Environment and Colonisation Sequence Are Key Parameters Driving Cooperation and Competition between Pseudomonas aeruginosa Cystic Fibrosis Strains and Oral Commensal Streptococci

Abstract

Cystic fibrosis (CF) patient airways harbour diverse microbial consortia that, in addition to the recognized principal pathogen Pseudomonas aeruginosa, include other bacteria commonly regarded as commensals. The latter include the oral (viridans) streptococci, which recent evidence indicates play an active role during infection of this environmentally diverse niche. As the interactions between inhabitants of the CF airway can potentially alter disease progression, it is important to identify key cooperators/competitors and environmental influences if therapeutic intervention is to be improved and pulmonary decline arrested. Importantly, we recently showed that virulence of the P. aeruginosa Liverpool Epidemic Strain (LES) could be potentiated by the Anginosus-group of streptococci (AGS). In the present study we explored the relationships between other viridans streptococci (Streptococcus oralis, Streptococcus mitis, Streptococcus gordonii and Streptococcus sanguinis) and the LES and observed that co-culture outcome was dependent upon inoculation sequence and environment. All four streptococcal species were shown to potentiate LES virulence factor production in co-culture biofilms. However, in the case of S. oralis interactions were environmentally determined; in air cooperation within a high cell density co-culture biofilm occurred together with stimulation of LES virulence factor production, while in an atmosphere containing added CO2 this species became a competitor antagonising LES growth through hydrogen peroxide (H2O2) production, significantly altering biofilm population dynamics and appearance. Streptococcus mitis, S. gordonii and S. sanguinis were also capable of H2O2 mediated inhibition of P. aeruginosa growth, but this was only visible when inoculated as a primary coloniser prior to introduction of the LES. Therefore, these observations, which are made in conditions relevant to the biology of CF disease pathogenesis, show that the pathogenic and colonisation potential of P. aeruginosa isolates can be modulated positively and negatively by the presence of oral commensal streptococci.

Effects of Propidium Monoazide (PMA) Treatment on Mycobiome and Bacteriome Analysis of Cystic Fibrosis Airways during Exacerbation

“…Several bacterial species detected in the CF respiratory microbiome here were also considered as the most frequent oral commensal bacteria such as Streptococcus , Prevotella , Porphyromonas , Rothia , Tannerella , Fusobacterium ,… This result confirmed the close relation between respiratory and buccal microbiotas due to microaspirations of salivary and potentially explained by the neutral dispersion model recently proposed [37–39]. In addition regarding the co-presence of Pseudomonas and oral commensal bacteria, there is recent evidences showing that the oral commensal streptococci could modulate the growth of Pseudomonas in CF disease condition [40]. …”

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

“…Furthermore, colonization sequence is also important for the ability of oral commensal streptococci to inhibit P. aeruginosa. S. gordonii and S. sanguinis inhibit the P. aeruginosa Liverpool epidemic strain in an H 2 O 2 -dependent manner when these streptococci are inoculated as the primary colonizer in the presence of CO 2 (Whiley et al, 2015), which is consistent with our previous and current studies that demonstrate H 2 O 2 -producing streptococci inhibit a chronic and acute isolate of P. aeruginosa in the presence of nitrite when oral commensal streptococci are the primary colonizers (Scoffield & Wu, 2015). Overall, more studies are required to strengthen our understanding of how H 2 O 2 -producing commensal streptococci and nitrite can negatively impact P. aeruginosa virulence.…”

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

“…More detailed examination of the interaction between DWW2 and 3a in a hypercapnic environment (10% CO 2 ) demonstrated increased virulence factor (pyocyanin) expression by the pseudomonad when in co-culture as seen previously with an LES and AGS partnership and between wound strain PAO1 and streptococci from the oropharynx [27,28,29]. The results from this study also demonstrated that the increase in pyocyanin was not due to increased expression throughout the biofilm but to the development of discrete pigmented areas within the biofilm that were dominated by the high pyocyanin expressing, non-mucoid phenotype together with higher numbers of the streptococcus which in turn was associated with an increased conversion of strain DWW2 from mucoid to non-mucoid.…”