Distinct Transcriptome and Traits of Freshly Dispersed Cells

Overview

Journal mSphere

Publisher American Society for Microbiology

Specialties Microbiology
Parasitology

Date 2024 Nov 27

PMID 39601567

Authors

Manmohit Kalia

Karin Sauer

Affiliations

Soon will be listed here.

Abstract

Importance: Dispersion is considered a transitionary phenotype, enabling bacteria to switch between the communal, biofilm lifestyle, where cells share resources and are protected from harmful conditions to the planktonic state. Here, we demonstrate that within minutes of leaving the biofilm, dispersed cells express genes and display phenotypic traits that are distinct from biofilms and planktonic cells. Our findings suggest that dispersed cells quickly adapt to a less structured and protected but more nutrient-rich environment, with this trade-off in environment coinciding with an awakening and a switch in virulence, specifically a switch from directly intoxicating host cells and potential competitors toward more broadly active virulence factors and strategies of evasion. To our knowledge, this is the first report of dispersed cells' distinct (trade-off) phenotype and their enhanced resilience so soon after egressing from the biofilm.

References

Matsuura M . Structural Modifications of Bacterial Lipopolysaccharide that Facilitate Gram-Negative Bacteria Evasion of Host Innate Immunity. Front Immunol. 2013; 4:109. PMC: 3662973. DOI: 10.3389/fimmu.2013.00109. View

Ryjenkov D, Tarutina M, Moskvin O, Gomelsky M . Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol. 2005; 187(5):1792-8. PMC: 1064016. DOI: 10.1128/JB.187.5.1792-1798.2005. View

Fleming D, Rumbaugh K . The Consequences of Biofilm Dispersal on the Host. Sci Rep. 2018; 8(1):10738. PMC: 6048044. DOI: 10.1038/s41598-018-29121-2. View

Petrova O, Sauer K . Dispersion by Pseudomonas aeruginosa requires an unusual posttranslational modification of BdlA. Proc Natl Acad Sci U S A. 2012; 109(41):16690-5. PMC: 3478618. DOI: 10.1073/pnas.1207832109. View

Cooke A, Florez C, Dunshee E, Lieber A, Terry M, Light C . Quinolone Signal-Induced Outer Membrane Vesicles Enhance Biofilm Dispersion in Pseudomonas aeruginosa. mSphere. 2020; 5(6). PMC: 7690959. DOI: 10.1128/mSphere.01109-20. View

Li Y, Petrova O, Su S, Lau G, Panmanee W, Na R . BdlA, DipA and induced dispersion contribute to acute virulence and chronic persistence of Pseudomonas aeruginosa. PLoS Pathog. 2014; 10(6):e1004168. PMC: 4047105. DOI: 10.1371/journal.ppat.1004168. View

Kalia M, Resch M, Cherny K, Sauer K . The Alginate and Motility Regulator AmrZ is Essential for the Regulation of the Dispersion Response by Biofilms. mSphere. 2022; 7(6):e0050522. PMC: 9769550. DOI: 10.1128/msphere.00505-22. View

Chambers J, Cherny K, Sauer K . Susceptibility of Pseudomonas aeruginosa Dispersed Cells to Antimicrobial Agents Is Dependent on the Dispersion Cue and Class of the Antimicrobial Agent Used. Antimicrob Agents Chemother. 2017; 61(12). PMC: 5700346. DOI: 10.1128/AAC.00846-17. View

Dow J, Fouhy Y, Lucey J, Ryan R . The HD-GYP domain, cyclic di-GMP signaling, and bacterial virulence to plants. Mol Plant Microbe Interact. 2006; 19(12):1378-84. DOI: 10.1094/MPMI-19-1378. View

10.

Barraud N, Schleheck D, Klebensberger J, Webb J, Hassett D, Rice S . Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol. 2009; 191(23):7333-42. PMC: 2786556. DOI: 10.1128/JB.00975-09. View

11.

Mah T, Pitts B, Pellock B, Walker G, Stewart P, OToole G . A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature. 2003; 426(6964):306-10. DOI: 10.1038/nature02122. View

12.

Cherny K, Sauer K . Pseudomonas aeruginosa Requires the DNA-Specific Endonuclease EndA To Degrade Extracellular Genomic DNA To Disperse from the Biofilm. J Bacteriol. 2019; 201(18). PMC: 6707924. DOI: 10.1128/JB.00059-19. View

13.

Huynh T, McDougald D, Klebensberger J, Al Qarni B, Barraud N, Rice S . Glucose starvation-induced dispersal of Pseudomonas aeruginosa biofilms is cAMP and energy dependent. PLoS One. 2012; 7(8):e42874. PMC: 3419228. DOI: 10.1371/journal.pone.0042874. View

14.

An S, Wu J, Zhang L . Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-Di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl Environ Microbiol. 2010; 76(24):8160-73. PMC: 3008239. DOI: 10.1128/AEM.01233-10. View

15.

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

16.

Berne C, Ellison C, Ducret A, Brun Y . Bacterial adhesion at the single-cell level. Nat Rev Microbiol. 2018; 16(10):616-627. DOI: 10.1038/s41579-018-0057-5. View

17.

Dasgupta N, Wolfgang M, Goodman A, Arora S, Jyot J, Lory S . A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol. 2003; 50(3):809-24. DOI: 10.1046/j.1365-2958.2003.03740.x. View

18.

Basu Roy A, Sauer K . Diguanylate cyclase NicD-based signalling mechanism of nutrient-induced dispersion by Pseudomonas aeruginosa. Mol Microbiol. 2014; 94(4):771-93. PMC: 4227967. DOI: 10.1111/mmi.12802. View

19.

Rumbaugh K, Sauer K . Biofilm dispersion. Nat Rev Microbiol. 2020; 18(10):571-586. PMC: 8564779. DOI: 10.1038/s41579-020-0385-0. View

20.

Spindler E, Hale J, Giddings Jr T, Hancock R, Gill R . Deciphering the mode of action of the synthetic antimicrobial peptide Bac8c. Antimicrob Agents Chemother. 2011; 55(4):1706-16. PMC: 3067151. DOI: 10.1128/AAC.01053-10. View