PrrT/A, a Pseudomonas aeruginosa Bacterial Encoded Toxin-Antitoxin System Involved in Prophage Regulation and Biofilm Formation

Shmidov, Esther; Lebenthal-Loinger, Ilana; Roth, Shira; Karako-Lampert, Sarit; Zander, Itzhak; Shoshani, Sivan; Danielli, Amos; Banin, Ehud

doi:10.1128/spectrum.01182-22

Cited by 7 publications

(9 citation statements)

References 60 publications

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“…In Escherichia coli , several TAS are involved in regulation of biofilm formation at different stages ( Kim et al, 2009 ; Kolodkin-Gal et al, 2009 ; Yamaguchi and Inouye, 2011 ; Soo and Wood, 2013 ; Zhao et al, 2013 ). Other TAS have been reported to regulate biofilms in different species, such as in Vibrio cholerae ( Wang et al, 2015 ), Staphylococcus aureus ( Kato et al, 2017 ), or Pseudomonas aeruginosa ( Wood and Wood, 2016 ; Shmidov et al, 2022 ; Song et al, 2022 ). O 2 limitation is one of the major environmental stresses experienced by bacteria in a mature biofilm ( Stewart and Franklin, 2008 ; Kostakioti et al, 2013 ) and some species, such as Shewanella oneidensis or P. aeruginosa , respond to O 2 depletion by triggering single cell dispersion ( Thormann et al, 2005 ; Barraud et al, 2009 ; Rumbaugh and Sauer, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin–antitoxin system

Berne

Zappa

Brun

2023

eLife

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In their natural environment, most bacteria preferentially live as complex surface-attached multicellular colonies called biofilms. Biofilms begin with a few cells adhering to a surface, where they multiply to form a mature colony. When conditions deteriorate, cells can leave the biofilm. This dispersion is thought to be an important process that modifies the overall biofilm architecture and that promotes colonization of new environments. In Caulobacter crescentus biofilms, extracellular DNA (eDNA) is released upon cell death and prevents newborn cells from joining the established biofilm. Thus, eDNA promotes the dispersal of newborn cells and the subsequent colonization of new environments. These observations suggest that eDNA is a cue for sensing detrimental environmental conditions in the biofilm. Here we show that the toxin-antitoxin system (TAS) ParDE4 stimulates cell death in areas of a biofilm with decreased O2 availability. In conditions where O2 availability is low, eDNA concentration is correlated with cell death. Cell dispersal away from biofilms is decreased when parDE4 is deleted, probably due to the lower local eDNA concentration. Expression of parDE4 is positively regulated by O2 and the expression of this operon is decreased in biofilms where O2 availability is low. Thus, a programmed cell death mechanism using an O2-regulated TAS stimulates dispersal away from areas of a biofilm with decreased O2 availability and favors colonization of a new, more hospitable environment.

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Section: Discussionmentioning

confidence: 99%

eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin–antitoxin system

Berne

Zappa

Brun

2023

eLife

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show abstract

“…In Escherichia coli , several TAS are involved in regulation of biofilm formation at different stages (Kim et al ., 2009, Kolodkin-Gal et al ., 2009, Yamaguchi & Inouye, 2011, Soo & Wood, 2013, Zhao et al ., 2013). Other TAS have been reported to regulate biofilms in different species, such as in Vibrio cholerae (Wang et al ., 2015), Staphylococcus aureus (Kato et al ., 2017), or Pseudomonas aeruginosa (Wood & Wood, 2016, Shmidov et al ., 2022).…”

Section: Discussionmentioning

confidence: 99%

eDNA-stimulated cell dispersion fromCaulobacter crescentusbiofilms upon oxygen limitation is dependent on a toxin-antitoxin system

