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Metaproteomics Analysis to Study Functionalities of the Gut Microbiota in Large Cohorts

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Metaproteomics Analysis to Study Functionalities of the Gut Microbiota in Large Cohorts SORBONNE UNIVERSITÉS DOCTORAL THESIS Metaproteomics analysis to study functionalities of the gut microbiota in large cohorts Author: Directed by: Ariane BASSIGNANI Dr. Catherine JUSTE Supervised by: Dr. Sandra PLANCADE Dr. Magali BERLAND Thesis jury: President Pr. Alessandra CARBONE Referee Dr. Jean ARMENGAUD Referee Dr. Delphine PFLIEGER Examiner Pr. Laurence SABATIER Examiner Pr. Alain DENISE A thesis submitted in fulfilment of the requirements for the degree of PhD in Bioinformatics in the Unités MetaGenoPolis, Micalis and MaIAGE Institut National de la Recherche Agronomique Publicly defended the 30th of September 2019 ii “Qui acquiert science s’acquiert du travail et du tourment.” Pierre Charron, Le traité de la sagesse “Pour frayer un sentier nouveau, il faut être capable de s’égarer.” Jean Rostand, Inquiétudes d’un biologiste “Je ne crois pas qu’il ait besoin d’être immortel. Je crois que tout ce qui lui faut, c’est écrire la bonne histoire. Parce que certaines histoires sont immortelles.” Stephen King, Le Chant de Susannah iii SORBONNE UNIVERSITÉS Abstract École Doctorale Physiologie, Physiopathologie et Thérapeutique Institut National de la Recherche Agronomique PhD Metaproteomics analysis to study functionalities of the gut microbiota in large cohorts by Ariane BASSIGNANI Metaproteomics focuses on identifying and quantifying proteins in complex bio- logical samples such as the human gut microbiota. Currently, only few studies on human gut microbiota exceed tens of subjects. The analysis of several hundred of samples is nevertheless of interest given the growing recognition of the gut mi- crobiota as a health partner. However, the methods and protocols used so far in proteomics and metaproteomics are not suitable for large-scale studies, whether in terms of time/memory consumption or calibration of parameters. We have therefore developed algorithms, evaluated and compared several identification approaches for peptides and proteins and proposed systematic evaluation criteria, with a partic- ular interest in the replicability of identifications, in order to develop a pre-treatment pipeline suitable for wide-ranging studies. The systematic comparison of these ap- proaches of identification as well as the study of the replicability bring a method- ological base so far missing in the field of the metaproteomics of the human gut mi- crobiota. Quantification of peptides and proteins by eXtracted Ion Chromatogram has never been performed on this type of data, we have also compared normal- ization methods and developed a methodology for imputing missing data to refine the abundance estimations obtained by the more classical method known as "Spec- tral Counting". This thesis work has highlighted microbial biomarkers of potential interest for predicting the response to a slimming diet, or to characterize various phenotypes of inflammatory bowel disease. We have also been able to analyse the metaproteome of more than 200 patients in the framework of the ProteoCardis ANR, which is ancillary to the European project MetaCardis, and which focuses on the potential link between gut microbiota and cardiovascular diseases. The search for proteins of interest among these data should allow us to discover protective or ag- gravating candidate biomarkers of cardiovascular diseases. v SORBONNE UNIVERSITÉS Résumé École Doctorale Physiologie, Physiopathologie et Thérapeutique Institut National de la Recherche Agronomique PhD Analyse métaprotéomique pour l’étude des fonctionnalités du microbiote intestinal dans de grandes cohortes par Ariane BASSIGNANI La métaprotéomique s’attache à identifier et quantifier les protéines d’échantillons biologiques complexes comme le microbiote intestinal humain. Actuellement, peu d’études sur le microbiote intestinal humain dépassent quelques dizaines de su- jets. L’analyse de plusieurs centaines d’échantillons revêt pourtant un intérêt évident compte tenu de la reconnaissance croissante du microbiote intestinal en tant que par- tenaire santé. Cependant, les méthodes et protocoles utilisés jusqu’à ce jour en pro- téomique et métaprotéomique ne sont pas adaptés à des études de grande ampleur, que ce soit en terme de temps/mémoire ou de calibrage des paramètres. Nous avons donc développé des algorithmes, évalué et comparé plusieurs approches d’identifi- cation des peptides et protéines et proposé des critères d’évaluation systématiques, avec un intérêt particulier porté sur la réplicabilité des identifications, afin de dé- velopper un pipeline de prétraitement adapté à des études d’envergure. La com- paraison systématique de ces approches d’identification ainsi que l’étude de la ré- plicabilité apportent un socle méthodologique jusqu’ici manquant dans le domaine de la métaprotéomique du microbiote intestinal humain. La quantification des pep- tides et protéines par eXtracted Ion Chromatogram