Impact of urbanization on the structuration of bacterial communities built from spillovers and coalescence processes leading to an emergence of synurbic strains

Résumé

Urbanization is an expanding process leading to a wide variety of urban morphologies and typologies which are matching social functions. The incidence of these organizations on the urban microbiology of outdoor surface environments remains to be characterized. A few reports presented recurrent bacterial taxa among cities and highlighted the presence of some human pathogens. However, the structuring processes of bacterial communities colonizing city surfaces remain poorly understood including the identification of the metabolic properties at the origin of the success of some bacterial taxa able to face the strong selective pressures induced by urban living conditions. This thesis explored the hypothesis of an emergence of reproducible urban outdoor surface microbiomes structured by socio-urbanistic parameters that would lead to the emergence of synurbic bacterial strains (i.e. adapted to urban living conditions). Deep socio-urbanistic surveys of two morphologies (industrial and city-center) were performed in order to characterize urban parameters and human activities that had a strong impact on the bacterial community structuring processes. In parallel, the bacterial communities of city surfaces were investigated by culture dependent and DNA-based approaches (qPCR and metabarcoding) with runoff waters used as proxies of the diversity found over delineated urban sub-catchments. Metabarcoding analyses were carried out using the universal 16S rRNA gene (classification at the genus level) and the tpm marker (developed during this thesis) allowing the discrimination of species and subspecie of genera belonging the gamma-proteobacteria, especially the Pseudomonas and Aeromonas. The inferred urban surface bacterial communities were found to be structured following the r/K ecological principle with (1) K-strategists forming core (i.e. highly recurrent among cities) and flexible sub-cores (i.e. specialists of one urban form) microbiomes, and (2) r-strategists representing opportunistic taxa whose the abundance was related to particular nutrient or chemical spillovers. The inferred core microbiome (K-strategists) was found to be made by about thirty genera including the Pseudomonas. The development of the tpm gene as a metabarcoding marker allowed to refine the understanding of these distribution patterns and to identify key synurbic species like P. koreensis and the human opportunistic pathogen P. aeruginosa. Structure of urban outdoor surface bacterial communities was found related to some socio-urbanistic parameters (e.g. high traffic, occurrences of wastes). To illustrate, r-strategists taxa such as Novosphingobium or Sulfurospirillum showed environmental bursts (almost half of the total bacteria) in line with a chemical spill near their sampling sites. Areas highly impacted by petroled engines showed higher rates of several genera of Actinobacteria, and of the P. stutzeri and P. extremaustralis species which are all known to be implicated in hydrocarbon degradation process. High tpm read numbers affiliated to the highly virulent P. aeruginosa PA7 clade were also recorded over city surfaces impacted by motorized trafic. The peculiar distribution patterns of P. aeruginosa led to the isolation and sequencing of almost 100 genomes of urban isolates. This allowed the characterization of a mobile genetic element involved in the degradation of alkanes among genomes of synurbic P. aeruginosa. Isolates of these synurbic P. aeruginosa and those of the PA7 clade were found cytotoxic towards A549 pulmonary cells.

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