The Bps polysaccharide of Bordetella pertussis promotes colonization and biofilm formation in the nose by functioning as an adhesin

Abstract

SummaryMany respiratory pathogens establish persistent infection or a carrier state in the human nasopharynx without overt disease symptoms but the presence of these in the lungs usually results in disease. Although the anatomy and microenvironments between nasopharynx and lungs are different, a virulence factor with an organ-specific function in the colonization of the nasopharynx is unknown. In contrast to the severity of pertussis and mortality in non-vaccinated young children, Bordetella pertussis results in milder and prolonged cough in vaccinated adolescents and adults. Individuals harbouring bacteria in the nasopharynx serve as reservoirs for intrafamilial and nosocomial transmission. We show that the Bps polysaccharide of B. pertussis is critical for initial colonization of the mouse nose and the trachea but not of the lungs. Our data reveal a biofilm lifestyle for B. pertussis in the nose and the requirement of Bps in this developmental process. Bps functions as an adhesin by promoting adherence of B. pertussis and Escherichia coli to human nasal but not to human lung epithelia. Patient serum specifically recognized Bps suggesting its expression during natural human infections. We describe the first bacterial factor that exhibits a differential role in colonization and adherence between the nasopharynx and the lungs.

BpsR Modulates Bordetella Biofilm Formation by Negatively Regulating the Expression of the Bps Polysaccharide

“…We have shown that both B. bronchiseptica and B. pertussis are capable of forming biofilms in the upper respiratory tract of infected animals (13,14,53). These findings, combined with the presence of clusters, microcolonies, and tangles of B. bronchiseptica and B. pertussis bacteria in explant tissues and nasal biopsy specimens of patients, strengthen the hypothesis that Bordetella bacteria utilize biofilms as a means to persist and circulate between their mammalian hosts (22,47,54).…”

“…We have previously shown that bpsA-D is not required for the early steps of biofilm formation, in particular, the initial attachment to abiotic surfaces (14,48). Instead, Bps is required at a step postattachment and contributes to the formation of the complex architecture of Bordetella biofilms (14,48).…”

“…Previously, we have demonstrated that the Bps polysaccharide is a biofilm matrix component and is essential for in vitro and in vivo biofilm development in B. bronchiseptica and B. pertussis (14,53). Moreover, Bps is necessary for persistent respiratory tract colonization of B. bronchiseptica and for efficient early colonization of the nose and the trachea for B. pertussis (14,53). Thus, while Bps is clearly emerging as an important Bordetella virulence factor, the mechanisms by which its expression is regulated in Bordetella are not known.…”

The Structure- and Metal-dependent Activity of Escherichia coli PgaB Provides Insight into the Partial De-N-acetylation of Poly-β-1,6-N-acetyl-d-glucosamine

“…A wide variety of medically important biofilm-forming bacteria produce partially de-N-acetylated poly-␤-1,6-N-acetyl-D-glucosamine (dPNAG) 5 exopolysaccharides, also referred to as polysaccharide intercellular adhesin. dPNAG was first described in Staphylococcus epidermidis (8) but has now been determined to be a component of the biofilm matrices of Staphylococcus aureus (9), Escherichia coli (10), Acinetobacter baumannii (11), Bordetella bronchiseptica (12), Bordetella pertussis (13), Actinobacillus pleuropneumoniae (14), Yersinia pestis (15), and Burkholderia species (16).…”

Translational Repression of NhaR, a Novel Pathway for Multi-Tier Regulation of Biofilm Circuitry by CsrA

“…Poly-␤-1,6-N-acetyl-D-glucosamine, variously referred to as PGA, PNAG, PIA, or Bps, is a secreted polymer that mediates cell-cell and cell-abiotic-surface interactions that stabilize biofilms of diverse bacterial species (1,10,16,23,31,34,48,49,62). This polysaccharide also promotes adherence to plant surfaces (41) and colonization of the mammalian respiratory tract (17) and is expressed by pathogenic Escherichia coli during mammalian infections (13). Genes of the E. coli pgaABCD operon are required for polymerization (pgaC, pgaD), partial N-deacetylation (pgaB), and secretion (pgaA, pgaB) of PGA (32).…”