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Co-evolution with Staphylococcus aureus leads to lipopolysaccharide alterations in Pseudomonas aeruginosa.

ABSTRACT: Detrimental and beneficial interactions between co-colonizing bacteria may influence the course of infections. In cystic fibrosis (CF) airways, Staphylococcus aureus prevails in childhood, whereas Pseudomonas aeruginosa progressively predominates thereafter. While a range of interactions has been identified, it is unclear if these represent specific adaptations or correlated responses to other aspects of the environment. Here, we investigate how P. aeruginosa adapts to S. aureus by evolving P. aeruginosa in the presence and absence of S. aureus. P. aeruginosa populations that evolved for 150 generations were sequenced and compared to the ancestor strain. Mutations in the Wsp signaling system were identified in both treatments and likely occurred because of low oxygen availability. Despite showing increased killing activity, wsp mutants were less fit in the presence of S. aureus. In contrast, mutations in lipopolysaccharide (LPS) biosynthesis occurred exclusively in co-cultures with S. aureus and conferred a fitness gain in its presence. Moreover, they increased resistance towards beta-lactam antibiotics. Strikingly, both mutations in wsp and LPS genes are observed in clinical isolates from CF-patients. Our results suggest that P. aeruginosa LPS mutations are a direct consequence of S. aureus imposed selection in vitro.

SUBMITTER: Tognon M

PROVIDER: S-EPMC5607365 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Co-evolution with Staphylococcus aureus leads to lipopolysaccharide alterations in Pseudomonas aeruginosa.

Tognon Mikael M Köhler Thilo T Gdaniec Bartosz G BG Hao Youai Y Lam Joseph S JS Beaume Marie M Luscher Alexandre A Buckling Angus A van Delden Christian C

The ISME journal 20170526 10

Detrimental and beneficial interactions between co-colonizing bacteria may influence the course of infections. In cystic fibrosis (CF) airways, Staphylococcus aureus prevails in childhood, whereas Pseudomonas aeruginosa progressively predominates thereafter. While a range of interactions has been identified, it is unclear if these represent specific adaptations or correlated responses to other aspects of the environment. Here, we investigate how P. aeruginosa adapts to S. aureus by evolving P. a ...[more]

PMID: 28548661

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Project description:Host-associated bacteria and fungi, comprising the microbiota, are critical to host health. In the airways, the composition and diversity of the mucosal microbiota of patients are associated with airway health status. However, the relationship between airway microbiota and respiratory inflammation is not well-understood. Chronic rhinosinusitis (CRS) is a complex disease that affects up to 14% of the US population. Previous studies have shown decreased microbial diversity in CRS patients and enrichment of either Staphylococcus aureus or Pseudomonas aeruginosa. Although bacterial community composition is variable across CRS patients, Malassezia is a dominant fungal genus in the upper airways of the majority of healthy and CRS subjects. We hypothesize that distinct bacterial-fungal interactions differentially influence host mucosal immune response. Thus, we investigated in vitro and in vivo interactions between Malassezia sympodialis, P. aeruginosa, and S. aureus. The in vitro interactions were evaluated using the modified Kirby-Bauer Assay, Crystal Violet assay for biofilm, and FISH. A pilot murine model of acute sinusitis was used to investigate relationships with the host immune response. S. aureus and P. aeruginosa were intranasally instilled in the presence or absence of M. sympodialis (n = 66 total mice; 3-5/group). Changes in the microbiota were determined using 16S rRNA gene sequencing and host immune response was measured using quantitative real-time PCR (qRT-PCR). In vitro, only late stage planktonic P. aeruginosa and its biofilms inhibited M. sympodialis. Co-infection of mice with M. sympodialis and P. aeruginosa or S. aureus differently influenced the immune response. In co-infected mice, we demonstrate different expression of fungal sensing (Dectin-1), allergic responses (IL-5, and IL-13) and inflammation (IL-10, and IL-17) in murine sinus depending on the bacterial species that co-infected with M. sympodialis (p < 0.05). The pilot results suggest that species-specific interactions in airway-associated microbiota may be implicated driving immune responses. The understanding of the role of bacterial-fungal interactions in CRS will contribute to development of novel therapies toward manipulation of the airway microbiota.

Project description:Cystic fibrosis (CF) patients chronically infected with both Pseudomonas aeruginosa and Staphylococcus aureus have worse health outcomes than patients who are monoinfected with either P. aeruginosa or S. aureus We showed previously that mucoid strains of P. aeruginosa can coexist with S. aureusin vitro due to the transcriptional downregulation of several toxic exoproducts typically produced by P. aeruginosa, including siderophores, rhamnolipids, and HQNO (2-heptyl-4-hydroxyquinoline N-oxide). Here, we demonstrate that exogenous alginate protects S. aureus from P. aeruginosa in both planktonic and biofilm coculture models under a variety of nutritional conditions. S. aureus protection in the presence of exogenous alginate is due to the transcriptional downregulation of pvdA, a gene required for the production of the iron-scavenging siderophore pyoverdine as well as the downregulation of the PQS (Pseudomonas quinolone signal) (2-heptyl-3,4-dihydroxyquinoline) quorum sensing system. The impact of exogenous alginate is independent of endogenous alginate production. We further demonstrate that coculture of mucoid P. aeruginosa with nonmucoid P. aeruginosa strains can mitigate the killing of S. aureus by the nonmucoid strain of P. aeruginosa, indicating that the mechanism that we describe here may function in vivo in the context of mixed infections. Finally, we investigated a panel of mucoid clinical isolates that retain the ability to kill S. aureus at late time points and show that each strain has a unique expression profile, indicating that mucoid isolates can overcome the S. aureus-protective effects of mucoidy in a strain-specific manner.IMPORTANCE CF patients are chronically infected by polymicrobial communities. The two dominant bacterial pathogens that infect the lungs of CF patients are P. aeruginosa and S. aureus, with ∼30% of patients coinfected by both species. Such coinfected individuals have worse outcomes than monoinfected patients, and both species persist within the same physical space. A variety of host and environmental factors have been demonstrated to promote P. aeruginosa-S. aureus coexistence, despite evidence that P. aeruginosa kills S. aureus when these organisms are cocultured in vitro Thus, a better understanding of P. aeruginosa-S. aureus interactions, particularly mechanisms by which these microorganisms are able to coexist in proximal physical space, will lead to better-informed treatments for chronic polymicrobial infections.

Dataset Information

Co-evolution with Staphylococcus aureus leads to lipopolysaccharide alterations in Pseudomonas aeruginosa.

Publications

Co-evolution with Staphylococcus aureus leads to lipopolysaccharide alterations in Pseudomonas aeruginosa.

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