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Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria

Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria
Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria
The marine bacterium Pseudoalteromonas tunicata produces an antibacterial and autolytic protein, AlpP, which causes death of a subpopulation of cells during biofilm formation and mediates differentiation, dispersal, and phenotypic variation among dispersal cells. The AlpP homologue (LodA) in the marine bacterium Marinomonas mediterranea was recently identified as a lysine oxidase which mediates cell death through the production of hydrogen peroxide. Here we show that AlpP in P. tunicata also acts as a lysine oxidase and that the hydrogen peroxide generated is responsible for cell death within microcolonies during biofilm development in both M. mediterranea and P. tunicata. LodA-mediated biofilm cell death is shown to be linked to the generation of phenotypic variation in growth and biofilm formation among M. mediterranea biofilm dispersal cells. Moreover, AlpP homologues also occur in several other gram-negative bacteria from diverse environments. Our results show that subpopulations of cells in microcolonies also die during biofilm formation in two of these organisms, Chromobacterium violaceum and Caulobacter crescentus. In all organisms, hydrogen peroxide was implicated in biofilm cell death, because it could be detected at the same time as the killing occurred, and the addition of catalase significantly reduced biofilm killing. In C. violaceum the AlpP-homologue was clearly linked to biofilm cell death events since an isogenic mutant (CVMUR1) does not undergo biofilm cell death. We propose that biofilm killing through hydrogen peroxide can be linked to AlpP homologue activity and plays an important role in dispersal and colonization across a range of gram-negative bacteria.
0021-9193
5493-5501
Mai-Prochnow, Anne
11d9ad32-68fb-4569-a471-8273b5063460
Lucas-Elio, Patricia
60ff6a68-cdb5-49fe-9870-80b1095d7d21
Egan, Suhelen
ed013d4f-f8c5-40b2-b3e1-caec2a6fb1fc
Thomas, Torsten
ec8f4082-7210-4d99-a17a-acaa7b66768a
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Sanchez-Amat, Antonio
1318d250-2434-4b53-8724-79c4f74ca8b8
Kjelleberg, Staffan
043b66b5-130c-42f2-99b3-ec3eecf3248e
Mai-Prochnow, Anne
11d9ad32-68fb-4569-a471-8273b5063460
Lucas-Elio, Patricia
60ff6a68-cdb5-49fe-9870-80b1095d7d21
Egan, Suhelen
ed013d4f-f8c5-40b2-b3e1-caec2a6fb1fc
Thomas, Torsten
ec8f4082-7210-4d99-a17a-acaa7b66768a
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Sanchez-Amat, Antonio
1318d250-2434-4b53-8724-79c4f74ca8b8
Kjelleberg, Staffan
043b66b5-130c-42f2-99b3-ec3eecf3248e

Mai-Prochnow, Anne, Lucas-Elio, Patricia, Egan, Suhelen, Thomas, Torsten, Webb, Jeremy S., Sanchez-Amat, Antonio and Kjelleberg, Staffan (2008) Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria. Journal of Bacteriology, 190 (15), 5493-5501. (doi:10.1128/JB.00549-08). (PMID:18502869)

Record type: Article

Abstract

The marine bacterium Pseudoalteromonas tunicata produces an antibacterial and autolytic protein, AlpP, which causes death of a subpopulation of cells during biofilm formation and mediates differentiation, dispersal, and phenotypic variation among dispersal cells. The AlpP homologue (LodA) in the marine bacterium Marinomonas mediterranea was recently identified as a lysine oxidase which mediates cell death through the production of hydrogen peroxide. Here we show that AlpP in P. tunicata also acts as a lysine oxidase and that the hydrogen peroxide generated is responsible for cell death within microcolonies during biofilm development in both M. mediterranea and P. tunicata. LodA-mediated biofilm cell death is shown to be linked to the generation of phenotypic variation in growth and biofilm formation among M. mediterranea biofilm dispersal cells. Moreover, AlpP homologues also occur in several other gram-negative bacteria from diverse environments. Our results show that subpopulations of cells in microcolonies also die during biofilm formation in two of these organisms, Chromobacterium violaceum and Caulobacter crescentus. In all organisms, hydrogen peroxide was implicated in biofilm cell death, because it could be detected at the same time as the killing occurred, and the addition of catalase significantly reduced biofilm killing. In C. violaceum the AlpP-homologue was clearly linked to biofilm cell death events since an isogenic mutant (CVMUR1) does not undergo biofilm cell death. We propose that biofilm killing through hydrogen peroxide can be linked to AlpP homologue activity and plays an important role in dispersal and colonization across a range of gram-negative bacteria.

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Published date: August 2008

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Local EPrints ID: 186805
URI: http://eprints.soton.ac.uk/id/eprint/186805
ISSN: 0021-9193
PURE UUID: 94085978-8326-4fc4-a0ad-032f10d79975
ORCID for Jeremy S. Webb: ORCID iD orcid.org/0000-0003-2068-8589

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Date deposited: 16 May 2011 09:56
Last modified: 15 Mar 2024 03:26

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Contributors

Author: Anne Mai-Prochnow
Author: Patricia Lucas-Elio
Author: Suhelen Egan
Author: Torsten Thomas
Author: Jeremy S. Webb ORCID iD
Author: Antonio Sanchez-Amat
Author: Staffan Kjelleberg

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