The biofilm life cycle and virulence of <i>Pseudomonas aeruginosa</i> are dependent on a filamentous prophage

Rice, Scott A.; Tan, Chuan Hao; Mikkelsen, Per Jensen; Kung, Vanderlene L.; Woo, Jerry K. K.; Tay, Martin; Hauser, Alan R.; McDougald, Diane; Webb, Jeremy S.; Kjelleberg, Staffan

doi:10.1038/ismej.2008.109

Cited by 316 publications

(410 citation statements)

References 47 publications

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“…Other studies have recently demonstrated a high level of bacteriophage release in biofilms (Resch et al, 2005;Rice et al, 2009). The resulting lysis of cells may provide nutrients and allow the persistence of neighbouring cells.…”

Section: Discussionmentioning

confidence: 99%

Treponema denticola biofilm-induced expression of a bacteriophage, toxin–antitoxin systems and transposases

et al. 2010

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Treponema denticola is an oral spirochaete that has been strongly associated with chronic periodontitis. The bacterium exists as part of a dense biofilm (subgingival dental plaque) accreted to the tooth. To determine T. denticola gene products important for persistence as a biofilm we developed a continuous-culture biofilm model and conducted a genome-wide transcriptomic analysis of biofilm and planktonic cells. A total of 126 genes were differentially expressed with a fold change of 1.5 or greater. This analysis identified the upregulation of putative prophage genes in the T. denticola 35405 genome. Intact bacteriophage particles were isolated from T. denticola and circular phage DNA was detected by PCR analysis. This represents the first, to our knowledge, functional bacteriophage isolated from T. denticola, which we have designated Qtd1. In biofilm cells there was also an upregulation of genes encoding several virulence factors, toxinantitoxin systems and a family of putative transposases. Together, these data indicate that there is a higher potential for genetic mobility in T. denticola when growing as a biofilm and that these systems are important for the biofilm persistence and therefore virulence of this bacterium.

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Section: Discussionmentioning

confidence: 99%

Treponema denticola biofilm-induced expression of a bacteriophage, toxin–antitoxin systems and transposases

et al. 2010

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“…Bacteriophages are highly abundant in all environments and are thought to outnumber prokaryotes in nature by a factor of 10 (Rohwer and Edwards, 2002;Rice et al, 2009). As opposed to phages that predominantly lyse cells, temperent phages can integrate as prophage into host cell genomes in a way that may benefit both host and prophage (Weinbauer, 2004;Chen et al, 2005).…”

Section: Mutants Lacking the Prophages Are Defective In Biofilm Formamentioning

confidence: 99%

“…The beststudied example in this regard is the role of the filamentous phage Pf4 in P. aeruginosa biofilm formation. Mutants lacking the phage form smaller colonies during the first days of biofilm formation and a potential role of phage-mediated cell lysis in eDNA release has been discussed but has not directly been demonstrated (Allesen-Holm et al, 2006;Rice et al, 2009). At later stages of biofilm development, Pf4 is thought to convert into a superinfective lytic form that causes cell death and hollowing of the structures, and, by that, significantly contributes to seeding dispersal of the community (Webb et al, 2003;Rice et al, 2009).…”

Section: Mutants Lacking the Prophages Are Defective In Biofilm Formamentioning

confidence: 99%

“…Mutants lacking the phage form smaller colonies during the first days of biofilm formation and a potential role of phage-mediated cell lysis in eDNA release has been discussed but has not directly been demonstrated (Allesen-Holm et al, 2006;Rice et al, 2009). At later stages of biofilm development, Pf4 is thought to convert into a superinfective lytic form that causes cell death and hollowing of the structures, and, by that, significantly contributes to seeding dispersal of the community (Webb et al, 2003;Rice et al, 2009). In addition, Pf4 has been linked to phenotypic variations in the dispersed cells, leading to small-colony variants that are characterized by accelerated biofilm formation (Webb et al, 2004;Rice et al, 2009).…”

