Predominant pathogen competition and core microbiota divergence in chronic airway infection

Abstract

Chronic bacterial lung infections associated with non-cystic fibrosis bronchiectasis represent a substantial and growing health-care burden. Where Pseudomonas aeruginosa is the numerically dominant species within these infections, prognosis is significantly worse. However, in many individuals, Haemophilus influenzae predominates, a scenario associated with less severe disease. The mechanisms that determine which pathogen is most abundant are not known. We hypothesised that the distribution of H. influenzae and P. aeruginosa would be consistent with strong interspecific competition effects. Further, we hypothesised that where P. aeruginosa is predominant, it is associated with a distinct 'accessory microbiota' that reflects a significant interaction between this pathogen and the wider bacterial community. To test these hypotheses, we analysed 16S rRNA gene pyrosequencing data generated previously from 60 adult bronchiectasis patients, whose airway microbiota was dominated by either P. aeruginosa or H. influenzae. The relative abundances of the two dominant species in their respective groups were not significantly different, and when present in the opposite pathogen group the two species were found to be in very low abundance, if at all. These findings are consistent with strong competition effects, moving towards competitive exclusion. Ordination analysis indicated that the distribution of the core microbiota associated with each pathogen, readjusted after removal of the dominant species, was significantly divergent (analysis of similarity (ANOSIM), R ¼ 0.07, P ¼ 0.019). Taken together, these findings suggest that both interspecific competition and also direct and/or indirect interactions between the predominant species and the wider bacterial community may contribute to the predominance of P. aeruginosa in a subset of bronchiectasis lung infections.

Community dynamics and the lower airway microbiota in stable chronic obstructive pulmonary disease, smokers and healthy non-smokers

“…Community dominance of a single taxa, reported in other chronic respiratory diseases such as cystic fibrosis (CF)26 and bronchiectasis,27 28 was rarely observed in the COPD cohort, with the exception of three samples in which clinically relevant taxa ( P. aeruginosa, n=1 patient; Haemophilus influenzae , n=2 patients) were detected by culture. In general, single taxa dominance did not exceed 50% of the observed relative abundance within a sample.…”

Microbiomes in respiratory health and disease: An Asia‐Pacific perspective

“…As such, studies of the gut and oral microbiota performed in our region improve our understanding of the development and progression of respiratory diseases that afflict populations in this region and contribute to global understanding. While direct metagenomic investigations of the airway microbiome in Asian populations are limited, several studies have emerged that have assessed diseases of increased regional prevalence such as non‐CF bronchiectasis, Mycobacterium tuberculosis infection and lung cancer . In the most comprehensive of these studies, Rogers et al defined the airway microbiome of Australian non‐CF bronchiectasis patients .…”

Management of bronchiectasis in adults

“…and Neisseria sp. [25,26]. Clinical translation to date suggests that loss of diversity, with dominance of one or a few species, is associated with worse lung function and more exacerbations, and that loss of diversity may occur during exacerbations [25][26][27][28].…”

“…[25,26]. Clinical translation to date suggests that loss of diversity, with dominance of one or a few species, is associated with worse lung function and more exacerbations, and that loss of diversity may occur during exacerbations [25][26][27][28]. Overall these studies are consistent with data from culture based studies, with Pseudomonas aeruginosa dominance being associated with worse lung function and more exacerbations whether by molecular-or culture-based means and high bacterial loads of "classical" bronchiectasis pathogens being associated with higher neutrophilic inflammation and more exacerbations [28].…”