Machado D, Cerca N* (2017). Can cooperation within the vaginal microbiome lead to the development of bacterial vaginosis? NZ Microbiological Society (NZMS) Conference, 20th – 23rd November, Auckland, New Zealand (*presenting author). Castro J*, França A, Bradwell KR, Serrano MG, Jefferson KK, Cerca N (2016). What happens to Gardnerella vaginalis when growing as a biofilm: a comparative transcriptomic analysis by RNA-seq. Biofilms 7 - Microbial Works of Art. No. SPM: 3, ISBN: 978- 989-97478-7-6, 26th – 28th June, Porto, Portugal (*presenting author). Poster presentations Castro J, Cerca N* (2018). Can the differential response to innate immune components by commensal and clinical Gardnerella vaginalis isolates be the key leading to the development of bacterial vaginosis? IUSTI, 2018 Word + European Congress, 27th – 30th June, Dublin, Ireland (*presenting author). Castro J*, França A, Bradwell KR, Serrano MG, Jefferson KK, Cerca N (2016). The bacterial vaginosis riddle: how transcriptomics can highlight key physiological adaptations of G. vaginalis when growing as biofilms? The New Microbiology - EMBO|FEBS Lecture course, 24th August – 1st September, Spetses, Greece (*presenting author). Castro J*, Machado D, Cerca N (2015). Assessing synergistic interaction between Gardnerella vaginalis and other urogenital pathogens. Eurobiofilms 2015: Fourth European Congress on Microbial Biofilms, 23rd – 26th June, Brno, Czech Republic (*presenting author). viii Determinação do potencial patogénico de isolados clínicos e comensais de Gardnerella vaginalis Sumário No último meio século, a vaginose bacteriana (VB) tem sido um tema controverso na microbiologia médica. Curiosamente, apesar de todo interesse e investigação no campo da VB, o agente etiológico ainda não foi definitivamente identificado. Os primeiros estudos realizados nesta área sugeriram que o agente infecioso causador da VB era a Gardnerella vaginalis. No entanto, de acordo com dados posteriores descobriu-se que G. vaginalis também estava presente em mulheres saudáveis. Tais descobertas levantaram dúvidas acerca do papel desta bactéria como agente etiológico na VB. Além disso, existem evidências que G. vaginalis não é capaz de causar VB de forma consistente. É de salientar, que outras espécies bacterianas também têm sido, comumente, associadas à VB. Tal facto, levou à postulação da teoria polimicrobiana para o desenvolvimento desta infeção. No entanto, dados epidemiológicos subsequentes também revelaram inconsistências com esta última teoria. Recentemente, surgiram as primeiras descrições dos biofilmes polimicrobianos de VB. Interessantemente, a G. vaginalis parece constituir a maior parte da biomassa desses biofilmes, que apresentam maior tolerância a estímulos externos. Estas descobertas levaram à formulação de uma nova hipótese, que sugere que variantes de estirpes de G. vaginalis com capacidade de induzir um biofilme podem, de facto, ser o agente causador de VB. Assim, numa tentativa de compreender as diferenças
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