Capsular Polysaccharide Interferes with Biofilm Formation by Pasteurella multocida Serogroup A

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dc.contributor.authorPetruzzi, Brianaen
dc.contributor.authorBriggs, Robert E.en
dc.contributor.authorSwords, W. Edwarden
dc.contributor.authorDe Castro, Cristinaen
dc.contributor.authorMolinaro, Antonioen
dc.contributor.authorInzana, Thomas J.en
dc.date.accessioned2019-05-09T16:27:38Zen
dc.date.available2019-05-09T16:27:38Zen
dc.date.issued2017-11en
dc.description.abstractPasteurella 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.en
dc.description.notesThis work was supported by grant 2013-67015-21314 from the U.S. Department of Agriculture-National Institute of Food and Agriculture to T.J.I. and funds from the Virginia-Maryland College of Veterinary Medicine.en
dc.description.sponsorshipU.S. Department of Agriculture-National Institute of Food and Agriculture [2013-67015-21314]en
dc.description.sponsorshipVirginia-Maryland College of Veterinary Medicineen
dc.format.mimetypeapplication/pdfen
dc.identifier.citationPetruzzi B, Briggs RE, Swords WE, De Castro C, Molinaro A, Inzana TJ. 2017. Capsular polysaccharide interferes with biofilm formation by Pasteurella multocida serogroup A. mBio 8:e01843-17. https://doi.org/10.1128/mBio.01843-17.en
dc.identifier.doihttps://doi.org/10.1128/mBio.01843-17en
dc.identifier.issn2150-7511en
dc.identifier.issue6en
dc.identifier.othere01843-17en
dc.identifier.urihttp://hdl.handle.net/10919/89435en
dc.identifier.volume8en
dc.language.isoenen
dc.publisherAmerican Society for Microbiologyen
dc.rightsCreative Commons Attribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleCapsular Polysaccharide Interferes with Biofilm Formation by Pasteurella multocida Serogroup Aen
dc.title.serialmBioen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten

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