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Differential impact on motility and biofilm dispersal of closely related phosphodiesterases in Pseudomonas aeruginosa

Differential impact on motility and biofilm dispersal of closely related phosphodiesterases in Pseudomonas aeruginosa
Differential impact on motility and biofilm dispersal of closely related phosphodiesterases in Pseudomonas aeruginosa

In Pseudomonas aeruginosa, the transition between planktonic and biofilm lifestyles is modulated by the intracellular secondary messenger cyclic dimeric-GMP (c-di-GMP) in response to environmental conditions. Here, we used gene deletions to investigate how the environmental stimulus nitric oxide (NO) is linked to biofilm dispersal, focusing on biofilm dispersal phenotype from proteins containing putative c-di-GMP turnover and Per-Arnt-Sim (PAS) sensory domains. We document opposed physiological roles for the genes ΔrbdA and Δpa2072 that encode proteins with identical domain structure: while ΔrbdA showed elevated c-di-GMP levels, restricted motility and promoted biofilm formation, c-di-GMP levels were decreased in Δpa2072, and biofilm formation was inhibited, compared to wild type. A second pair of genes, ΔfimX and ΔdipA, were selected on the basis of predicted impaired c-di-GMP turnover function: ΔfimX showed increased, ΔdipA decreased NO induced biofilm dispersal, and the genes effected different types of motility, with reduced twitching for ΔfimX and reduced swimming for ΔdipA. For all four deletion mutants we find that NO-induced biomass reduction correlates with increased NO-driven swarming, underlining a significant role for this motility in biofilm dispersal. Hence P. aeruginosa is able to differentiate c-di-GMP output using structurally highly related proteins that can contain degenerate c-di-GMP turnover domains.

2045-2322
1-12
Cai, Yu-Ming
475b20b8-ece3-40a4-bcf5-a4670897858c
Hutchin, Andrew
5659cf31-f52e-451e-9cf0-4e786924d1ae
Craddock, Jack
a82f6526-9bd4-4c22-9b25-9d6e84fc7fbc
Walsh, Martin A
c51d771b-68b4-4c84-8906-650fc25bdad3
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Tews, Ivo
9117fc5e-d01c-4f8d-a734-5b14d3eee8dd
Cai, Yu-Ming
475b20b8-ece3-40a4-bcf5-a4670897858c
Hutchin, Andrew
5659cf31-f52e-451e-9cf0-4e786924d1ae
Craddock, Jack
a82f6526-9bd4-4c22-9b25-9d6e84fc7fbc
Walsh, Martin A
c51d771b-68b4-4c84-8906-650fc25bdad3
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Tews, Ivo
9117fc5e-d01c-4f8d-a734-5b14d3eee8dd

Cai, Yu-Ming, Hutchin, Andrew, Craddock, Jack, Walsh, Martin A, Webb, Jeremy S. and Tews, Ivo (2020) Differential impact on motility and biofilm dispersal of closely related phosphodiesterases in Pseudomonas aeruginosa. Scientific Reports, 10 (1), 1-12, [6232]. (doi:10.1038/s41598-020-63008-5).

Record type: Article

Abstract

In Pseudomonas aeruginosa, the transition between planktonic and biofilm lifestyles is modulated by the intracellular secondary messenger cyclic dimeric-GMP (c-di-GMP) in response to environmental conditions. Here, we used gene deletions to investigate how the environmental stimulus nitric oxide (NO) is linked to biofilm dispersal, focusing on biofilm dispersal phenotype from proteins containing putative c-di-GMP turnover and Per-Arnt-Sim (PAS) sensory domains. We document opposed physiological roles for the genes ΔrbdA and Δpa2072 that encode proteins with identical domain structure: while ΔrbdA showed elevated c-di-GMP levels, restricted motility and promoted biofilm formation, c-di-GMP levels were decreased in Δpa2072, and biofilm formation was inhibited, compared to wild type. A second pair of genes, ΔfimX and ΔdipA, were selected on the basis of predicted impaired c-di-GMP turnover function: ΔfimX showed increased, ΔdipA decreased NO induced biofilm dispersal, and the genes effected different types of motility, with reduced twitching for ΔfimX and reduced swimming for ΔdipA. For all four deletion mutants we find that NO-induced biomass reduction correlates with increased NO-driven swarming, underlining a significant role for this motility in biofilm dispersal. Hence P. aeruginosa is able to differentiate c-di-GMP output using structurally highly related proteins that can contain degenerate c-di-GMP turnover domains.

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Accepted/In Press date: 28 February 2020
e-pub ahead of print date: 10 April 2020

Identifiers

Local EPrints ID: 439375
URI: http://eprints.soton.ac.uk/id/eprint/439375
ISSN: 2045-2322
PURE UUID: 3baf5441-fb91-4bcc-9c89-883b6a556ff6
ORCID for Jack Craddock: ORCID iD orcid.org/0000-0001-9193-0366
ORCID for Jeremy S. Webb: ORCID iD orcid.org/0000-0003-2068-8589
ORCID for Ivo Tews: ORCID iD orcid.org/0000-0002-4704-1139

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Date deposited: 20 Apr 2020 16:30
Last modified: 18 Feb 2021 17:28

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Contributors

Author: Yu-Ming Cai
Author: Andrew Hutchin
Author: Jack Craddock ORCID iD
Author: Martin A Walsh
Author: Jeremy S. Webb ORCID iD
Author: Ivo Tews ORCID iD

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