n’ayant jamais été réalisée sur ce type de données, nous avons également comparé des méthodes de normalisation et développé une méthodologie d’imputation des données manquantes permettant d’affiner les estimations d’abondances obtenues par la méthode plus classique dite « de Spectral Counting ». Ce travail de thèse a permis de mettre en évidence des biomarqueurs microbiens potentiellement d’intérêt pour prédire la réponse à un ré- gime amaigrissant, ou encore pour caractériser différents phénotypes de maladies inflammatoires chroniques de l’intestin. Nous avons également pu analyser le mé- taprotéome de plus de 200 patients dans le cadre de l’ANR ProteoCardis adossée au projet européen MetaCardis, et s’intéressant au lien possible entre microbiote in- testinal et maladies cardiovasculaires. La recherche de protéines d’intérêt parmi ces données devrait permettre de découvrir des candidats biomarqueurs protecteurs ou aggravants de maladies cardiovasculaires. vii Remerciements Tout d’abord, je souhaite remercier les membres de mon jury, qui ont accepté de venir écouter le fruit de mes trois dernières années de travail. Je suis particulière- ment reconnaissante envers Jean Armengaud et Delphine Pflieger, qui ont la lourde tâche de relire ce mémoire. J’espère que la lecture sera agréable, et que ma présenta- tion vous intéressera. Merci à Catherine, qui a dirigé ma thèse avec beaucoup d’implication. Je serai toujours impressionnée par ta volonté de vouloir tout comprendre et tout essayer, et par la passion qui t’anime dans ton travail. Merci à Sandra pour ta patience, surtout quand il s’agit de me faire comprendre des concepts mathématiques. Merci à Magali pour ton côté calmant, et pour voir toujours le bon côté des choses. ch Merci à Olivier et Melisande, mes co-encadrants "non-officiels". Je ne com- prendrais probablement encore rien à la protéomique si je n’avais pas pu apprendre grâce à vous. Cela vaut aussi pour Michel, Thierry, Filippo, et Marlène. En dehors de l’apport scientifique, je m’engage à passer plus souvent vous voir pour prendre un café et philosopher sur le sens de la vie ou le week-end de Marlène, mais pas aller à la cantine, car (i) c’est dégueulasse et (ii) Thierry ne parle que de spectrométrie de masse en mangeant. Merci aux autres membres du Moulon pour leur accueil, les discussions à la cafet’, les food-truck et le Père-Noël secret : Alice, Emmanuelle, Gaëlle, Julie (petit ange parti trop tôt dans le sud), Yannick, Anthony, Harry, Dorian et Pierre. Je n’oublie pas le coin fumeur, avec Xavier, Arnaud et Adrien. Vient le tour de MetaGenoPolis, ou MGP, ou "la famille". Parce que oui, c’est comme ça qu’on se sent là-bas. Je n’aurais pu rêver meilleurs collègues pour passer cette thèse, car dans le meilleur comme dans le pire, aller au labo a toujours été un plaisir, et vous voir tous les jours parfois un soulagement. Merci à Nicolas Maziers pour les discussions philosophiques au retour de la cantine, à Kevin Kweiszer pour m’avoir sauvé du pétrin plus d’une fois (rm -r * tmtc), Florence Thirion pour ses réflexions acérées. Merci à Florence Haimet, qui s’occupe de nous comme d’une maman et dont les compétences en botanique sont impressionnantes. Merci à Sébastien pour avoir toujours le sourire. Merci à Léonard pour nous faire partager ses idées complètement cinglées (et bon courage pour ta thèse). Merci à Parfait pour ses anecdotes toujours délirantes; sérieux, on pourrait faire un film avec tes aventures. Merci à Océane, dont la capacité à bitcher donne toujours des pauses clopes hilarantes. Merci à Matthieu, qui a une capacité incroyable à me faire taper des fous-rires. Merci à Samar pour ta gentillesse et ton soutien moral. Merci à Susie pour être aussi drôle, j’espère te revoir à La Réunion, ou quand tu reviendras sur Paris. Merci à Victoria pour tes conseils et ton franc-parler. Merci viii à Laurie pour être une personne sincère, honnête et drôle (même si je ne sais pas comment tu fais pour dormir si peu). Merci à Anne-Sophie pour ta gentillesse, et pour ne pas nous avoir oublié après être partie du labo, ça me fait toujours autant plaisir de te voir pendant les pique-nique du soir. Merci à Hugo pour être aussi passionné par ton travail (mais arrête d’en parler quand tu as trop bu). Merci à Alexandre pour les pauses-clopes et les soirées. Merci à Fatou pour être aussi épuisée par le fait de vivre, ça me fait toujours autant rire. Merci à Florian pour être une personne avec qui on peut avoir des discussions extrêmement sérieuse, et extrêmement délirante. Je compte sur toi pour la création future du poulailler de MGP. Merci à Franck pour tes enseignements en bash, pour le badminton avec tout ce qui nous passe sous la main, pour evotar et pour tous nos petits délires. Merci à Hanna pour être un sage chinois un peu dingo. Merci à Nicolas Pons pour ton aide dans le travail, les BBQ et le week-end MGP, mais aussi parce que tu es une bonne personne. Mais arrête de travailler autant. Merci à Magali (encore), pour ta patience dans le travail, et surtout de toujours avoir cru en moi, même quand je n’y croyais pas moi-même.
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