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Bacterial Inter-Species Communication Mediated By BACTERIAL INTER-SPECIES COMMUNICATION MEDIATED BY THE AUTOINDUCER-2 SIGNAL Catarina Sim-Sim Pereira Oeiras, July 2011 Bacterial Signaling Group Instituto Gulbenkian de Ciência Instituto de Tecnologia Química e Biológica Rua da Quinta Grande, 6 P-2780-156 Oeiras Portugal Supervisor: Karina de Bivar Xavier Examiners: Prof. Dieter Haas, Prof. Carlos São-José, Prof. Cecília M. Arraiano and Prof. Carlos Romão. Dissertation presented to obtain the Ph.D degree in Biology by Universidade Nova de Lisboa, Instituto de Tecnologia Química e Biológica, Instituto Gulbenkian de Ciência. iii From left to right: Dieter Haas, Karina B. Xavier, Catarina S. Pereira, Carlos São-José, Carlos Romão. Cecília M. Arraiano. Oeiras, 8th July 2011 iv ACKNOWLEDGEMENTS First and foremost I thank my supervisor Karina. She has given me enormous support, great opportunities and true friendship through all the years of this research. I am thankful for her excellent model as a scientist and above all as a person. The passion and persistence she has in solving nature puzzles was motivational for me, even during difficult periods in my Ph.D quest. I feel truly honored to be her first Ph.D student. To the members of the best group ever, the bacterial signaling group, who have contributed immensely not only to this thesis but also to my personal time at the IGC. The group has been a source of good mood as well as excellent collaboration and insightful (sometimes endless) scientific discussions. To start with (and also to end with!) I thank the most persistent member of the group João: for his days of good humor and also for the ones of bad that always pushed me to be optimistic! To Michal: “Let’s go for a ‘meia de leite?’”, thanks for all our conversations about the present and future of scientific life as well as of motherhood. To António: it was an enormous pleasure to work with you and I am sure that such a great person as you will succeed in all the areas of your life. To Bruno, the noisiest member of the lab: thank you for reminding me always what is true enthusiasm for science and also for your companionship. To Rita: whom I was proud to teach and I am thankful for not letting me pass a day without a good and loud laugh. To Paulo: for helping me in the PTS quest. To Pol and Jess for elevating the parameter of good mood in the lab (which was already very high). A very special thanks to Jess for reviewing this thesis and thanks to other past and present group members: Daniel, Andreia and Fabio. I also thank the IGC for providing a great scientific environment and the Fundação para a Ciência e Tecnologia for their financial support with the grant SFRH / BD / 28543 / 2006. v There are people that made me grow as a scientist and without whom this thesis would not be the same, therefore, I am very thankful to: - Bonnie Bassler, my grandmother in science, and all her lab, where I first met the Quorum-sensing world; - Graham Walker and his group at MIT, especially Michi Taga, who taught me everything she knows about Sinorhizobium and plants; - Andres Mäe and his group at Tartu University, particularly Liis Andresen who showed me the “magic world of Erwinia”; - Jörg Becker for helping me with the Sinorhizobium microarrays; - Prof. Winfried Boos for returning to the lab and doing the experiments for me while I was pregnant, Manuel is also grateful! - Steve for being an excellent collaborator that is always willing to test new ideas; - Members of my thesis committee, Adriano O. Henriques, Miguel Godinho-Ferreira and Sérgio Raposo Filipe for the assistance they provided at all levels of this research project; - Evolutionary Biology lab for the symbiotic scientific relation and for being the best lunch buddies; To Sara and Tania my closest friends in the IGC. To all my friends that make me put things in perspective when an experiment went wrong. You are the best I have! To my family: Para a família do João (ou Miguel) que agora também é minha, pelos bons momentos passados e futuros. Um agradecimento especial à Lena por todo o apoio que tem dado com o Manel. Para o meu avô Manel, tios e primos pela memória sempre presente e pelo exemplo de valores de vida. Para a minha avó Tinita, o Vasco, os meus sobrinhos João e Rita o meu tio Zé Luís, os meus tios Guida e Gino e primas Mariana e Inês por serem uma família maravilhosa. Viva o conde da Guarda! Para a minha AnaMana que me ouve sempre e me dá os melhores conselhos. Para a Tóia e para o Quim com um orgulho imenso de ser vossa filha. vi Para o Manel que me mostrou o melhor da vida. Para o João pelo teu abraço no final do dia. vii viii ABSTRACT During the last few decades, scientists have come to appreciate the immense complexity in bacterial signaling interactions that sustain microbial communities. Quorum-sensing (QS) is a cell-cell communication