Taxonomic position, antibiotic resistance and virulence factor production by Stenotrophomonas isolates from patients with cystic fibrosis and other chronic respiratory infections.
Antibiotic resistance
Cystic fibrosis
Respiratory infection
Stenotrophomonas
Taxonomy
Virulence
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
12 05 2022
12 05 2022
Historique:
received:
21
05
2021
accepted:
07
02
2022
entrez:
13
5
2022
pubmed:
14
5
2022
medline:
18
5
2022
Statut:
epublish
Résumé
The potential pathogenic role of Stenotrophomonas maltophilia in lung disease and in particular in cystic fibrosis is unclear. To develop further understanding of the biology of this taxa, the taxonomic position, antibiotic resistance and virulence factors of S. maltophilia isolates from patients with chronic lung disease were studied. A total of 111 isolates recovered between 2003 and 2016 from respiratory samples from patients in five different countries were included. Based on a cut-off of 95%, analysis of average nucleotide identity by BLAST (ANIb) showed that the 111 isolates identified as S. maltophilia by Matrix-assisted laser desorption/ionization time of flight mass spectrometry (MALDI-TOF/MS) belonged to S. maltophilia (n = 65), S. pavanii (n = 6) and 13 putative novel species (n = 40), which each included 1-5 isolates; these groupings coincided with the results of the 16S rDNA analysis, and the L1 and L2 ß-lactamase Neighbor-Joining phylogeny. Chromosomally encoded aminoglycoside resistance was identified in all S. maltophilia and S. pavani isolates, while acquired antibiotic resistance genes were present in only a few isolates. Nevertheless, phenotypic resistance levels against commonly used antibiotics, determined by standard broth microbroth dilution, were high. Although putative virulence genes were present in all isolates, the percentage of positive isolates varied. The Xps II secretion system responsible for the secretion of the StmPr1-3 proteases was mainly limited to isolates identified as S. maltophilia based on ANIb, but no correlation with phenotypic expression of protease activity was found. The RPF two-component quorum sensing system involved in virulence and antibiotic resistance expression has two main variants with one variant lacking 190 amino acids in the sensing region. The putative novel Stenotrophomonas species recovered from patient samples and identified by MALDI-TOF/MS as S. maltophilia, differed from S. maltophilia in resistance and virulence genes, and therefore possibly in pathogenicity. Revision of the Stenotrophomonas taxonomy is needed in order to reliably identify strains within the genus and elucidate the role of the different species in disease.
Sections du résumé
BACKGROUND
The potential pathogenic role of Stenotrophomonas maltophilia in lung disease and in particular in cystic fibrosis is unclear. To develop further understanding of the biology of this taxa, the taxonomic position, antibiotic resistance and virulence factors of S. maltophilia isolates from patients with chronic lung disease were studied.
RESULTS
A total of 111 isolates recovered between 2003 and 2016 from respiratory samples from patients in five different countries were included. Based on a cut-off of 95%, analysis of average nucleotide identity by BLAST (ANIb) showed that the 111 isolates identified as S. maltophilia by Matrix-assisted laser desorption/ionization time of flight mass spectrometry (MALDI-TOF/MS) belonged to S. maltophilia (n = 65), S. pavanii (n = 6) and 13 putative novel species (n = 40), which each included 1-5 isolates; these groupings coincided with the results of the 16S rDNA analysis, and the L1 and L2 ß-lactamase Neighbor-Joining phylogeny. Chromosomally encoded aminoglycoside resistance was identified in all S. maltophilia and S. pavani isolates, while acquired antibiotic resistance genes were present in only a few isolates. Nevertheless, phenotypic resistance levels against commonly used antibiotics, determined by standard broth microbroth dilution, were high. Although putative virulence genes were present in all isolates, the percentage of positive isolates varied. The Xps II secretion system responsible for the secretion of the StmPr1-3 proteases was mainly limited to isolates identified as S. maltophilia based on ANIb, but no correlation with phenotypic expression of protease activity was found. The RPF two-component quorum sensing system involved in virulence and antibiotic resistance expression has two main variants with one variant lacking 190 amino acids in the sensing region.
CONCLUSIONS
The putative novel Stenotrophomonas species recovered from patient samples and identified by MALDI-TOF/MS as S. maltophilia, differed from S. maltophilia in resistance and virulence genes, and therefore possibly in pathogenicity. Revision of the Stenotrophomonas taxonomy is needed in order to reliably identify strains within the genus and elucidate the role of the different species in disease.
