Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa

LeRoux, Michele; Kirkpatrick, Robin L.; Montauti, Elena; Tran, Bao; Peterson, S. Brook; Harding, Brittany N.; Whitney, John C.; Russell, Alan D.; Traxler, Beth; Goo, Young Ah; Wiggins, Paul A.; Mougous, Joseph D.

doi:10.7554/elife.05701

Cited by 119 publications

(139 citation statements)

References 78 publications

(135 reference statements)

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“…The CF lung is highly enriched in DNA derived primarily from neutrophils, including the presence of NETs that trap and kill bacteria (47,49,57). It was recently shown that P. aeruginosa lysates induce the H1-T6SS of kin cells but that the signal is unknown (51). Therefore, we sought to decipher whether DNA isolated from human neutrophil cells or P. aeruginosa is capable of inducing P. aeruginosa H1-T6SS dynamics.…”

Section: Resultsmentioning

confidence: 99%

“…A recent report indicated that P. aeruginosa lysates, prepared by microbial interaction or sonication, can trigger a defensive response in the remaining P. aeruginosa kin population, termed the P. aeruginosa response to antagonism (PARA), but that the signaling molecule(s) involved remains unknown (51). However, it is important to delineate that eDNA exposure results in rapid (occurring on the order of seconds to minutes) firing of the H1-T6SS whereas PARA occurs over hours (51) independently of the TagQRST pathway.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, P. aeruginosa can sense some unknown signals released by killed P. aeruginosa cells during interspecies competition and can respond by increasing the expression of the H1-T6SS, the response termed P. aeruginosa response to antagonism (PARA) (51). Similarly, the H1-T6SS is transcriptionally induced when P. aeruginosa is cultivated in CF mucus (52) and secretion of Hcp is readily detectable in clinical CF sputum samples (27).…”

Section: Ystic Fibrosis (Cf) Is a Common Lethal Inherited Disease Inmentioning

confidence: 99%

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Chelation of Membrane-Bound Cations by Extracellular DNA Activates the Type VI Secretion System in Pseudomonas aeruginosa

et al. 2016

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e Pseudomonas aeruginosa employs its type VI secretion system (T6SS) as a highly effective and tightly regulated weapon to deliver toxic molecules to target cells. T6SS-secreted proteins of P. aeruginosa can be detected in the sputum of cystic fibrosis (CF) patients, who typically present a chronic and polymicrobial lung infection. However, the mechanism of T6SS activation in the CF lung is not fully understood. Here we demonstrate that extracellular DNA (eDNA), abundant within the CF airways, stimulates the dynamics of the H1-T6SS cluster apparatus in Pseudomonas aeruginosa PAO1. Addition of Mg 2؉ or DNase with eDNA abolished such activation, while treatment with EDTA mimicked the eDNA effect, suggesting that the eDNA-mediated effect is due to chelation of outer membrane-bound cations. DNA-activated H1-T6SS enables P. aeruginosa to nonselectively attack neighboring species regardless of whether or not it was provoked. Because of the importance of the T6SS in interspecies interactions and the prevalence of eDNA in the environments that P. aeruginosa inhabits, our report reveals an important adaptation strategy that likely contributes to the competitive fitness of P. aeruginosa in polymicrobial communities.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Ystic Fibrosis (Cf) Is a Common Lethal Inherited Disease Inmentioning

confidence: 99%

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Chelation of Membrane-Bound Cations by Extracellular DNA Activates the Type VI Secretion System in Pseudomonas aeruginosa

et al. 2016

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“…Strains of P. aeruginosa that are deficient in the production of all known T6SS effectors still retaliate against T6SS-mediated attacks and engage in dueling with effective killing activity (116). If P. aeruginosa cells lose their duels and are lysed by competitors, they release diffusible danger signals that stimulate T6SS activity and promote the survival of siblings (119).…”

Section: Contact-mediated Competitionmentioning

confidence: 99%

Multifaceted Interfaces of Bacterial Competition

2016

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bMicrobial communities span many orders of magnitude, ranging in scale from hundreds of cells on a single particle of soil to billions of cells within the lumen of the gastrointestinal tract. Bacterial cells in all habitats are members of densely populated local environments that facilitate competition between neighboring cells. Accordingly, bacteria require dynamic systems to respond to the competitive challenges and the fluctuations in environmental circumstances that tax their fitness. The assemblage of bacteria into communities provides an environment where competitive mechanisms are developed into new strategies for survival. In this minireview, we highlight a number of mechanisms used by bacteria to compete between species. We focus on recent discoveries that illustrate the dynamic and multifaceted functions used in bacterial competition and discuss how specific mechanisms provide a foundation for understanding bacterial community development and function.

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“…Not only can cells detect a Type VI attack from another, but they mount a counterattack by assembling their own poisoned spear at the site of the attack. In another surprising twist, once a cell is lysed by T6SS, the lysate can induce T6SS activity in addition to other antibacterial compounds in neighboring kin (17). This suggests that cells not only sense competition directly but also indirectly via damage done to neighboring cells.…”

mentioning

confidence: 99%