Differential Potentiation of the Virulence of the Pseudomonas aeruginosa Cystic Fibrosis Liverpool Epidemic Strain by Oral Commensal Streptococci

Whiley, Robert A.; Sheikh, Nargis P.; Mushtaq, Naseem; Hagi‐Pavli, Eleni; Personne, Yoann; Javaid, Danish; Waite, Richard

doi:10.1093/infdis/jit568

Cited by 43 publications

(53 citation statements)

References 48 publications

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“…A strong correlation between pyocyanin production and virulence was confirmed for the entire panel (PCA and Spearman rank correlation coefficient R50.36, Pv0.02). In contrast to earlier studies (Hendrickson et al, 2001;Sonnleitner et al, 2003), these data indicate that pyocyanin may contribute to virulence in the G. mellonella, as shown recently (Whiley et al, 2014).…”

Section: Discussioncontrasting

confidence: 99%

Phenotypic characterization of an international Pseudomonas aeruginosa reference panel: strains of cystic fibrosis (CF) origin show less in vivo virulence than non-CF strains

et al. 2015

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Pseudomonas aeruginosa causes chronic lung infections in people with cystic fibrosis (CF) and acute opportunistic infections in people without CF. Forty-two P. aeruginosa strains from a range of clinical and environmental sources were collated into a single reference strain panel to harmonise research on this diverse opportunistic pathogen. To facilitate further harmonized and comparable research on P. aeruginosa, we characterized the panel strains for growth rates, motility, virulence in the Galleria mellonella infection model, pyocyanin and alginate production, mucoid phenotype, LPS pattern, biofilm formation, urease activity, and antimicrobial and phage susceptibilities. Phenotypic diversity across the P. aeruginosa panel was apparent for all phenotypes examined, agreeing with the marked variability seen in this species. However, except for growth rate, the phenotypic diversity among strains from CF versus non-CF sources was comparable. CF strains were less virulent in the G. mellonella model than non-CF strains (P50.037). Transmissible CF strains generally lacked O-antigen, produced less pyocyanin and had low virulence in G. mellonella. Furthermore, in the three sets of sequential CF strains,

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Section: Discussioncontrasting

confidence: 99%

Phenotypic characterization of an international Pseudomonas aeruginosa reference panel: strains of cystic fibrosis (CF) origin show less in vivo virulence than non-CF strains

et al. 2015

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“…However, it is important to note that polymicrobial interactions involving P. aeruginosa and oral streptococci in the CF lung are complex, and are often controlled by the dynamics of specific streptococcal populations, colonization sequence and environmental conditions. For example, streptococcal species that belong to the Streptococcus milleri and Streptococcus anginosus groups have also been found to be co-colonized with P. aeruginosa in the CF airway and upregulate P. aeruginosa virulence, and as a result are considered pathogens in some cases of CF (Parkins et al, 2008;Sibley et al, 2008;Whiley et al, 2014). Furthermore, colonization sequence is also important for the ability of oral commensal streptococci to inhibit P. aeruginosa.…”

Section: Discussionmentioning

confidence: 99%

Nitrite reductase is critical for Pseudomonas aeruginosa survival during co-infection with the oral commensal Streptococcus parasanguinis

Scoffield

2016

Microbiology

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Pseudomonas aeruginosa is the major aetiological agent of chronic pulmonary infections in cystic fibrosis (CF) patients. However, recent evidence suggests that the polymicrobial community of the CF lung may also harbour oral streptococci, and colonization by these micro-organisms may have a negative impact on P. aeruginosa within the CF lung. Our previous studies demonstrated that nitrite abundance plays an important role in P. aeruginosa survival during co-infection with oral streptococci. Nitrite reductase is a key enzyme involved in nitrite metabolism. Therefore, the objective of this study was to examine the role nitrite reductase (gene nirS) plays in P. aeruginosa survival during co-infection with an oral streptococcus, Streptococcus parasanguinis. Inactivation of nirS in both the chronic CF isolate FRD1 and acute wound isolate PAO1 reduced the survival rate of P. aeruginosa when co-cultured with S. parasanguinis. Growth of both mutants was restored when co-cultured with S. parasanguinis that was defective for H 2 O 2 production. Furthermore, the nitrite reductase mutant was unable to kill Drosophila melanogaster during co-infection with S. parasanguinis. Taken together, these results suggest that nitrite reductase plays an important role for survival of P. aeruginosa during co-infection with S. parasanguinis.