Section: Mutants Lacking the Prophages Are Defective In Biofilm Formamentioning

confidence: 99%

“…At later stages of biofilm development, Pf4 is thought to convert into a superinfective lytic form that causes cell death and hollowing of the structures, and, by that, significantly contributes to seeding dispersal of the community (Webb et al, 2003;Rice et al, 2009). In addition, Pf4 has been linked to phenotypic variations in the dispersed cells, leading to small-colony variants that are characterized by accelerated biofilm formation (Webb et al, 2004;Rice et al, 2009). In contrast to MuSo2 and LambdaSo, MuSo1 does not form functional phage particles under the conditions tested.…”

Section: Mutants Lacking the Prophages Are Defective In Biofilm Formamentioning

confidence: 99%

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Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1

et al. 2010

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Shewanella oneidensis MR-1 is capable of forming highly structured surface-attached communities. By DNase I treatment, we demonstrated that extracellular DNA (eDNA) serves as a structural component in all stages of biofilm formation under static and hydrodynamic conditions. We determined whether eDNA is released through cell lysis mediated by the three prophages LambdaSo, MuSo1 and MuSo2 that are harbored in the genome of S. oneidensis MR-1. Mutant analyses and infection studies revealed that all three prophages may individually lead to cell lysis. However, only LambdaSo and MuSo2 form infectious phage particles. Phage release and cell lysis already occur during early stages of static incubation. A mutant devoid of the prophages was significantly less prone to lysis in pure culture. In addition, the phage-less mutant was severely impaired in biofilm formation through all stages of development, and three-dimensional growth occurred independently of eDNA as a structural component. Thus, we suggest that in S. oneidensis MR-1 prophage-mediated lysis results in the release of crucial biofilm-promoting factors, in particular eDNA.

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Filamentous Bacteriophages: Biology and Applications

Rakonjac¹

2012

Encyclopedia of Life Sciences

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Filamentous bacteriophages contain a circular single‐stranded deoxyribonucleic acid (ssDNA) genome packaged into long filaments. These phages do not reproduce by lysing bacteria; instead, they are secreted into the environment without killing the host. Well‐studied Escherichia coli K12‐infecting Ff phages (f1, fd or M13) always replicate episomally; however a growing number of ‘lysogenic’ or chromosomally integrated filamentous phages of Gram‐negative bacteria are being discovered. The ‘lysogens’ can be induced; however phage reproduction does not require genome excision from bacterial chromosome and does not lyse the host cells. Some filamentous phages enhance the virulence of their host organisms, the most striking example being the CTXφ of Vibrio cholerae , which encodes cholera toxin. E. coli Ff phages are the workhorse of phage display technology, whose most notable ‘products’ are therapeutic recombinant antibodies. Ff are also being used in nanotechnology as templates for assembly of nanostructures, which has already led to their incorporation into a working nanobattery. Key Concepts: Filamentous bacteriophages are long filaments (6–7 nm×>500 nm) that contain a single‐stranded circular DNA genome. Filamentous bacteriophages replicate via a rolling circle mechanism, one strand at a time. Filamentous bacteriophages do not lyse the cells; they are released by secretion, using a dedicated filamentous phage assembly secretion system. Filamentous phage secretion‐assembly requires the proton‐motive force and ATP. Some filamentous phages replicate exclusively as episomes, while others also integrate their genomes into the host chromosome, forming a lysogen. Induction of the lysogen does not result in cell lysis. Ff filamentous phages of E. coli (f1, M13 and fd) have been used interchangeably as vectors and helper phages in DNA sequencing, as a protein display platform in phage display technology and as a template for assembly of nanostructures in nanotechnology.

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The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage

Cited by 316 publications

References 47 publications

Treponema denticola biofilm-induced expression of a bacteriophage, toxin–antitoxin systems and transposases

Treponema denticola biofilm-induced expression of a bacteriophage, toxin–antitoxin systems and transposases

Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1

Filamentous Bacteriophages: Biology and Applications

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