Biofilm Formation by Streptococcus pneumoniae: Role of Choline, Extracellular DNA, and Capsular Polysaccharide in Microbial Accretion

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Published inJournal of Bacteriology Vol. 188; no. 22; pp. 7785 - 7795
Main Authors MOSCOSO, Miriam, GARCIA, Ernesto, LOPEZ, Rubens
Format Journal Article
LanguageEnglish
Published Washington, DC American Society for Microbiology 01.11.2006
Subjects
Amidohydrolases - genetics
Amidohydrolases - physiology
Antigens, Bacterial - genetics
Antigens, Bacterial - physiology
Bacterial Capsules - physiology
Bacterial Proteins - genetics
Bacterial Proteins - physiology
Bacteriology
Biofilms - growth & development
Biological and medical sciences
Carrier Proteins - genetics
Carrier Proteins - physiology
Choline - metabolism
Choline - physiology
DNA, Bacterial - physiology
Fundamental and applied biological sciences. Psychology
Glass
Humans
Microbial Communities and Interactions
Microbiology
Miscellaneous
Muramidase - genetics
Muramidase - physiology
Mutation
N-Acetylmuramoyl-L-alanine Amidase - genetics
N-Acetylmuramoyl-L-alanine Amidase - physiology
Pneumococcal Infections - microbiology
Polystyrenes
Streptococcus pneumoniae
Streptococcus pneumoniae - physiology
Teichoic Acids - chemistry
Microorganism capsule
Choleretic
Streptococcaceae
Microbiology
Hepatoprotector
Choline
Biofilm
Bacteria
Micrococcales
Polysaccharide
Bacteriology
Streptococcus pneumoniae
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Abstract Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue JB About JB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0021-9193 Online ISSN: 1098-5530 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JB .asm.org, visit: JB       
AbstractList Streptococcus pneumoniae colonizes the human upper respiratory tract, and this asymptomatic colonization is known to precede pneumococcal disease. In this report, chemically defined and semisynthetic media were used to identify the initial steps of biofilm formation by pneumococcus during growth on abiotic surfaces such as polystyrene or glass. Unencapsulated pneumococci adhered to abiotic surfaces and formed a three-dimensional structure about 25 microm deep, as observed by confocal laser scanning microscopy and low-temperature scanning electron microscopy. Choline residues of cell wall teichoic acids were found to play a fundamental role in pneumococcal biofilm development. The role in biofilm formation of choline-binding proteins, which anchor to the teichoic acids of the cell envelope, was determined using unambiguously characterized mutants. The results showed that LytA amidase, LytC lysozyme, LytB glucosaminidase, CbpA adhesin, PcpA putative adhesin, and PspA (pneumococcal surface protein A) mutants had a decreased capacity to form biofilms, whereas no such reduction was observed in Pce phosphocholinesterase or CbpD putative amidase mutants. Moreover, encapsulated, clinical pneumococcal isolates were impaired in their capacity to form biofilms. In addition, a role for extracellular DNA and proteins in the establishment of S. pneumoniae biofilms was demonstrated. Taken together, these observations provide information on conditions that favor the sessile mode of growth by S. pneumoniae. The experimental approach described here should facilitate the study of bacterial genes that are required for biofilm formation. Those results, in turn, may provide insight into strategies to prevent pneumococcal colonization of its human host.
ABSTRACT Streptococcus pneumoniae colonizes the human upper respiratory tract, and this asymptomatic colonization is known to precede pneumococcal disease. In this report, chemically defined and semisynthetic media were used to identify the initial steps of biofilm formation by pneumococcus during growth on abiotic surfaces such as polystyrene or glass. Unencapsulated pneumococci adhered to abiotic surfaces and formed a three-dimensional structure about 25 μm deep, as observed by confocal laser scanning microscopy and low-temperature scanning electron microscopy. Choline residues of cell wall teichoic acids were found to play a fundamental role in pneumococcal biofilm development. The role in biofilm formation of choline-binding proteins, which anchor to the teichoic acids of the cell envelope, was determined using unambiguously characterized mutants. The results showed that LytA amidase, LytC lysozyme, LytB glucosaminidase, CbpA adhesin, PcpA putative adhesin, and PspA (pneumococcal surface protein A) mutants had a decreased capacity to form biofilms, whereas no such reduction was observed in Pce phosphocholinesterase or CbpD putative amidase mutants. Moreover, encapsulated, clinical pneumococcal isolates were impaired in their capacity to form biofilms. In addition, a role for extracellular DNA and proteins in the establishment of S. pneumoniae biofilms was demonstrated. Taken together, these observations provide information on conditions that favor the sessile mode of growth by S. pneumoniae . The experimental approach described here should facilitate the study of bacterial genes that are required for biofilm formation. Those results, in turn, may provide insight into strategies to prevent pneumococcal colonization of its human host.
