Evolutionary rescue of spherical mreB deletion mutants of the rod-shape bacterium Pseudomonas fluorescens SBW25

Author:

Yulo P Richard J1ORCID,Desprat Nicolas234ORCID,Gerth Monica L5ORCID,Ritzl-Rinkenberger Barbara67,Farr Andrew D8ORCID,Liu Yunhao5ORCID,Zhang Xue-Xian1ORCID,Miller Michael1ORCID,Cava Felipe67ORCID,Rainey Paul B589ORCID,Hendrickson Heather L110ORCID

Affiliation:

1. Institute of Natural and Mathematical Science, Massey University

2. Laboratoire de Physique de l’ENS, Ecole Normale Supérieure, PSL Research University; Université Paris-Cité; Sorbonne Universités; CNRS; 24 rue Lhomond

3. Institut de biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University

4. Université Paris Cité

5. New Zealand Institute for Advanced Study, Massey University

6. Department of Molecular Biology, Umeå University

7. Laboratory for Molecular Infection Medicine Sweden, Umeå Centre for Microbial Research, SciLifeLab, Umeå Centre for Microbial Research, Umeå University

8. Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology

9. Laboratoire Biophysique et Évolution, CBI, ESPCI Paris, Université PSL

10. School of Biological Sciences, University of Canterbury

Abstract

Maintenance of rod-shape in bacterial cells depends on the actin-like protein MreB. Deletion of mreB from Pseudomonas fluorescens SBW25 results in viable spherical cells of variable volume and reduced fitness. Using a combination of time-resolved microscopy and biochemical assay of peptidoglycan synthesis we show that reduced fitness is a consequence of perturbed cell size homeostasis that arises primarily from differential growth of daughter cells. A 1,000-generation selection experiment resulted in rapid restoration of fitness with derived cells retaining spherical shape. Mutations in the peptidoglycan synthesis protein Pbp1A were identified as the main route for fitness restoration with genetic reconstructions demonstrating causality. The pbp1A mutations targeting transpeptidase activity enhance homogeneity in cell wall synthesis on lateral surfaces, thus restoring cell size homeostasis in the population. Together our experimental approach emphasizes the new knowledge to be gained from strategies that exploit the power of natural selection to rescue fitness-compromised mutants.

Publisher

eLife Sciences Publications, Ltd

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