Contribution of Short Chain Fatty Acids to the Growth of Pseudomonas aeruginosa in Rhinosinusitis

Do Yeon Cho, Daniel Skinner, Ryan C. Hunter, Christopher Weeks, Dong Jin Lim, Harrison Thompson, Christopher R. Walz, Shaoyan Zhang, Jessica W. Grayson, William E. Swords, Steven M. Rowe, Bradford A. Woodworth

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Abstract

Background: Chronic rhinosinusitis (CRS) is characterized by complex bacterial infections with persistent inflammation. Based on our rabbit model of sinusitis, blockage of sinus ostia generated a shift in microbiota to a predominance of mucin degrading microbes (MDM) with acute inflammation at 2 weeks. This was followed by conversion to chronic sinus inflammation at 3 months with a robust increase in pathogenic bacteria (e.g., Pseudomonas). MDMs are known to produce acid metabolites [short chain fatty acids (SCFA)] that have the potential to stimulate pathogen growth by offering a carbon source to non-fermenting sinus pathogens (e.g., Pseudomonas). The objective of this study is to evaluate the concentrations of SCFA within the mucus and its contribution to the growth of P. aeruginosa. Methods: Healthy and sinusitis mucus from the rabbit model were collected and co-cultured with the PAO1 strain of P. aeruginosa for 72 h and colony forming units (CFUs) were determined with the targeted quantification of three SCFAs (acetate, propionate, butyrate). Quantification of SCFAs in healthy and sinusitis mucus from patients with P. aeruginosa was also performed via high performance liquid chromatography. Results: To provide evidence of fermentative activity, SCFAs were quantified within the mucus samples from rabbits with and without sinusitis. Acetate concentrations were significantly greater in sinusitis mucus compared to controls (4.13 ± 0.53 vs. 1.94 ± 0.44 mM, p < 0.01). After 72 h of co-culturing mucus samples with PAO1 in the presence of mucin medium, the blue-green pigment characteristic of Pseudomonas was observed throughout tubes containing sinusitis mucus. CFUs were higher in cultures containing mucus samples from sinusitis (8.4 × 109 ± 4.8 × 107) compared to control (1.4 × 109 ± 2.0 × 107) or no mucus (1.5 × 109 ± 2.1 × 107) (p < 0.0001). To provide evidence of fermentative activity in human CRS with P. aeruginosa, the presence of SCFAs in human mucus was analyzed and all SCFAs were significantly higher in CRS with P. aeruginosa compared to controls (p < 0.05). Conclusion: Given that SCFAs are solely derived from bacterial fermentation, our evidence suggests a critical role for mucin-degrading bacteria in generating carbon-source nutrients for pathogens. MDM may contribute to the development of recalcitrant CRS by degrading mucins, thus providing nutrients for potential pathogens like P. aeruginosa.

Original languageEnglish (US)
Article number412
JournalFrontiers in Cellular and Infection Microbiology
Volume10
DOIs
StatePublished - Aug 11 2020

Bibliographical note

Funding Information:
A part of this manuscript was presented at North American Cystic Fibrosis Conference 2018 in Denver, Colorado. Funding. This work was supported by National Institutes of Health (NIH)/National Heart, Lung, and Blood Institute (1 R01 HL133006-05) to BW; National Institute of Diabetes and Digestive and Kidney Diseases (5P30DK072482-02) to SR; and NIH/National Institutes of Allergy and Infectious disease (K08AI146220), John W. Kirklin Research and Education Foundation Fellowship Award, UAB Faculty Development Research Award, American Rhinologic Society New Investigator Award, Triological Society Career Development Award, and Cystic Fibrosis Foundation K08 Boost Award (CHO20A0-KB) to D-YC.

Publisher Copyright:
© Copyright © 2020 Cho, Skinner, Hunter, Weeks, Lim, Thompson, Walz, Zhang, Grayson, Swords, Rowe and Woodworth.

Keywords

  • Chronic sinusitis
  • anaerobes
  • fermentation
  • hypoxia
  • mucin-fermenter
  • pseudomonas
  • rhinosinusitis
  • short chain fatty acid

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

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