A genetic switch controls Pseudomonas aeruginosa surface colonization

Manner, Christina; Dias Teixeira, Raphael; Saha, Dibya; Kaczmarczyk, Andreas; Zemp, Raphaela; Wyss, Fabian; Jaeger, Tina; Laventie, Benoit-Joseph; Boyer, Sebastien; Malone, Jacob G.; Qvortrup, Katrine; Andersen, Jens Bo; Givskov, Michael; Tolker-Nielsen, Tim; Hiller, Sebastian; Drescher, Knut; Jenal, Urs

doi:10.1038/s41564-023-01403-0

Cited by 28 publications

(16 citation statements)

References 69 publications

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“…When P. aeruginosa encounters a surface, intracellular levels of c-di-GMP rapidly accumulate and promote gene expression signatures associated with tissue adherence, biofilm formation, and virulence [ 55 ]. Once surface attachment is achieved, asymmetric cell division leads to daughter cells with opposing functionality, resulting from their differing c-di-GMP levels.…”

Section: Discussionmentioning

confidence: 99%

“…The cell with high c-di-GMP is adherent, while the low c-di-GMP is flagellated and geared toward dispersal [ 56 ]. While this process is important in early colonization, c-di-GMP plays an equally critical role in established chronic infections, mediating surface exploration, the formation of microcolonies and eventually biofilms [ 55 ].…”

Section: Discussionmentioning

confidence: 99%

“…We observed the loss of function mutations in bifA under non-CF conditions and mutations in another phosphodiesterase, dipA , in populations evolved in CF sinus or LM. The genetic switch controlling P. aeruginosa surface colonization is mediated by inhibition of BifA, triggered through HecE activity under conditions of nutrient limitation or elevated temperature [ 55 ]. Loss of BifA function in airway-adapted P. aeruginosa might fix cells into a regulatory mode geared toward surface-attachment and a sessile lifestyle.…”

Section: Discussionmentioning

confidence: 99%

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Secondary messenger signalling influences Pseudomonas aeruginosa adaptation to sinus and lung environments

Ruhluel,

Fisher,

Barton

et al. 2024

The ISME Journal

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Pseudomonas aeruginosa is a cause of chronic respiratory tract infections in people with cystic fibrosis (CF), non-CF bronchiectasis and chronic obstructive pulmonary disease. Prolonged infection allows accumulation of mutations and horizontal gene transfer, increasing the likelihood of adaptive phenotypic traits. Adaptation is proposed to arise first in bacterial populations colonising upper airway environments. Here, we model this process using an experimental evolution approach. P. aeruginosa PAO1, which is not airway adapted, was serially passaged, separately, in media chemically reflective of upper or lower airway environments. To explore whether the CF environment selects for unique traits, we separately passaged PAO1 in airway-mimicking media with or without CF-specific factors. Our findings demonstrated that all airway environments – sinus and lungs, under CF and non-CF conditions – selected for loss of twitching motility, increased resistance to multiple antibiotic classes and a hyper-biofilm phenotype. These traits conferred increased airway colonisation potential in an in vivo model. CF-like conditions exerted stronger selective pressures, leading to emergence of more pronounced phenotypes. Loss of twitching was associated with mutations in type IV pili genes. Type IV pili mediate surface attachment, twitching and induction of cAMP signalling. We additionally identified multiple evolutionary routes to increased biofilm formation involving regulation of cyclic-di-GMP signalling. These included loss of function mutations in bifA and dipA phosphodiesterase genes and activating mutations in the siaA phosphatase. These data highlight that airway environments select for traits associated with sessile lifestyles and suggest upper airway niches support emergence of phenotypes that promote establishment of lung infection.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Secondary messenger signalling influences Pseudomonas aeruginosa adaptation to sinus and lung environments

