Reversible adhesion by type IV pili leads to formation of permanent localized clusters
María Victoria Pepe,
Celeste Dea,
Camila Genskowsky,
Darío Capasso,
Mara Sabrina Roset,
Adriana Valeria Jäger,
Fernando Peruani,
Arlinet Kierbel
Affiliations
María Victoria Pepe
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín (UNSAM), CONICET, Buenos Aires B1650HMP, Argentina
Celeste Dea
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín (UNSAM), CONICET, Buenos Aires B1650HMP, Argentina
Camila Genskowsky
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín (UNSAM), CONICET, Buenos Aires B1650HMP, Argentina
Darío Capasso
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín (UNSAM), CONICET, Buenos Aires B1650HMP, Argentina
Mara Sabrina Roset
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín (UNSAM), CONICET, Buenos Aires B1650HMP, Argentina
Adriana Valeria Jäger
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín (UNSAM), CONICET, Buenos Aires B1650HMP, Argentina
Fernando Peruani
Laboratoire de Physique Théorique et Modélisation, UMR 8089, CY Cergy Paris Université, 95302 Cergy-Pontoise, France; Corresponding author
Arlinet Kierbel
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín (UNSAM), CONICET, Buenos Aires B1650HMP, Argentina; Corresponding author
Summary: The formation of long-lived, multicellular clusters is a fundamental step in the physiopathology of many disease-causing bacteria. Experiments on abiotic surfaces suggest that bacterial colonization, including initial cluster formation, requires (1) irreversible adhesion, (2) cell proliferation, and (3) a phenotypic transition. However, here we show that on infection of a polarized MDCK epithelium, Pseudomonas aeruginosa (PA) forms long-lived – i.e., permanent – bacterial clusters without requiring irreversible adhesion, cell proliferation, or a phenotypic transition. By combining experiments and a mathematical model, we reveal that the cluster formation process is mediated by type IV pili (T4P). Furthermore, we unveil how T4P quantitatively operate during adhesion, finding that it is a stochastic process that involves an activation time, requires the retraction of pili, and results in reversible attachment. We explain how such reversible attachment process leads to the formation of permanent bacterial clusters and quantify the cluster growth dynamics.