process whereby single cell bacteria regulate gene expression synchronously in a population in response to self-produced extracellular signal molecules, called autoinducers. Autoinducer-2 (AI-2), the synthase of which, LuxS, is present in both Gram-negative and Gram-positive bacteria, was proposed to represent a non-species-specific signal that mediates inter-species communication. In enteric bacteria, extracellular AI-2 levels peak in late exponential phase and rapidly decline as bacteria continue to grow. This depletion occurs because AI-2 activates the expression of an operon, lsr (for LuxS Regulated), encoding the Lsr transporter and enzymes that degrade the signal. As the Lsr system imports self and non-self AI-2, lsr-containing bacteria can interfere with AI-2 signaling of other species and shut off group behaviors regulated by this molecule: this system represents the first example of interference with a bacterial inter-species QS signal. The main goal of the research reported in this thesis was to characterize the Lsr system and its regulatory networks for AI-2 detection and interference, with the long term aim of increasing understanding of the role of AI-2 inter-species communication in multi-species environments. To identify regulators of the lsr operon a genetic screen was performed in Escherichia coli (Chapter III). This led to the identification of the phosphotransferase system (PTS) as a central player in the regulatory network of the Lsr system. Mutants of components of PTS prevent AI-2 internalization and processing. This phenotype is overcome when the Lsr system is constitutively expressed. Overall, these results indicate that in order to activate its specific transport system, Lsr, PTS-dependent uptake of AI-2 must first occur. As Lsr transport is dependent on the PTS, this suggests a mechanism through which information about the physiological state of bacteria and regulation of AI-2 signal uptake is integrated. ix There are two known AI-2 receptors: LuxP, found in the Vibrio genus and LsrB, first identified in Salmonella enterica subspecies enterica serovar Typhimurium. The research in Chapter IV was designed to determine the occurrence of the Lsr system within all the available bacterial genome sequences. Based on sequence analysis and structure prediction, a set of criteria was established to identify functional LsrB-like AI-2 receptors. Bioinformatic predictions were confirmed experimentally by assaying selected species for AI-2 internalization in vivo, and testing their LsrB orthologs for AI- 2 binding in vitro. The presence of functional AI-2 receptors in the phylogenetically distant families Enterobacteriaceae, Rhizobiaceae, and Bacillaceae was thus demonstrated. Furthermore, it was shown that two residues that interact with AI-2 (D166 and A222) were conserved in all the LsrB orthologs analyzed and proved essential for AI-2 binding ability. Additionally, the evolutionary history of the lsrB gene was studied by phylogenetic analysis which suggests a single LsrB origin in a common ancestor of the Enterobacteriales and Pasteurellales families with two subsequent events of lateral gene transfer. These results provide a method for identifying and validating functional LsrB-type AI-2 receptors, an important step to the understanding of the molecular basis of AI-2-mediated behavioral regulation in a variety of new species. Chapter V details the characterization of the Lsr system from a non-AI- 2 producer, the plant symbiont Sinorhizobium meliloti. Sequence analysis revealed that S. meliloti has orthologs of all the proteins of the AI-2- inteference Lsr system found in enteric bacteria: this operon could be similarly involved in AI-2 sequestration and degradation. Accordingly, transcription of this operon is induced by AI-2 and this microorganism can completely eliminate the AI-2 secreted by Erwinia carotovora, a plant pathogen shown to use AI-2 to regulate virulence, while lsrK mutant cannot. Moreover the transcriptional profile shows that, in the conditions tested, apart from inducing transcription of its own incorporation and processing system, the presence of the AI-2 signal in S. meliloti cultures does not regulate expression of any other genes. These findings suggest that S. meliloti is capable of x ‘eavesdropping’ on the AI-2 signaling of other species and interfering with AI- 2-regulated phenotypes, possibly gaining a benefit in colonization of niches containing multiple species of bacteria The mechanisms by which microorganisms interfere with other species ability to communicate, for example, through the Lsr system studied in this research, can be exploited to design new clinical and biotechnological strategies towards the manipulation of bacterial behaviors such as virulence. xi xii RESUMO Nas últimas décadas, a noção de comportamento bacteriano alterou-se drasticamente.
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