Community Composition Determines Activity of Antibiotics against Multispecies Biofilms

Tavernier, Sarah; Crabbé, Aurélie; Hacıoğlu, Mayram; Stuer, Liesbeth; Henry, Silke; Rigole, Petra; Dhondt, Inne; Coenye, Tom

doi:10.1128/aac.00302-17

Cited by 44 publications

(29 citation statements)

References 57 publications

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“…Furthermore, using an in vivo burn wound co-infection model of P. aeruginosa and S. aureus, RADLINSKI et al [66] found that the antibiotic-potentiating effect of LasA dominates over the antibiotic-antagonising effect of HQNO, resulting in a net increased susceptibility of S. aureus in the presence of P. aeruginosa. These data are in agreement with recent findings by TAVERNIER et al [49], who reported a decreased tolerance of S. aureus to different antibiotic classes when grown in a multispecies biofilm with P. aeruginosa and S. anginosus. Co-culturing of S. aureus with these two CF community members prevented vancomycin-induced thickening of the cell wall (a protective mechanism during antibiotic exposure), which might be explained by the production of LasA by P. aeruginosa [66].…”

Section: Through Alterations Of the Cell Wallsupporting

confidence: 94%

“…The enhanced tolerance of S. anginosus to vancomycin was due to an increased cell wall thickness, as a result of co-culturing with these CF pathogens [50]. Furthermore, it was found that soluble factors produced by S. aureus were mediating the enhanced antibiotic tolerance in the described multispecies community, in a strain-independent manner [49]. Another example of antibiotic protection through alterations of cell wall components was described by TOGNON et al [51].…”

Section: Through Alterations Of the Cell Wallmentioning

confidence: 95%

“…Another mechanism that may enable CF pathogens to be protected from antibiotic treatment is through effects of members of the lung microbiome on the cell wall. Streptococcus anginosus grown in a biofilm with P. aeruginosa and S. aureus became more tolerant to various cell wall-acting antibiotics [49]. The enhanced tolerance of S. anginosus to vancomycin was due to an increased cell wall thickness, as a result of co-culturing with these CF pathogens [50].…”

Section: Through Alterations Of the Cell Wallmentioning

confidence: 99%

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Influence of the lung microbiome on antibiotic susceptibility of cystic fibrosis pathogens

et al. 2019

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The lungs of patients with cystic fibrosis (CF) are colonised by a microbial community comprised of pathogenic species, such as Pseudomonas aeruginosa and Staphylococcus aureus, and microorganisms that are typically not associated with worse clinical outcomes (considered as commensals). Antibiotics directed at CF pathogens are often not effective and a discrepancy is observed between activity of these agents in vitro and in the patient. This review describes how interspecies interactions within the lung microbiome might influence the outcome of antibiotic treatment targeted at common CF pathogens. Protective mechanisms by members of the microbiome such as antibiotic degradation (indirect pathogenicity), alterations of the cell wall, production of matrix components decreasing antibiotic penetration, and changes in metabolism are discussed. Interspecies interactions that increase bacterial susceptibility are also addressed. Furthermore, we discuss how experimental conditions, such as culture media, oxygen levels, incorporation of host–pathogen interactions, and microbial community composition may influence the outcome of microbial interaction studies related to antibiotic activity. Hereby, the importance to create in vitro conditions reflective of the CF lung microenvironment is highlighted. Understanding the role of the CF lung microbiome in antibiotic efficacy may help find novel therapeutic and diagnostic approaches to better tackle chronic lung infections in this patient population.

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Section: Through Alterations Of the Cell Wallsupporting

confidence: 94%

Section: Through Alterations Of the Cell Wallmentioning

confidence: 95%

Section: Through Alterations Of the Cell Wallmentioning

confidence: 99%

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Influence of the lung microbiome on antibiotic susceptibility of cystic fibrosis pathogens

et al. 2019

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“…Due to this reduced mucociliary clearance, bacteria colonize the lungs of patients with CF and establish chronic, polymicrobial infections that cause increased inflammation and respiratory function decline (2). Recent studies have demonstrated that the microbiota in the lungs form polymicrobial biofilms, and that mixed bacterial biofilm populations can affect antibiotic tolerance and bacterial virulence (3, 4).…”

Section: Introductionmentioning

confidence: 99%

Pseudomonas aeruginosaCan Inhibit Growth of Streptococcal Species via Siderophore Production

