Salmonella biofilm formation on Aspergillus niger involves cellulose - chitin interactions

Authors: Brandl, Maria; Carter, Michelle; Parker, Craig; CHAPMAN, MATTHEW - University Of Michigan; Huynh, Steven; Zhou, Yaguang

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/6/2011
Publication Date: 9/23/2011
Citation: Brandl, M., Carter, M.Q., Parker, C., Chapman, M.R., Huynh, S., Zhou, Y. 2011. Salmonella biofilm formation on Aspergillus niger involves cellulose - chitin interactions. PloS ONE 6(10):e25553.

Interpretive Summary: The human enteric pathogen Salmonella enterica cycles between host and nonhost environments, where it may become an active member of complex microbial communities. We report here the rapid attachment and biofilm formation by S. enterica Typhimurium on Aspergillus niger, a common microbial inhabitant of agricultural crops and soil. Several serovars of S. enterica engaged in a similar association with A. niger whereas other bacterial species were unable to bind to the fungus, suggesting a certain level of specificity in this interaction. Bacterial attachment to chitin beads followed the same specificity. N-acetylglucosamine, a major component of chitin and therefore, of fungal cell walls, inhibited S. enterica attachment to chitin beads and to A. niger hyphae, indicating a role for chitin in the binding of the pathogen to the fungus. A cellulose-deficient mutant of S. Typhimurium did not bind to chitin beads nor to the fungus. Complementation of the mutant with the cellulose operon restored binding to both, as well as the ability to form biofilms, providing evidence that cellulose is involved in the attachment of the pathogen to A. niger via the chitin component of its cell wall. Time course studies with curli-deficient mutants showed that the fimbriae contributed primarily to the long-term stability of the biofilm structure. Our results suggest that cellulose–chitin interactions are required for the production of mixed Salmonella-A. niger biofilms, and support the hypothesis that encounters with chitinaceous alternate hosts may contribute to the ecological success of human pathogens.

Technical Abstract: Salmonella cycles between host and nonhost environments, where it can become an active member of complex microbial communities. The role of fungi in the environmental adaptation of enteric pathogens remains relatively unexplored. We have discovered that S. enterica Typhimurium rapidly attaches to and forms biofilms on the hyphae of the common fungus, Aspergillus niger. Several Salmonella enterica serovars displayed a similar interaction, whereas other bacterial species were unable to bind to the fungus. Bacterial attachment to chitin, a major constituent of fungal cell walls, mirrored this specificity. Pre-incubation of S. Typhimurium with N-acetylglucosamine, the monomeric component of chitin, reduced binding to chitin beads by as much as 727-fold, and inhibited attachment to A. niger hyphae considerably. A cellulose-deficient mutant of S. Typhimurium failed to attach to chitin beads and to the fungus. Complementation of this mutant with the cellulose operon restored binding to chitin beads to 79% of that of the parental strain and allowed for attachment and biofilm formation on A. niger, indicating that cellulose is involved in bacterial attachment to the fungus via the chitin component of its cell wall. In contrast to cellulose, S. Typhimurium curli fimbriae were not required for attachment and biofilm development on the hyphae but were critical for its stability. Our results suggest that cellulose–chitin interactions are required for the production of mixed Salmonella-A. niger biofilms, and support the hypothesis that encounters with chitinaceous alternate hosts may contribute to the ecological success of human pathogens.