Streptococcus pneumoniae colonizes the human upper respiratory tract, and this asymptomatic colonization is known to precede pneumococcal disease. In this report, chemically defined and semisynthetic media were used to identify the initial steps of biofilm formation by pneumococcus during growth on abiotic surfaces such as polystyrene or glass. Unencapsulated pneumococci adhered to abiotic surfaces and formed a three-dimensional structure about 25 μm deep, as observed by confocal laser scanning microscopy and low-temperature scanning electron microscopy. Choline residues of cell wall teichoic acids were found to play a fundamental role in pneumococcal biofilm development. The role in biofilm formation of choline-binding proteins, which anchor to the teichoic acids of the cell envelope, was determined using unambiguously characterized mutants. The results showed that LytA amidase, LytC lysozyme, LytB glucosaminidase, CbpA adhesin, PcpA putative adhesin, and PspA (pneumococcal surface protein A) mutants had a decreased capacity to form biofilms, whereas no such reduction was observed in Pce phosphocholinesterase or CbpD putative amidase mutants. Moreover, encapsulated, clinical pneumococcal isolates were impaired in their capacity to form biofilms. In addition, a role for extracellular DNA and proteins in the establishment of S. pneumoniae biofilms was demonstrated. Taken together, these observations provide information on conditions that favor the sessile mode of growth by S. pneumoniae . The experimental approach described here should facilitate the study of bacterial genes that are required for biofilm formation. Those results, in turn, may provide insight into strategies to prevent pneumococcal colonization of its human host.
Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue JB About JB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0021-9193 Online ISSN: 1098-5530 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JB .asm.org, visit: JB       
Streptococcus pneumoniae colonizes the human upper respiratory tract, and this asymptomatic colonization is known to precede pneumococcal disease. In this report, chemically defined and semisynthetic media were used to identify the initial steps of biofilm formation by pneumococcus during growth on abiotic surfaces such as polystyrene or glass. Unencapsulated pneumococci adhered to abiotic surfaces and formed a three-dimensional structure about 25 mu m deep, as observed by confocal laser scanning microscopy and low-temperature scanning electron microscopy. Choline residues of cell wall teichoic acids were found to play a fundamental role in pneumococcal biofilm development. The role in biofilm formation of choline-binding proteins, which anchor to the teichoic acids of the cell envelope, was determined using unambiguously characterized mutants. The results showed that LytA amidase, LytC lysozyme, LytB glucosaminidase, CbpA adhesin, PcpA putative adhesin, and PspA (pneumococcal surface protein A) mutants had a decreased capacity to form biofilms, whereas no such reduction was observed in Pce phosphocholinesterase or CbpD putative amidase mutants. Moreover, encapsulated, clinical pneumococcal isolates were impaired in their capacity to form biofilms. In addition, a role for extracellular DNA and proteins in the establishment of S. pneumoniae biofilms was demonstrated. Taken together, these observations provide information on conditions that favor the sessile mode of growth by S. pneumoniae. The experimental approach described here should facilitate the study of bacterial genes that are required for biofilm formation. Those results, in turn, may provide insight into strategies to prevent pneumococcal colonization of its human host.
Author Rubens López
Miriam Moscoso
Ernesto García
AuthorAffiliation Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain
AuthorAffiliation_xml – name: Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain
Author_xml – sequence: 1
  givenname: Miriam
  surname: MOSCOSO
  fullname: MOSCOSO, Miriam
  organization: Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain
– sequence: 2
  givenname: Ernesto
  surname: GARCIA
  fullname: GARCIA, Ernesto
  organization: Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain
– sequence: 3
  givenname: Rubens
  surname: LOPEZ
  fullname: LOPEZ, Rubens
  organization: Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain
BackLink http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=18255131$$DView record in Pascal Francis
https://www.ncbi.nlm.nih.gov/pubmed/16936041$$D View this record in MEDLINE/PubMed
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Keywords Microorganism capsule
Choleretic
Streptococcaceae
Microbiology
Hepatoprotector
Choline
Biofilm
Bacteria
Micrococcales
Polysaccharide
Bacteriology
Streptococcus pneumoniae
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Corresponding author. Mailing address: Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain. Phone: 34 91 837 3112. Fax: 34 91 536 0432. E-mail: e.garcia@cib.csic.es.
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Snippet Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
Streptococcus pneumoniae colonizes the human upper respiratory tract, and this asymptomatic colonization is known to precede pneumococcal disease. In this...
ABSTRACT Streptococcus pneumoniae colonizes the human upper respiratory tract, and this asymptomatic colonization is known to precede pneumococcal disease. In...
Streptococcus pneumoniae colonizes the human upper respiratory tract, and this asymptomatic colonization is known to precede pneumococcal disease. In this...
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StartPage 7785
SubjectTerms Amidohydrolases - genetics
Amidohydrolases - physiology
Antigens, Bacterial - genetics
Antigens, Bacterial - physiology
Bacterial Capsules - physiology
Bacterial Proteins - genetics
Bacterial Proteins - physiology
Bacteriology
Biofilms - growth & development
Biological and medical sciences
Carrier Proteins - genetics
Carrier Proteins - physiology
Choline - metabolism
Choline - physiology
DNA, Bacterial - physiology
Fundamental and applied biological sciences. Psychology
Glass
Humans
Microbial Communities and Interactions
Microbiology
Miscellaneous
Muramidase - genetics
Muramidase - physiology
Mutation
N-Acetylmuramoyl-L-alanine Amidase - genetics
N-Acetylmuramoyl-L-alanine Amidase - physiology
Pneumococcal Infections - microbiology
Polystyrenes
Streptococcus pneumoniae
Streptococcus pneumoniae - physiology
Teichoic Acids - chemistry
Title Biofilm Formation by Streptococcus pneumoniae: Role of Choline, Extracellular DNA, and Capsular Polysaccharide in Microbial Accretion
URI http://jb.asm.org/content/188/22/7785.abstract
https://www.ncbi.nlm.nih.gov/pubmed/16936041
https://search.proquest.com/docview/19965888
https://search.proquest.com/docview/69026590
https://pubmed.ncbi.nlm.nih.gov/PMC1636320
Volume 188
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