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“…aeruginosa Liverpool Epidemic strain (LES) demonstrated increased numbers of AGS in co-culture and increased expression of virulence factors by P . aeruginosa giving a more pathogenic LES+AGS partnership [28]. Similarly LES pathogenicity was potentiated through co-culture with Mitis group streptococci including Streptococcus oralis , Streptococcus mitis , Streptococcus gordonii and Streptococcus sanguinis with co-operation or competition between the partners dependent on culture atmospheric conditions and order of colonisation [29].…”

Section: Introductionmentioning

confidence: 99%

“…Therefore the aim of this study was to determine whether AGS are able to grow in co-culture with a mucoid strain of P . aeruginosa under varying atmospheric conditions reflecting the range of microenvironments present in the CF lung and to characterise the interactions occurring between the two strains under hypercapnic conditions (10% CO 2 ) using the co-culture system used previously in this context [28,29]. This study demonstrates that AGS, the potentially key but previously unrecognised ‘hidden pathogens’ in CF airway infection [25] can co-exist and thrive together with the mucoid phenotype of the most common CF pathogen, P .…”

Section: Introductionmentioning

confidence: 99%

Modulation of behaviour and virulence of a high alginate expressing Pseudomonas aeruginosa strain from cystic fibrosis by oral commensal bacterium Streptococcus anginosus

2017

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Cystic fibrosis (CF) airways harbour complex and dynamic polymicrobial communities that include many oral bacteria. Despite increased knowledge of CF airway microbiomes the interaction between established CF pathogens and other resident microbes and resulting impact on disease progression is poorly understood. Previous studies have demonstrated that oral commensal streptococci of the Anginosus group (AGS) can establish chronic pulmonary infections and become numerically dominant in CF sputa indicating that they play an important role in CF microbiome dynamics. In this study a strain of Pseudomonas aeruginosa (DWW2) of the mucoid alginate overproducing phenotype associated with chronic CF airway infection and a strain of the oral commensal AGS species Streptococcus anginosus (3a) from CF sputum were investigated for their ability to co-exist and their responses to biofilm co-culture. Bacteria in biofilms were quantified, pyocyanin expression by DWW2 was measured and the effect of AGS strain 3a on reversion of DWW2 to a non-mucoidal phenotype investigated. The virulence of DWW2, 3a and colony variant phenotypes of DWW2 in mono- and co-culture were compared in a Galleria mellonella infection model. Co-culture biofilms were formed in normoxic, hypercapnic (10% CO2) and anoxic atmospheres with the streptococcus increasing in number in co-culture, indicating that these bacteria would be able to co-exist and thrive within the heterogeneous microenvironments of the CF airway. The streptococcus caused increased pyocyanin expression by DWW2 and colony variants by stimulating reversion of the mucoid phenotype to the high pyocyanin expressing non-mucoid phenotype. The latter was highly virulent in the infection model with greater virulence when in co-culture with the streptococcus. The results of this study demonstrate that the oral commensal S. anginosus benefits from interaction with P. aeruginosa of the CF associated mucoid phenotype and modulates the behaviour of the pseudomonad in ways that may be clinically relevant.

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Differential Potentiation of the Virulence of the Pseudomonas aeruginosa Cystic Fibrosis Liverpool Epidemic Strain by Oral Commensal Streptococci

Cited by 43 publications

References 48 publications

Phenotypic characterization of an international Pseudomonas aeruginosa reference panel: strains of cystic fibrosis (CF) origin show less in vivo virulence than non-CF strains

Phenotypic characterization of an international Pseudomonas aeruginosa reference panel: strains of cystic fibrosis (CF) origin show less in vivo virulence than non-CF strains

Nitrite reductase is critical for Pseudomonas aeruginosa survival during co-infection with the oral commensal Streptococcus parasanguinis

Modulation of behaviour and virulence of a high alginate expressing Pseudomonas aeruginosa strain from cystic fibrosis by oral commensal bacterium Streptococcus anginosus

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