Berne

Zappa

Brun

2022

Preprint

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In their natural environment, most bacteria preferentially live as complex surface-attached multicellular colonies called biofilms. Biofilms begin with a few cells adhering to a surface, where they multiply to form a mature colony. When conditions deteriorate, cells can leave the biofilm. This dispersion is thought to be an important process that modifies the overall biofilm architecture and that promotes colonization of new environments. In Caulobacter crescentus biofilms, extracellular DNA (eDNA) is released upon cell death and prevents newborn cells from joining the established biofilm. Thus, eDNA promotes the dispersal of newborn cells and the subsequent colonization of new environments. These observations suggest that eDNA is a cue for sensing detrimental environmental conditions in the biofilm. Here we show that the toxin-antitoxin ParDE4 stimulates cell death in areas of a biofilm with decreased O2 availability. In conditions where O2 availability is low, eDNA concentration is correlated with cell death. Cell dispersal away from biofilms is decreased when parDE4 is deleted, probably due to the lower local eDNA concentration. Expression of parDE4 is positively regulated by O2 and the expression of this operon is decreased in biofilms where O2 availability is low. Thus, PCD by an O2-regulated toxin-antitoxin system stimulates dispersal away from areas of a biofilm with decreased O2 availability and favors colonization of a new, more hospitable environment.

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“…Ten pairs of type II TA systems have been experimentally verified in P. aeruginosa ( Table 1 ), as follows: HigB/HigA [ 19 ], ParD/ParE [ 20 ], HicA/HicB [ 21 ], RelB/RelE [ 22 ], ResA/XreA [ 23 ], PrrT/PrrA [ 24 ], CrlT/CrlA [ 25 ], PacT/PacA [ 26 ], PumA/PumB [ 27 ], and PfiT/PfiA [ 28 ]. In type II TA systems, genes encoding the toxin and antitoxin are within a single operon ( Figure 1 ).…”

Section: Transcriptional Regulation Of Type II Ta Systems In ...mentioning

confidence: 99%

“…In P. aeruginosa , most type II TA systems are encoded on the chromosome [ 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 ], the exceptions being PfiT/PfiA and PumA/PumB (phage and plasmid, respectively) [ 27 , 28 ]. These TA systems have diverse biological functions, such as virulence and biofilm formation [ 34 , 35 , 36 ], protection host against antibiotics [ 20 ], persistence [ 23 ], plasmid maintenance [ 27 ], and prophage production [ 25 , 37 ] ( Figure 2 ).…”

Section: Biological Functions Of Type II Ta Systems In P Ae...mentioning

confidence: 99%

“…Dai et al found 16,963 TA gene hits in 5432 genomic sequences of P. aeruginosa from the NCBI Genome database, most of which were in chromosome sequences (94%) and belonged to type II TA systems (16,808 hits) [ 18 ]. To date, at least 10 pairs of type II TA systems have been experimentally characterised in P. aeruginosa , 8 of which are located on the chromosome [ 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 ], whereas PumA/PumB and PfiT/PfiA were identified in plasmid pUM505 and prophage Pf4, respectively [ 27 , 28 ]. These TA systems have multiple biological functions and regulatory mechanisms, which makes TA research more interesting and attractive.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Type II Toxin–Antitoxin Systems in Pseudomonas aeruginosa

Guo

Song

et al. 2023

Toxins

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Toxin–antitoxin (TA) systems are typically composed of a stable toxin and a labile antitoxin; the latter counteracts the toxicity of the former under suitable conditions. TA systems are classified into eight types based on the nature and molecular modes of action of the antitoxin component so far. The 10 pairs of TA systems discovered and experimentally characterised in Pseudomonas aeruginosa are type II TA systems. Type II TA systems have various physiological functions, such as virulence and biofilm formation, protection host against antibiotics, persistence, plasmid maintenance, and prophage production. Here, we review the type II TA systems of P. aeruginosa, focusing on their biological functions and regulatory mechanisms, providing potential applications for the novel drug design.

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PrrT/A, a Pseudomonas aeruginosa Bacterial Encoded Toxin-Antitoxin System Involved in Prophage Regulation and Biofilm Formation

Abstract: The functions attributed to bacterial TA systems are controversial and remain largely unknown. Our study suggests new insights into the potential functions of bacterial TA systems.

Cited by 7 publications

References 60 publications

eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin–antitoxin system

eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin–antitoxin system

eDNA-stimulated cell dispersion fromCaulobacter crescentusbiofilms upon oxygen limitation is dependent on a toxin-antitoxin system

Type II Toxin–Antitoxin Systems in Pseudomonas aeruginosa

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