Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa

Biofilm development in Pseudomonas aeruginosa is in part dependent on a filamentous phage, Pf4, which contributes to biofilm maturation, cell death, dispersal and variant formation, e.g., small colony variants (SCVs). These biofilm phenotypes correlate with the conversion of the Pf4 phage into a sup...

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Main Authors: Hui, Janice G. K., Mai-Prochnow, Anne, Kjelleberg, Staffan, McDougald, Diane, Rice, Scott A.
Other Authors: School of Biological Sciences
Format: Article
Language:English
Published: 2015
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Online Access:https://hdl.handle.net/10356/104637
http://hdl.handle.net/10220/24678
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spelling sg-ntu-dr.10356-1046372022-02-16T16:27:30Z Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa Hui, Janice G. K. Mai-Prochnow, Anne Kjelleberg, Staffan McDougald, Diane Rice, Scott A. School of Biological Sciences Singapore Centre for Environmental Life Sciences Engineering DRNTU::Science::Biological sciences::Microbiology Biofilm development in Pseudomonas aeruginosa is in part dependent on a filamentous phage, Pf4, which contributes to biofilm maturation, cell death, dispersal and variant formation, e.g., small colony variants (SCVs). These biofilm phenotypes correlate with the conversion of the Pf4 phage into a superinfection (SI) variant that reinfects and kills the prophage carrying host, in contrast to other filamentous phage that normally replicate without killing their host. Here we have investigated the physiological cues and genes that may be responsible for this conversion. Flow through biofilms typically developed SI phage approximately days 4 or 5 of development and corresponded with dispersal. Starvation for carbon or nitrogen did not lead to the development of SI phage. In contrast, exposure of the biofilm to nitric oxide, H2O2 or the DNA damaging agent, mitomycin C, showed a trend of increased numbers of SI phage, suggesting that reactive oxygen or nitrogen species (RONS) played a role in the formation of SI phage. In support of this, mutation of oxyR, the major oxidative stress regulator in P. aeruginosa, resulted in higher level of and earlier superinfection compared to the wild-type (WT). Similarly, inactivation of mutS, a DNA mismatch repair gene, resulted in the early appearance of the SI phage and this was four log higher than the WT. In contrast, loss of recA, which is important for DNA repair and the SOS response, also resulted in a delayed and decreased production of SI phage. Treatments or mutations that increased superinfection also correlated with an increase in the production of morphotypic variants. The results suggest that the accumulation of RONS by the biofilm may result in DNA lesions in the Pf4 phage, leading to the formation of SI phage, which subsequently selects for morphotypic variants, such as SCVs. Published version 2015-01-20T03:28:04Z 2019-12-06T21:36:42Z 2015-01-20T03:28:04Z 2019-12-06T21:36:42Z 2014 2014 Journal Article Hui, J. G. K., Mai-Prochnow, A., Kjelleberg, S., McDougald, D., & Rice, S. A. (2014). Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa. Frontiers in microbiology, 5. 654-. 1664-302X https://hdl.handle.net/10356/104637 http://hdl.handle.net/10220/24678 10.3389/fmicb.2014.00654 25520708 en Frontiers in microbiology © 2014 Hui, Mai-Prochnow, Kjelleberg, McDougald and Rice. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. 8 p. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic DRNTU::Science::Biological sciences::Microbiology
spellingShingle DRNTU::Science::Biological sciences::Microbiology
Hui, Janice G. K.
Mai-Prochnow, Anne
Kjelleberg, Staffan
McDougald, Diane
Rice, Scott A.
Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa
description Biofilm development in Pseudomonas aeruginosa is in part dependent on a filamentous phage, Pf4, which contributes to biofilm maturation, cell death, dispersal and variant formation, e.g., small colony variants (SCVs). These biofilm phenotypes correlate with the conversion of the Pf4 phage into a superinfection (SI) variant that reinfects and kills the prophage carrying host, in contrast to other filamentous phage that normally replicate without killing their host. Here we have investigated the physiological cues and genes that may be responsible for this conversion. Flow through biofilms typically developed SI phage approximately days 4 or 5 of development and corresponded with dispersal. Starvation for carbon or nitrogen did not lead to the development of SI phage. In contrast, exposure of the biofilm to nitric oxide, H2O2 or the DNA damaging agent, mitomycin C, showed a trend of increased numbers of SI phage, suggesting that reactive oxygen or nitrogen species (RONS) played a role in the formation of SI phage. In support of this, mutation of oxyR, the major oxidative stress regulator in P. aeruginosa, resulted in higher level of and earlier superinfection compared to the wild-type (WT). Similarly, inactivation of mutS, a DNA mismatch repair gene, resulted in the early appearance of the SI phage and this was four log higher than the WT. In contrast, loss of recA, which is important for DNA repair and the SOS response, also resulted in a delayed and decreased production of SI phage. Treatments or mutations that increased superinfection also correlated with an increase in the production of morphotypic variants. The results suggest that the accumulation of RONS by the biofilm may result in DNA lesions in the Pf4 phage, leading to the formation of SI phage, which subsequently selects for morphotypic variants, such as SCVs.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Hui, Janice G. K.
Mai-Prochnow, Anne
Kjelleberg, Staffan
McDougald, Diane
Rice, Scott A.
format Article
author Hui, Janice G. K.
Mai-Prochnow, Anne
Kjelleberg, Staffan
McDougald, Diane
Rice, Scott A.
author_sort Hui, Janice G. K.
title Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa
title_short Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa
title_full Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa
title_fullStr Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa
title_full_unstemmed Environmental cues and genes involved in establishment of the superinfective Pf4 phage of pseudomonas aeruginosa
title_sort environmental cues and genes involved in establishment of the superinfective pf4 phage of pseudomonas aeruginosa
publishDate 2015
url https://hdl.handle.net/10356/104637
http://hdl.handle.net/10220/24678
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