Scott

Filkins

et al. 2018

Preprint

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Cystic Fibrosis (CF) is a genetic disease that causes patients to accumulate thick, dehydrated mucus in the lung and develop chronic, polymicrobial infections due to reduced mucociliary clearance. These chronic polymicrobial infections and subsequent decline in lung function are significant factors in the morbidity and mortality of CF. Pseudomonas aeruginosa and Streptococcus spp. are among the most prevalent organisms in the CF lung; the presence of P. aeruginosa correlates with lung function decline and the Streptococcus milleri group (SMG), a subgroup of the viridans streptococci, is associated with exacerbations in patients with CF. Here we characterize the interspecies interactions that occur between these two genera. We demonstrated that multiple P. aeruginosa laboratory strains and clinical CF isolates promote the growth of multiple SMG strains and oral streptococci in an in vitro coculture system. We investigated the mechanism by which P. aeruginosa enhances growth of streptococci by screening for mutants of P. aeruginosa PA14 unable to enhance Streptococcus growth, and we identified the P. aeruginosa pqsL::TnM mutant, which failed to promote growth of S. constellatus and S. sanguinis. Characterization of the P. aeruginosa ΔpqsL mutant revealed that this strain cannot promote Streptococcus growth. Our genetic data and growth studies support a model whereby the P. aeruginosa ΔpqsL mutant overproduces siderophores, and thus likely outcompetes Streptococcus sanguinis for limited iron. We propose a model whereby competition for iron represents one important means of interaction between P. aeruginosa and Streptococcus spp.ImportanceCystic fibrosis (CF) lung infections are increasingly recognized for their polymicrobial nature. These polymicrobial infections may alter the biology of the organisms involved in CF-related infections, leading to changes in growth, virulence and/or antibiotic tolerance, and could thereby affect patient health and response to treatment. In this study, we demonstrate interactions between P. aeruginosa and streptococci using a coculture model, and show that one interaction between these microbes is likely competition for iron. Thus, these data indicate that one CF pathogen may influence the growth of another and add to our limited knowledge of polymicrobial interactions in the CF airway.

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“…decline (2). Recent studies have demonstrated that the microbiota in the lungs form polymicrobial biofilms and that mixed bacterial biofilm populations can affect antibiotic tolerance and bacterial virulence (3,65).…”

mentioning

confidence: 99%

Pseudomonas aeruginosa Can Inhibit Growth of Streptococcal Species via Siderophore Production

Scott

Filkins

et al. 2019

J Bacteriol

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Cystic fibrosis (CF) is a genetic disease that causes patients to accumulate thick, dehydrated mucus in the lung and develop chronic, polymicrobial infections due to reduced mucociliary clearance. These chronic polymicrobial infections and subsequent decline in lung function are significant factors in the morbidity and mortality of CF. Pseudomonas aeruginosa and Streptococcus spp. are among the most prevalent organisms in the CF lung; the presence of P. aeruginosa correlates with lung function decline, and the Streptococcus milleri group (SMG), a subgroup of the viridans streptococci, is associated with exacerbations in patients with CF. Here we characterized the interspecies interactions that occur between these two genera. We demonstrated that multiple P. aeruginosa laboratory strains and clinical CF isolates promote the growth of multiple SMG strains and oral streptococci in an in vitro coculture system. We investigated the mechanism by which P. aeruginosa enhances growth of streptococci by screening for mutants of P. aeruginosa PA14 that are unable to enhance Streptococcus growth, and we identified the P. aeruginosa pqsL::TnM mutant, which failed to promote growth of Streptococcus constellatus and S. sanguinis. Characterization of the P. aeruginosa ΔpqsL mutant revealed that this strain cannot promote Streptococcus growth. Our genetic data and growth studies support a model whereby the P. aeruginosa ΔpqsL mutant overproduces siderophores and thus likely outcompetes Streptococcus sanguinis for limited iron. We propose a model whereby competition for iron represents one important means of interaction between P. aeruginosa and Streptococcus spp. IMPORTANCE Cystic fibrosis (CF) lung infections are increasingly recognized for their polymicrobial nature. These polymicrobial infections may alter the biology of the organisms involved in CF-related infections, leading to changes in growth, virulence, and/or antibiotic tolerance, and could thereby affect patient health and response to treatment. In this study, we demonstrate interactions between P. aeruginosa and streptococci using a coculture model and show that one interaction between these microbes is likely competition for iron. Thus, these data indicate that one CF pathogen may influence the growth of another, and they add to our limited knowledge of polymicrobial interactions in the CF airway.

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Community Composition Determines Activity of Antibiotics against Multispecies Biofilms

Cited by 44 publications

References 57 publications

Influence of the lung microbiome on antibiotic susceptibility of cystic fibrosis pathogens

Influence of the lung microbiome on antibiotic susceptibility of cystic fibrosis pathogens

Pseudomonas aeruginosaCan Inhibit Growth of Streptococcal Species via Siderophore Production

Pseudomonas aeruginosa Can Inhibit Growth of Streptococcal Species via Siderophore Production

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