Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A

ABSTRACT Pasteurella multocida is an important multihost animal and zoonotic pathogen that is capable of causing respiratory and multisystemic diseases, bacteremia, and bite wound infections. The glycosaminoglycan capsule of P. multocida is an essential virulence factor that protects the bacterium f...

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Autores principales:	Briana Petruzzi, Robert E. Briggs, W. Edward Swords, Cristina De Castro, Antonio Molinaro, Thomas J. Inzana
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Pasteurella multocida biofilms capsule chronic infection exopolysaccharide Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8c1b1203097042d2b07b14dc92d5b10e
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spelling	oai:doaj.org-article:8c1b1203097042d2b07b14dc92d5b10e2021-11-15T15:51:55ZCapsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A10.1128/mBio.01843-172150-7511https://doaj.org/article/8c1b1203097042d2b07b14dc92d5b10e2017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01843-17https://doaj.org/toc/2150-7511ABSTRACT Pasteurella multocida is an important multihost animal and zoonotic pathogen that is capable of causing respiratory and multisystemic diseases, bacteremia, and bite wound infections. The glycosaminoglycan capsule of P. multocida is an essential virulence factor that protects the bacterium from host defenses. However, chronic infections (such as swine atrophic rhinitis and the carrier state in birds and other animals) may be associated with biofilm formation, which has not been characterized in P. multocida. Biofilm formation by clinical isolates was inversely related to capsule production and was confirmed with capsule-deficient mutants of highly encapsulated strains. Capsule-deficient mutants formed biofilms with a larger biomass that was thicker and smoother than the biofilm of encapsulated strains. Passage of a highly encapsulated, poor-biofilm-forming strain under conditions that favored biofilm formation resulted in the production of less capsular polysaccharide and a more robust biofilm, as did addition of hyaluronidase to the growth medium of all of the strains tested. The matrix material of the biofilm was composed predominately of a glycogen exopolysaccharide (EPS), as determined by gas chromatography-mass spectrometry, nuclear magnetic resonance, and enzymatic digestion. However, a putative glycogen synthesis locus was not differentially regulated when the bacteria were grown as a biofilm or planktonically, as determined by quantitative reverse transcriptase PCR. Therefore, the negatively charged capsule may interfere with biofilm formation by blocking adherence to a surface or by preventing the EPS matrix from encasing large numbers of bacterial cells. This is the first detailed description of biofilm formation and a glycogen EPS by P. multocida. IMPORTANCE Pasteurella multocida is an important pathogen responsible for severe infections in food animals, domestic and wild birds, pet animals, and humans. P. multocida was first isolated by Louis Pasteur in 1880 and has been studied for over 130 years. However, aspects of its lifecycle have remained unknown. Although formation of a biofilm by P. multocida has been proposed, this report is the first to characterize biofilm formation by P. multocida. Of particular interest is that the biofilm matrix material contained a newly reported amylose-like glycogen as the exopolysaccharide component and that production of capsular polysaccharide (CPS) was inversely related to biofilm formation. However, even highly mucoid, poor-biofilm-forming strains could form abundant biofilms by loss of CPS or following in vitro passage under biofilm growth conditions. Therefore, the carrier state or subclinical chronic infections with P. multocida may result from CPS downregulation with concomitant enhanced biofilm formation.Briana PetruzziRobert E. BriggsW. Edward SwordsCristina De CastroAntonio MolinaroThomas J. InzanaAmerican Society for MicrobiologyarticlePasteurella multocidabiofilmscapsulechronic infectionexopolysaccharideMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pasteurella multocida biofilms capsule chronic infection exopolysaccharide Microbiology QR1-502
spellingShingle	Pasteurella multocida biofilms capsule chronic infection exopolysaccharide Microbiology QR1-502 Briana Petruzzi Robert E. Briggs W. Edward Swords Cristina De Castro Antonio Molinaro Thomas J. Inzana Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A
description	ABSTRACT Pasteurella multocida is an important multihost animal and zoonotic pathogen that is capable of causing respiratory and multisystemic diseases, bacteremia, and bite wound infections. The glycosaminoglycan capsule of P. multocida is an essential virulence factor that protects the bacterium from host defenses. However, chronic infections (such as swine atrophic rhinitis and the carrier state in birds and other animals) may be associated with biofilm formation, which has not been characterized in P. multocida. Biofilm formation by clinical isolates was inversely related to capsule production and was confirmed with capsule-deficient mutants of highly encapsulated strains. Capsule-deficient mutants formed biofilms with a larger biomass that was thicker and smoother than the biofilm of encapsulated strains. Passage of a highly encapsulated, poor-biofilm-forming strain under conditions that favored biofilm formation resulted in the production of less capsular polysaccharide and a more robust biofilm, as did addition of hyaluronidase to the growth medium of all of the strains tested. The matrix material of the biofilm was composed predominately of a glycogen exopolysaccharide (EPS), as determined by gas chromatography-mass spectrometry, nuclear magnetic resonance, and enzymatic digestion. However, a putative glycogen synthesis locus was not differentially regulated when the bacteria were grown as a biofilm or planktonically, as determined by quantitative reverse transcriptase PCR. Therefore, the negatively charged capsule may interfere with biofilm formation by blocking adherence to a surface or by preventing the EPS matrix from encasing large numbers of bacterial cells. This is the first detailed description of biofilm formation and a glycogen EPS by P. multocida. IMPORTANCE Pasteurella multocida is an important pathogen responsible for severe infections in food animals, domestic and wild birds, pet animals, and humans. P. multocida was first isolated by Louis Pasteur in 1880 and has been studied for over 130 years. However, aspects of its lifecycle have remained unknown. Although formation of a biofilm by P. multocida has been proposed, this report is the first to characterize biofilm formation by P. multocida. Of particular interest is that the biofilm matrix material contained a newly reported amylose-like glycogen as the exopolysaccharide component and that production of capsular polysaccharide (CPS) was inversely related to biofilm formation. However, even highly mucoid, poor-biofilm-forming strains could form abundant biofilms by loss of CPS or following in vitro passage under biofilm growth conditions. Therefore, the carrier state or subclinical chronic infections with P. multocida may result from CPS downregulation with concomitant enhanced biofilm formation.
format	article
author	Briana Petruzzi Robert E. Briggs W. Edward Swords Cristina De Castro Antonio Molinaro Thomas J. Inzana
author_facet	Briana Petruzzi Robert E. Briggs W. Edward Swords Cristina De Castro Antonio Molinaro Thomas J. Inzana
author_sort	Briana Petruzzi
title	Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A
title_short	Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A
title_full	Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A
title_fullStr	Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A
title_full_unstemmed	Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A
title_sort	capsular polysaccharide interferes with biofilm formation by <italic toggle="yes">pasteurella multocida</italic> serogroup a
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/8c1b1203097042d2b07b14dc92d5b10e
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Capsular Polysaccharide Interferes with Biofilm Formation by <italic toggle="yes">Pasteurella multocida</italic> Serogroup A

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