Moonlighting in the matrix
Cynthia B. Whitchurch A B *
+ Author Affiliations
- Author Affiliations
A Quadram Institute Bioscience, Norwich Research Park, Norwich, NR4 7UQ, UK.
B School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK.
Cynthia Whitchurch FAA is a Professor of Microbiology at the Quadram Institute Bioscience. Her research interests are in alternate bacterial lifestyles including biofilms and cell wall deficiency. |
* Correspondence to: cynthia.whitchurch@quadram.ac.uk
Microbiology Australia 44(2) 75-78 https://doi.org/10.1071/MA23022
Submitted: 20 April 2023 Accepted: 11 May 2023 Published: 25 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the ASM. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
The biofilm matrix is a complex, heterogeneous mixture of polymers, macromolecules, small molecules, and higher-order particulate structures. The primary functions of some matrix components are specific for building biofilms. However, there are many components of the biofilm matrix that have primary cellular functions yet provide additional distinct ‘moonlighting’ functions when located in the biofilm matrix. Moonlighting matrix components include proteins and nucleic acids as well as higher-order structures such as membranes and bacteriophage. This review will describe some of the moonlighting matrix components found in Pseudomonas aeruginosa biofilms.
Keywords: bacteriophage, biofilm, BMV, EPC, EPS, eDNA, extracellular DNA, MV, OMV, Pseudomonas, slime.
References
[1] Flemming, H-C et al. (2023) The biofilm matrix: multitasking in a shared space. Nat Rev Microbiol 21, 70–86.| The biofilm matrix: multitasking in a shared space.Crossref | GoogleScholarGoogle Scholar |
[2] Reichhardt, C (2023) The Pseudomonas aeruginosa biofilm matrix protein CdrA has similarities to other fibrillar adhesin proteins. J Bacteriol , e00019-23.
| The Pseudomonas aeruginosa biofilm matrix protein CdrA has similarities to other fibrillar adhesin proteins.Crossref | GoogleScholarGoogle Scholar |
[3] Jeffery, CJ (2014) An introduction to protein moonlighting. Biochem Soc Trans 42, 1679–1683.
| An introduction to protein moonlighting.Crossref | GoogleScholarGoogle Scholar |
[4] Ebner, P and Götz, F (2019) Bacterial excretion of cytoplasmic proteins (ECP): occurrence, mechanism, and function. Trends Microbiol 27, 176–187.
| Bacterial excretion of cytoplasmic proteins (ECP): occurrence, mechanism, and function.Crossref | GoogleScholarGoogle Scholar |
[5] Turnbull, L et al. (2016) Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat Commun 7, 11220.
| Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms.Crossref | GoogleScholarGoogle Scholar |
[6] Whitchurch, CB et al. (2002) Extracellular DNA required for bacterial biofilm formation. Science 295, 1487.
| Extracellular DNA required for bacterial biofilm formation.Crossref | GoogleScholarGoogle Scholar |
[7] Hynen, AL et al. (2021) Multiple holins contribute to extracellular DNA release in Pseudomonas aeruginosa biofilms. Microbiology 167, 000990.
| Multiple holins contribute to extracellular DNA release in Pseudomonas aeruginosa biofilms.Crossref | GoogleScholarGoogle Scholar |
[8] Pingle, H et al. (2018) Minimal attachment of Pseudomonas aeruginosa to DNA modified surfaces. Biointerphases 13, 06E405.
| Minimal attachment of Pseudomonas aeruginosa to DNA modified surfaces.Crossref | GoogleScholarGoogle Scholar |
[9] Toyofuku, M et al. (2012) Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix. J Proteome Res 11, 4906–4915.
| Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix.Crossref | GoogleScholarGoogle Scholar |
[10] Couto, N et al. (2015) Proteome profiles of outer membrane vesicles and extracellular matrix of Pseudomonas aeruginosa biofilms. J Proteome Res 14, 4207–4222.
| Proteome profiles of outer membrane vesicles and extracellular matrix of Pseudomonas aeruginosa biofilms.Crossref | GoogleScholarGoogle Scholar |
[11] Dengler, V et al. (2015) An electrostatic net model for the role of extracellular DNA in biofilm formation by Staphylococcus aureus. J Bacteriol 197, 3779–3787.
| An electrostatic net model for the role of extracellular DNA in biofilm formation by Staphylococcus aureus.Crossref | GoogleScholarGoogle Scholar |
[12] Jeffery, CJ (2018) Protein moonlighting: what is it, and why is it important? Phil Trans R Soc B 373, 20160523.
| Protein moonlighting: what is it, and why is it important?Crossref | GoogleScholarGoogle Scholar |
[13] Goto, M et al. (2003) Induction of apoptosis in macrophages by Pseudomonas aeruginosa azurin: tumour-suppressor protein p53 and reactive oxygen species, but not redox activity, as critical elements in cytotoxicity. Mol Microbiol 47, 549–559.
