Anaerobiosis influences virulence properties of Pseudomonas aeruginosa cystic fibrosis isolates and the interaction with Staphylococcus aureus

Pallett, Ross; Leslie, Laura J.; Lambert, Peter A.; Milic, Ivana; Devitt, Andrew; Marshall, Lindsay J.

doi:10.1038/s41598-019-42952-x

Cited by 45 publications

(44 citation statements)

References 99 publications

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“…Also, longitudinal clinical studies would be appropriate to analyze the kinetics of interaction evolution over time and determine how it could affect patients’ health. Furthermore, the conditions and environmental factors leading to co-existence instead of competition require clarification, particularly through studies such one conducted recently that demonstrated the positive impact of hypoxia found in static mucus within CF airways on a coexisting interaction 32 .…”

Section: Discussionmentioning

confidence: 99%

“…Since this state of coexistence is apparently solely attributable to P. aeruginosa , the selective advantage for P. aeruginosa leads to questions. Indeed, previous studies showed that cocultivation with S. aureus induces LPS mutation in P. aeruginosa associated with fitness gain and antibiotic resistance 41 , and that S. aureus exoproducts restore and enhance P. aeruginosa motility 32 . The state of coexistence could thus represent a trade-off allowing both pathogens to benefit mutually and maintain equilibrium.…”

Section: Discussionmentioning

confidence: 99%

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Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells

Briaud

Camus

Bastien

et al. 2019

Sci Rep

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Cystic fibrosis (CF) is the most common life-threatening genetic disease among Caucasians. CF patients suffer from chronic lung infections due to the presence of thick mucus, caused by cftr gene dysfunction. The two most commonly found bacteria in the mucus of CF patients are Staphylococcus aureus and Pseudomonas aeruginosa. It is well known that early-infecting P. aeruginosa strains produce anti-staphylococcal compounds and inhibit S. aureus growth. More recently, it has been shown that late-infecting P. aeruginosa strains develop commensal-like/coexistence interaction with S. aureus. The aim of this study was to decipher the impact of P. aeruginosa strains on S. aureus. RNA sequencing analysis showed 77 genes were specifically dysregulated in the context of competition and 140 genes in the context of coexistence in the presence of P. aeruginosa. In coexistence, genes encoding virulence factors and proteins involved in carbohydrates, lipids, nucleotides and amino acids metabolism were downregulated. On the contrary, several transporter family encoding genes were upregulated. In particular, several antibiotic pumps belonging to the Nor family were upregulated: tet38, norA and norC, leading to an increase in antibiotic resistance of S. aureus when exposed to tetracycline and ciprofloxacin and an enhanced internalization rate within epithelial pulmonary cells. This study shows that coexistence with P. aeruginosa affects the S. aureus transcriptome and virulence.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells

Briaud

Camus

Bastien

et al. 2019

Sci Rep

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Section: Discussionmentioning

confidence: 99%

Coexistence withPseudomonas aeruginosaaltersStaphylococcus aureustranscriptome, antibiotic resistance and internalization into epithelial cells

Briaud

Camus

Bastien

et al. 2019

Preprint

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15Cystic fibrosis (CF) is the most common life-threatening genetic disease among Caucasians. CF 16 patients suffer from chronic lung infections due to the presence of thick mucus, caused by cftr 17 gene dysfunction. The two most commonly found bacteria in the mucus of CF patients are 18Staphylococcus aureus and Pseudomonas aeruginosa. It is well known that early-infecting P. 19 aeruginosa strains produce anti-staphylococcal compounds and inhibit S. aureus growth. More 20 recently, it has been shown that late-infecting P. aeruginosa strains develop commensal-21 like/coexistence interaction with S. aureus. The aim of this study was to decipher the impact of P. 22While P. aeruginosa is recognized as the leading cause of lung function decline, the significance 49 of S. aureus in the course of CF disease is still being debated. It has been shown that one of the 50 risk factors for initial P. aeruginosa airway infection includes S. aureus pre-colonization [8][9][10] . 51However, the impact of coinfection by the two pathogens on the evolution of the disease remains 52 unclear 11-13 . 53 S. aureus and P. aeruginosa have been identified in the same lobe of CF lungs 14,15 , suggesting 54 that both pathogens are present in the same niche and can in fact interact in vivo. Interactions 55 4 have been widely studied and it is commonly admitted that P. aeruginosa outcompetes S. aureus. 56 Different mechanisms have been described 16 : for example, P. aeruginosa secreted products can 57 inhibit the growth or lyse S. aureus as well as induce epithelial cells to kill S. aureus and other 58Gram-positive bacteria 8,17,18 . 59 However, these interactions can evolve during chronic colonization. Indeed, P. aeruginosa strains 60 isolated from early infection outcompete S. aureus, as previously described, while strains isolated 61 from chronic infection are less aggressive and can be co-cultivated with S. aureus 19,20 . 62 Furthermore, P. aeruginosa isolates from mono-infected patients are more competitive towards S. 63 aureus than isolates from coinfected patients 21 . 64 In contrast to antagonistic interactions, nothing is known about the effects of P. aeruginosa and 65 S. aureus interactions in this context of coexisting bacteria within the same infectious niche. 66Using a transcriptomic approach, we analyzed how co-cultivation with non-competitive P. 67 aeruginosa altered S. aureus gene expression, especially genes encoding Nor family efflux 68 pumps. In the presence of P. aeruginosa, over-expression of these genes increased S. aureus 69 antibiotic tolerance and the rate of internalization into epithelial cells, two key determinants of 70 chronic infection. 71 72 5 RESULTS 73Coexistence interaction involves more than half of the S. aureus and P. aeruginosa isolates 74 from co-infected CF patients. 75Two types of interactions between S. aureus and P. aeruginosa could be observed with CF 76 patient isolates: the well-described competitive phenotype, where P. aeruginosa inhibits S. 77 aureus growth, 16 and the newly describe...

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“…In CF patients, during the adolescence and early adulthood, P. aeruginosa replaces S. aureus but sometimes this latter is still detected in CF adults. Pallet et al studied the co-infection of CF airways by S. aureus and P. aeruginosa under normoxia and anoxia [113]. Amongst three CF isolates, one presented no anti-staphylococcal activity.…”

Section: Proteomics For Host-pathogen Studiesmentioning

confidence: 99%

Exoproteomics for Better Understanding Pseudomonas aeruginosa Virulence

Sauvage

Hardouin

2020

Toxins

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Pseudomonas aeruginosa is the most common human opportunistic pathogen associated with nosocomial diseases. In 2017, the World Health Organization has classified P. aeruginosa as a critical agent threatening human health, and for which the development of new treatments is urgently necessary. One interesting avenue is to target virulence factors to understand P. aeruginosa pathogenicity. Thus, characterising exoproteins of P. aeruginosa is a hot research topic and proteomics is a powerful approach that provides important information to gain insights on bacterial virulence. The aim of this review is to focus on the contribution of proteomics to the studies of P. aeruginosa exoproteins, highlighting its relevance in the discovery of virulence factors, post-translational modifications on exoproteins and host-pathogen relationships.

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Anaerobiosis influences virulence properties of Pseudomonas aeruginosa cystic fibrosis isolates and the interaction with Staphylococcus aureus

Cited by 45 publications

References 99 publications

Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells

Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells

Coexistence withPseudomonas aeruginosaaltersStaphylococcus aureustranscriptome, antibiotic resistance and internalization into epithelial cells

Exoproteomics for Better Understanding Pseudomonas aeruginosa Virulence

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