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Type-IV pili tune an adhesion-migration trade-off during surface colonization of Pseudomonas aeruginosa

Ahmet Nihat Simsek, Matthias D. Koch, Joseph E. Sanfilippo, Zemer Gitai, View ORCID ProfileGerhard Gompper, View ORCID ProfileBenedikt Sabass
doi: https://doi.org/10.1101/2023.05.09.538458
Ahmet Nihat Simsek
1Theoretical Physics of Living Matter, Institute of Biological Information Processes, Forschungszentrum Jülich, 52425 Jülich, Germany
2Institute for Infectious Diseases and Zoonoses, Department of Veterinary Sciences, Ludwig-Maximilians-Universität München, 80752 Munich, Germany
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Matthias D. Koch
3Department of Biology, Texas A&M University, College Station, Texas 77843, USA
4Lewis-Sigler Institute for Integrative Genomics, Princeton University, NJ 08544, USA
5Department of Molecular Biology, Princeton University, NJ 08544, USA
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Joseph E. Sanfilippo
6Department of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
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Zemer Gitai
5Department of Molecular Biology, Princeton University, NJ 08544, USA
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Gerhard Gompper
1Theoretical Physics of Living Matter, Institute of Biological Information Processes, Forschungszentrum Jülich, 52425 Jülich, Germany
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Benedikt Sabass
1Theoretical Physics of Living Matter, Institute of Biological Information Processes, Forschungszentrum Jülich, 52425 Jülich, Germany
2Institute for Infectious Diseases and Zoonoses, Department of Veterinary Sciences, Ludwig-Maximilians-Universität München, 80752 Munich, Germany
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  • ORCID record for Benedikt Sabass
  • For correspondence: benedikt.sabass@gmx.de
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Abstract

Bacterial pathogenicity relies on both firm surface adhesion and cell dissemination. How twitching bacteria resolve the fundamental contradiction between adhesion and migration is unknown. To address this question, we employ live-cell imaging of type-IV pili (T4P) and therewith construct a comprehensive mathematical model of Pseudomonas aeruginosa migration. The data show that only 10% to 50% of T4P bind to substrates and contribute to migration through random extension and retraction. Individual T4P do not display a measurable sensory response to surfaces, but their number increases on cellular surface contact. Attachment to surfaces is mediated, besides T4P, by passive adhesive forces acting on the cell body. Passive adhesions slow down cell migration and result in local random motion on short time scales, which is followed by directionally persistent, superdiffusive motion on longer time scales. Moreover, passive adhesions strongly enhance surface attachment under shear flow. ΔpilA mutants, which produce no T4P, robustly stick to surfaces under shear flow. In contrast, rapidly migrating ΔpilH cells, which produce an excessive number of T4P, are easily detached by shear. Wild-type cells sacrifice migration speed for robust surface attachment by maintaining a low number of active pili. The different cell strains pertain to disjunct regimes in a generic adhesion-migration trait space. Depending on the nature of the adhesion structures, adhesion and migration are either compatible or a trade-off is required for efficient bacterial surface colonization under different conditions.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵† b.sabass{at}fz-juelich.de

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Posted May 09, 2023.
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Type-IV pili tune an adhesion-migration trade-off during surface colonization of Pseudomonas aeruginosa
Ahmet Nihat Simsek, Matthias D. Koch, Joseph E. Sanfilippo, Zemer Gitai, Gerhard Gompper, Benedikt Sabass
bioRxiv 2023.05.09.538458; doi: https://doi.org/10.1101/2023.05.09.538458
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Type-IV pili tune an adhesion-migration trade-off during surface colonization of Pseudomonas aeruginosa
Ahmet Nihat Simsek, Matthias D. Koch, Joseph E. Sanfilippo, Zemer Gitai, Gerhard Gompper, Benedikt Sabass
bioRxiv 2023.05.09.538458; doi: https://doi.org/10.1101/2023.05.09.538458

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