Identifiants
pubmed: 35549675
doi: 10.1186/s12866-022-02466-5
pii: 10.1186/s12866-022-02466-5
pmc: PMC9097388
doi:
Substances chimiques
Anti-Bacterial Agents
0
Virulence Factors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
129Informations de copyright
© 2022. The Author(s).
Références
Antimicrob Agents Chemother. 2001 Feb;45(2):413-9
pubmed: 11158734
Front Microbiol. 2015 Sep 16;6:951
pubmed: 26441885
J Antimicrob Chemother. 2005 Jul;56(1):220-3
pubmed: 15928010
PLoS One. 2014 Oct 06;9(10):e108409
pubmed: 25285537
Infect Dis (Lond). 2019 Mar;51(3):168-178
pubmed: 30422737
J Cyst Fibros. 2016 May;15(3):357-65
pubmed: 26429520
Clin Microbiol Infect. 2015 May;21(5):464-7
pubmed: 25753190
BMC Microbiol. 2010 Apr 07;10:102
pubmed: 20374629
Evolution. 1985 Jul;39(4):783-791
pubmed: 28561359
Proc Natl Acad Sci U S A. 2009 Nov 10;106(45):19126-31
pubmed: 19855009
Antimicrob Agents Chemother. 2015 Nov;59(11):7136-41
pubmed: 26349828
Pediatr Pulmonol. 2018 Apr;53(4):426-430
pubmed: 29314745
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549
pubmed: 29722887
J Biol Chem. 2014 Jan 3;289(1):312-25
pubmed: 24257754
Proc Natl Acad Sci U S A. 2004 Jul 27;101(30):11030-5
pubmed: 15258291
Clin Microbiol Infect. 2004 Apr;10(4):272-88
pubmed: 15059115
Eur Respir J. 2018 Jul 11;52(1):
pubmed: 29946004
J Med Microbiol. 2018 Jul;67(7):992-1002
pubmed: 29799387
Arch Microbiol. 2018 Jan;200(1):183-187
pubmed: 28965241
Antimicrob Agents Chemother. 2004 Feb;48(2):666-9
pubmed: 14742234
Res Microbiol. 2007 Oct-Nov;158(8-9):702-11
pubmed: 18054205
Afr Health Sci. 2020 Sep;20(3):1118-1123
pubmed: 33402956
Infect Immun. 2015 Oct;83(10):3825-37
pubmed: 26169274
Int J Med Microbiol. 2011 Jan;301(1):34-43
pubmed: 20952251
Front Microbiol. 2015 Jul 28;6:761
pubmed: 26284046
Environ Microbiol. 2014 May;16(5):1282-96
pubmed: 24447641
J Cyst Fibros. 2012 May;11(3):163-72
pubmed: 22138067
Int J Syst Bacteriol. 1999 Oct;49 Pt 4:1749-60
pubmed: 10555357
J Antimicrob Chemother. 2012 Nov;67(11):2640-4
pubmed: 22782487
Mol Biol Evol. 1987 Jul;4(4):406-25
pubmed: 3447015
BMC Microbiol. 2011 Jul 05;11:159
pubmed: 21729271
J Bacteriol. 2007 Jul;189(13):4964-8
pubmed: 17468254
Antimicrob Agents Chemother. 1998 Apr;42(4):921-6
pubmed: 9559809
Lett Appl Microbiol. 2006 Oct;43(4):443-9
pubmed: 16965377
ISME J. 2012 May;6(5):939-50
pubmed: 22134647
ACS Infect Dis. 2016 Jan 8;2(1):62-70
pubmed: 27622948
J Bacteriol. 2009 May;191(9):2934-43
pubmed: 19251858
Antimicrob Agents Chemother. 2010 Jan;54(1):580-1
pubmed: 19841154
Int J Antimicrob Agents. 2019 Jan;53(1):84-88
pubmed: 30240837
Infect Immun. 2017 Nov 17;85(12):
pubmed: 28893914
Mol Microbiol. 2008 Apr;68(1):75-86
pubmed: 18312265
Antimicrob Agents Chemother. 1997 Jul;41(7):1460-4
pubmed: 9210666
Front Microbiol. 2017 Nov 30;8:2276
pubmed: 29250041
J Bacteriol. 2007 Sep;189(18):6695-703
pubmed: 17631636
J Bacteriol. 2014 Jul;196(13):2431-42
pubmed: 24769700
Biochim Biophys Acta. 1994 Jun 21;1218(2):199-201
pubmed: 8018721
Front Microbiol. 2017 Aug 17;8:1548
pubmed: 28861062