A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia

ABSTRACT Streptococcus pneumoniae acquires genes for resistance to antibiotics such as streptomycin (Str) or trimethoprim (Tmp) by recombination via transformation of DNA released by other pneumococci and closely related species. Using naturally transformable pneumococci, including strain D39 seroty...

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Autores principales:	Santiago M. Lattar, Xueqing Wu, Jennifer Brophy, Fuminori Sakai, Keith P. Klugman, Jorge E. Vidal
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Streptococcus pneumoniae antibiotic resistance consortial biofilms unidirectional transformation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/17abeb42db214578907bc8ca8d99c9e2
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spelling	oai:doaj.org-article:17abeb42db214578907bc8ca8d99c9e22021-11-15T16:00:25ZA Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia10.1128/mBio.00561-182150-7511https://doaj.org/article/17abeb42db214578907bc8ca8d99c9e22018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00561-18https://doaj.org/toc/2150-7511ABSTRACT Streptococcus pneumoniae acquires genes for resistance to antibiotics such as streptomycin (Str) or trimethoprim (Tmp) by recombination via transformation of DNA released by other pneumococci and closely related species. Using naturally transformable pneumococci, including strain D39 serotype 2 (S2) and TIGR4 (S4), we studied whether pneumococcal nasopharyngeal transformation was symmetrical, asymmetrical, or unidirectional. Incubation of S2Tet and S4Str in a bioreactor simulating the human nasopharynx led to the generation of SpnTet/Str recombinants. Double-resistant pneumococci emerged soon after 4 h postinoculation at a recombination frequency (rF) of 2.5 × 10−4 while peaking after 8 h at a rF of 1.1 × 10−3. Acquisition of antibiotic resistance genes by transformation was confirmed by treatment with DNase I. A high-throughput serotyping method demonstrated that all double-resistant pneumococci belonged to one serotype lineage (S2Tet/Str) and therefore that unidirectional transformation had occurred. Neither heterolysis nor availability of DNA for transformation was a factor for unidirectional transformation given that the density of each strain and extracellular DNA (eDNA) released from both strains were similar. Unidirectional transformation occurred regardless of the antibiotic-resistant gene carried by donors or acquired by recipients and regardless of whether competence-stimulating peptide-receptor cross talk was allowed. Moreover, unidirectional transformation occurred when two donor strains (e.g., S4Str and S19FTmp) were incubated together, leading to S19FStr/Tmp but at a rF 3 orders of magnitude lower (4.9 × 10−6). We finally demonstrated that the mechanism leading to unidirectional transformation was due to inhibition of transformation of the donor by the recipient. IMPORTANCE Pneumococcal transformation in the human nasopharynx may lead to the acquisition of antibiotic resistance genes or genes encoding new capsular variants. Antibiotics and vaccines are currently putting pressure on a number of strains, leading to an increase in antibiotic resistance and serotype replacement. These pneumococcal strains are also acquiring virulence traits from vaccine types via transformation. In this study, we recapitulated multiple-strain colonization with strains carrying a resistance marker and selected for those acquiring resistance to two or three antibiotics, such as would occur in the human nasopharynx. Strains acquiring dual and triple resistance originated from one progenitor, demonstrating that transformation was unidirectional. Unidirectional transformation was the result of inhibition of transformation of donor strains. Unidirectional transformation has implications for the understanding of acquisition patterns of resistance determinants or capsule-switching events.Santiago M. LattarXueqing WuJennifer BrophyFuminori SakaiKeith P. KlugmanJorge E. VidalAmerican Society for MicrobiologyarticleStreptococcus pneumoniaeantibiotic resistanceconsortial biofilmsunidirectional transformationMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Streptococcus pneumoniae antibiotic resistance consortial biofilms unidirectional transformation Microbiology QR1-502
spellingShingle	Streptococcus pneumoniae antibiotic resistance consortial biofilms unidirectional transformation Microbiology QR1-502 Santiago M. Lattar Xueqing Wu Jennifer Brophy Fuminori Sakai Keith P. Klugman Jorge E. Vidal A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia
description	ABSTRACT Streptococcus pneumoniae acquires genes for resistance to antibiotics such as streptomycin (Str) or trimethoprim (Tmp) by recombination via transformation of DNA released by other pneumococci and closely related species. Using naturally transformable pneumococci, including strain D39 serotype 2 (S2) and TIGR4 (S4), we studied whether pneumococcal nasopharyngeal transformation was symmetrical, asymmetrical, or unidirectional. Incubation of S2Tet and S4Str in a bioreactor simulating the human nasopharynx led to the generation of SpnTet/Str recombinants. Double-resistant pneumococci emerged soon after 4 h postinoculation at a recombination frequency (rF) of 2.5 × 10−4 while peaking after 8 h at a rF of 1.1 × 10−3. Acquisition of antibiotic resistance genes by transformation was confirmed by treatment with DNase I. A high-throughput serotyping method demonstrated that all double-resistant pneumococci belonged to one serotype lineage (S2Tet/Str) and therefore that unidirectional transformation had occurred. Neither heterolysis nor availability of DNA for transformation was a factor for unidirectional transformation given that the density of each strain and extracellular DNA (eDNA) released from both strains were similar. Unidirectional transformation occurred regardless of the antibiotic-resistant gene carried by donors or acquired by recipients and regardless of whether competence-stimulating peptide-receptor cross talk was allowed. Moreover, unidirectional transformation occurred when two donor strains (e.g., S4Str and S19FTmp) were incubated together, leading to S19FStr/Tmp but at a rF 3 orders of magnitude lower (4.9 × 10−6). We finally demonstrated that the mechanism leading to unidirectional transformation was due to inhibition of transformation of the donor by the recipient. IMPORTANCE Pneumococcal transformation in the human nasopharynx may lead to the acquisition of antibiotic resistance genes or genes encoding new capsular variants. Antibiotics and vaccines are currently putting pressure on a number of strains, leading to an increase in antibiotic resistance and serotype replacement. These pneumococcal strains are also acquiring virulence traits from vaccine types via transformation. In this study, we recapitulated multiple-strain colonization with strains carrying a resistance marker and selected for those acquiring resistance to two or three antibiotics, such as would occur in the human nasopharynx. Strains acquiring dual and triple resistance originated from one progenitor, demonstrating that transformation was unidirectional. Unidirectional transformation was the result of inhibition of transformation of donor strains. Unidirectional transformation has implications for the understanding of acquisition patterns of resistance determinants or capsule-switching events.
format	article
author	Santiago M. Lattar Xueqing Wu Jennifer Brophy Fuminori Sakai Keith P. Klugman Jorge E. Vidal
author_facet	Santiago M. Lattar Xueqing Wu Jennifer Brophy Fuminori Sakai Keith P. Klugman Jorge E. Vidal
author_sort	Santiago M. Lattar
title	A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia
title_short	A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia
title_full	A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia
title_fullStr	A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia
title_full_unstemmed	A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia
title_sort	mechanism of unidirectional transformation, leading to antibiotic resistance, occurs within nasopharyngeal pneumococcal biofilm consortia
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/17abeb42db214578907bc8ca8d99c9e2
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A Mechanism of Unidirectional Transformation, Leading to Antibiotic Resistance, Occurs within Nasopharyngeal Pneumococcal Biofilm Consortia

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