Ruhluel,

Fisher,

Barton

et al. 2024

The ISME Journal

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“…Most bacteriophages infecting Pseudomonas aeruginosa target type IV pili or lipopolysaccharides as receptors to initiate infection, with the notable exception of phage OMKO1 which uses the outer membrane protein OprM as host receptor ( 1 – 3 ). A recent report suggested that phage Knedl, a small siphovirus infecting P. aeruginosa laboratory strain PAO1, exploits the extracellular polysaccharide Psl as receptor to initiate infection ( 4 , 5 ). We now expand on this finding by reporting the complete genome sequence of this phage.…”

Section: Announcementmentioning

confidence: 99%

Complete genome sequence of Pseudomonas aeruginosa phage Knedl

Maffei,

Manner,

Jenal

et al. 2024

Microbiol Resour Announc

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Bacteriophage Knedl is the first reported Pseudomonas aeruginosa phage that targets the Psl exopolysaccharide as receptor. Here, we report the genome of Knedl, demonstrating that it belongs to the genus Iggyvirus of the Queuovirinae subfamily. Future studies on the infection mechanism of Knedl could inform phage-based approaches to eradicate biofilms.

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“…Thereby, upon cell division, localized cyclic di‐GMP turnover proteins become unequally distributed to the daughter cell causing cell heterogeneity (Christen et al, 2010; Kulasekara et al, 2013). Remarkably, upon asymmetric surface sensing by, for example, a polar flagellum, the cyclic di‐GMP concentration can be modulated within seconds and cell polarity in cyclic di‐GMP synthesis reverted upon cell division to produce surface exploring spreader cells (Manner et al, 2023). With the transition between motility and sessility to be gradually conducted by surface appendages such as the flagellum and subsequently surface‐induced type IV pili with functionalities in both lifestyles (Conrad et al, 2011; Nakane et al, 2022; Zhao et al, 2013), observations on the single‐cell level indicated transient, but lasting cellular states that conduct both biosynthesis of extracellular matrix equally as surface motility that are promoted by low‐ and high‐cyclic di‐GMP, respectively.…”

Section: Heterogeneity and Differential Single‐cell Polarity Of Cycli...mentioning

confidence: 99%

Cyclic di‐GMP signaling—Where did you come from and where will you go?

Römling

2023

Molecular Microbiology

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Microbes including bacteria are required to respond to their often continuously changing ecological niches in order to survive. While many signaling molecules are produced as seemingly circumstantial byproducts of common biochemical reactions, there are a few second messenger signaling systems such as the ubiquitous cyclic di‐GMP second messenger system that arise through the synthesis of dedicated multidomain enzymes triggered by multiple diverse external and internal signals. Being one of the most numerous and widespread signaling system in bacteria, cyclic di‐GMP signaling contributes to adjust physiological and metabolic responses in all available ecological niches. Those niches range from deep‐sea and hydrothermal springs to the intracellular environment in human immune cells such as macrophages. This outmost adaptability is possible by the modularity of the cyclic di‐GMP turnover proteins which enables coupling of enzymatic activity to the diversity of sensory domains and the flexibility in cyclic di‐GMP binding sites. Nevertheless, commonly regulated fundamental microbial behavior include biofilm formation, motility, and acute and chronic virulence. The dedicated domains carrying out the enzymatic activity indicate an early evolutionary origin and diversification of “bona fide” second messengers such as cyclic di‐GMP which is estimated to have been present in the last universal common ancestor of archaea and bacteria and maintained in the bacterial kingdom until today. This perspective article addresses aspects of our current view on the cyclic di‐GMP signaling system and points to knowledge gaps that still await answers.

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A genetic switch controls Pseudomonas aeruginosa surface colonization

Cited by 28 publications

References 69 publications

Secondary messenger signalling influences Pseudomonas aeruginosa adaptation to sinus and lung environments

Secondary messenger signalling influences Pseudomonas aeruginosa adaptation to sinus and lung environments

Complete genome sequence of Pseudomonas aeruginosa phage Knedl

Cyclic di‐GMP signaling—Where did you come from and where will you go?

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