| Induction of apoptosis in macrophages by Pseudomonas aeruginosa azurin: tumour-suppressor protein p53 and reactive oxygen species, but not redox activity, as critical elements in cytotoxicity.Crossref | GoogleScholarGoogle Scholar |
[14] Novotny, LA et al. (2016) Monoclonal antibodies against DNA-binding tips of DNABII proteins disrupt biofilms in vitro and induce bacterial clearance in vivo. eBioMedicine 10, 33–44.
| Monoclonal antibodies against DNA-binding tips of DNABII proteins disrupt biofilms in vitro and induce bacterial clearance in vivo.Crossref | GoogleScholarGoogle Scholar |
[15] Campoccia, D et al. (2021) Extracellular DNA (eDNA). A major ubiquitous element of the bacterial biofilm architecture. Int J Mol Sci 22, 9100.
| Extracellular DNA (eDNA). A major ubiquitous element of the bacterial biofilm architecture.Crossref | GoogleScholarGoogle Scholar |
[16] Das, T et al. (2011) DNA-mediated bacterial aggregation is dictated by acid–base interactions. Soft Matter 7, 2927–2935.
| DNA-mediated bacterial aggregation is dictated by acid–base interactions.Crossref | GoogleScholarGoogle Scholar |
[17] Seviour, T et al. (2021) The biofilm matrix scaffold of Pseudomonas aeruginosa contains G-quadruplex extracellular DNA structures. NPJ Biofilms Microbiomes 7, 27.
| The biofilm matrix scaffold of Pseudomonas aeruginosa contains G-quadruplex extracellular DNA structures.Crossref | GoogleScholarGoogle Scholar |
[18] Finkel, SE and Kolter, R (2001) DNA as a nutrient: novel role for bacterial competence gene homologs. J Bacteriol 183, 6288–6293.
| DNA as a nutrient: novel role for bacterial competence gene homologs.Crossref | GoogleScholarGoogle Scholar |
[19] Mulcahy, H et al. (2010) Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ Microbiol 12, 1621–1629.
| Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source.Crossref | GoogleScholarGoogle Scholar |
[20] Mulcahy, H et al. (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4, e1000213.
| Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms.Crossref | GoogleScholarGoogle Scholar |
[21] Lewenza, S (2013) Extracellular DNA-induced antimicrobial peptide resistance mechanisms in Pseudomonas aeruginosa. Front Microbiol 4, 21.
| Extracellular DNA-induced antimicrobial peptide resistance mechanisms in Pseudomonas aeruginosa.Crossref | GoogleScholarGoogle Scholar |
[22] Wilton, M et al. (2016) Extracellular DNA acidifies biofilms and induces aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 60, 544–553.
| Extracellular DNA acidifies biofilms and induces aminoglycoside resistance in Pseudomonas aeruginosa.Crossref | GoogleScholarGoogle Scholar |
[23] Das, T et al. (2015) Phenazine virulence factor binding to extracellular DNA is important for Pseudomonas aeruginosa biofilm formation. Sci Rep 5, 8398.
| Phenazine virulence factor binding to extracellular DNA is important for Pseudomonas aeruginosa biofilm formation.Crossref | GoogleScholarGoogle Scholar |
[24] Saunders, SH et al. (2020) Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms. Cell 182, 919–932.e19.
| Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms.Crossref | GoogleScholarGoogle Scholar |
[25] Gloag, ES et al. (2013) Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci USA 110, 11541–11546.
| Self-organization of bacterial biofilms is facilitated by extracellular DNA.Crossref | GoogleScholarGoogle Scholar |
[26] Barken, KB et al. (2008) Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10, 2331–2343.
| Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms.Crossref | GoogleScholarGoogle Scholar |
[27] Schooling, SR and Beveridge, TJ (2006) Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188, 5945–5957.
| Membrane vesicles: an overlooked component of the matrices of biofilms.Crossref | GoogleScholarGoogle Scholar |
[28] Schooling, SR et al. (2009) Interactions of DNA with biofilm-derived membrane vesicles. J Bacteriol 191, 4097–4102.
| Interactions of DNA with biofilm-derived membrane vesicles.Crossref | GoogleScholarGoogle Scholar |
[29] Johnston, EL et al. (2023) Planktonic and biofilm-derived Pseudomonas aeruginosa outer membrane vesicles facilitate horizontal gene transfer of plasmid DNA. Microbiol Spectr 11, e05179-22.
| Planktonic and biofilm-derived Pseudomonas aeruginosa outer membrane vesicles facilitate horizontal gene transfer of plasmid DNA.Crossref | GoogleScholarGoogle Scholar |
[30] Secor, PR et al. (2015) Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe 18, 549–559.
| Filamentous bacteriophage promote biofilm assembly and function.Crossref | GoogleScholarGoogle Scholar |
