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Cooperativity between Stenotrophomonas maltophilia and Pseudomonas aeruginosa during polymicrobial airway infections.

Abstract

Stenotrophomonas maltophilia is a Gram-negative bacterium found ubiquitously in the environment that has historically been regarded as nonpathogenic. S. maltophilia is increasingly observed in patient sputa in cystic fibrosis (CF), and while existing epidemiology indicates that patients with S. maltophilia have poorer diagnoses, its clinical significance remains unclear. Moreover, as multidrug resistance is common among S. maltophilia isolates, treatment options for these infections may be limited. Here we investigated the pathogenicity of S. maltophilia alone and during polymicrobial infection with Pseudomonas aeruginosa. Colonization, persistence, and virulence of S. maltophilia were assessed in experimental respiratory infections of mice. The results of this study indicate that S. maltophilia transiently colonizes the lung accompanied by significant weight loss and immune cell infiltration, and the expression of early inflammatory markers including IL-6, IL-1α, and TNF-α. Importantly, polymicrobial infection with P. aeruginosa elicited significantly higher S. maltophilia counts in bronchoalveolar lavages and lung tissue homogenates. This increase in bacterial load was directly correlated with the density of the P. aeruginosa population, and required viable P. aeruginosa bacteria. Microscopic analysis of biofilms formed in vitro revealed that S. maltophilia formed well-integrated biofilms with P. aeruginosa, and these organisms colocalize in the lung during dual species infection. Based on these results, we conclude that active cellular processes by P. aeruginosa afford significant benefit to S. maltophilia during polymicrobial infections. Further, these results indicate that S. maltophilia may have clinical significance in respiratory infections.

Authors+Show Affiliations

Division of Pulmonary, Allergy and Critical Care Medicine Gregory Fleming James Center for Cystic Fibrosis Research Comparative Pathology Laboratory, University of Alabama at Birmingham. Division of Pulmonary, Allergy and Critical Care Medicine Gregory Fleming James Center for Cystic Fibrosis Research Comparative Pathology Laboratory, University of Alabama at Birmingham.Division of Pulmonary, Allergy and Critical Care Medicine Gregory Fleming James Center for Cystic Fibrosis Research Comparative Pathology Laboratory, University of Alabama at Birmingham.Division of Pulmonary, Allergy and Critical Care Medicine Gregory Fleming James Center for Cystic Fibrosis Research Comparative Pathology Laboratory, University of Alabama at Birmingham wswords@uabmc.edu. Division of Pulmonary, Allergy and Critical Care Medicine Gregory Fleming James Center for Cystic Fibrosis Research Comparative Pathology Laboratory, University of Alabama at Birmingham.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31932329

Citation

McDaniel, Melissa S., et al. "Cooperativity Between Stenotrophomonas Maltophilia and Pseudomonas Aeruginosa During Polymicrobial Airway Infections." Infection and Immunity, 2020.
McDaniel MS, Schoeb T, Swords WE. Cooperativity between Stenotrophomonas maltophilia and Pseudomonas aeruginosa during polymicrobial airway infections. Infect Immun. 2020.
McDaniel, M. S., Schoeb, T., & Swords, W. E. (2020). Cooperativity between Stenotrophomonas maltophilia and Pseudomonas aeruginosa during polymicrobial airway infections. Infection and Immunity, doi:10.1128/IAI.00855-19.
McDaniel MS, Schoeb T, Swords WE. Cooperativity Between Stenotrophomonas Maltophilia and Pseudomonas Aeruginosa During Polymicrobial Airway Infections. Infect Immun. 2020 Jan 13; PubMed PMID: 31932329.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Cooperativity between Stenotrophomonas maltophilia and Pseudomonas aeruginosa during polymicrobial airway infections. AU - McDaniel,Melissa S, AU - Schoeb,Trenton, AU - Swords,W Edward, Y1 - 2020/01/13/ PY - 2020/1/15/entrez JF - Infection and immunity JO - Infect. Immun. N2 - Stenotrophomonas maltophilia is a Gram-negative bacterium found ubiquitously in the environment that has historically been regarded as nonpathogenic. S. maltophilia is increasingly observed in patient sputa in cystic fibrosis (CF), and while existing epidemiology indicates that patients with S. maltophilia have poorer diagnoses, its clinical significance remains unclear. Moreover, as multidrug resistance is common among S. maltophilia isolates, treatment options for these infections may be limited. Here we investigated the pathogenicity of S. maltophilia alone and during polymicrobial infection with Pseudomonas aeruginosa. Colonization, persistence, and virulence of S. maltophilia were assessed in experimental respiratory infections of mice. The results of this study indicate that S. maltophilia transiently colonizes the lung accompanied by significant weight loss and immune cell infiltration, and the expression of early inflammatory markers including IL-6, IL-1α, and TNF-α. Importantly, polymicrobial infection with P. aeruginosa elicited significantly higher S. maltophilia counts in bronchoalveolar lavages and lung tissue homogenates. This increase in bacterial load was directly correlated with the density of the P. aeruginosa population, and required viable P. aeruginosa bacteria. Microscopic analysis of biofilms formed in vitro revealed that S. maltophilia formed well-integrated biofilms with P. aeruginosa, and these organisms colocalize in the lung during dual species infection. Based on these results, we conclude that active cellular processes by P. aeruginosa afford significant benefit to S. maltophilia during polymicrobial infections. Further, these results indicate that S. maltophilia may have clinical significance in respiratory infections. SN - 1098-5522 UR - https://www.unboundmedicine.com/medline/citation/31932329/Cooperativity_between_Stenotrophomonas_maltophilia_and_Pseudomonas_aeruginosa_during_polymicrobial_airway_infections L2 - http://iai.asm.org/cgi/pmidlookup?view=long&pmid=31932329 DB - PRIME DP - Unbound Medicine ER -