Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: March 25, 2011
Publication Date: April 8, 2011
Repository URL: http://doi:10.1128/AEM.02315-10
Citation: Carter, M.Q., Brandl, M., Louie, J.W., Kyle, J.L., Carychao, D.K., Cooley, M.B., Parker, C., Bates, A.H., Mandrell, R.E. 2011. Curli variants of enterohemorrhagic Escherichia coli O157:H7 display distinct survival fitness. Applied and Environmental Microbiology. 77:3685-3695. Interpretive Summary: Curli is a bacterial appendage produced by many enteric bacteria and it enhances the initial attachment of bacteria to a solid surface and subsequently, the formation of biofilm. Curli is also an important virulence factor as they mediate host cell invasion, and are potent inducers of the host inflammatory response. E. coli O157:H7 (EcO157) is the most common enterohemorrhagic E. coli serotype and contributes significantly to human infections and outbreaks in the US, and is a major public health concern. In this study, we examined the ecological significance of maintaining curli variants in the EcO157 population. We observed both inter- and intra-strain variations in curli production in EcO157. Moreover, we found that curli variants derived from the same strain display distinct survival fitness: curli-producing (C+) variants grow better in nutrients-limited conditions than curli deficient variants (C-) whereas C- variants are much more acid resistant than C+ variants. C+ variants are stronger biofilm producers in general; however, this characteristic is strain-specific and depends on growth conditions. Environmental factors promoting the switch between C+ and C- variants appear strain specific too. For variants derived from strains associated with 2006 US spinach-outbreak, switch is unidirectional, from C- to C+, and enhanced significantly in the aged culture; for variants derived from strains associated with a 1993 hamburger-outbreak, the switch is bidirectional, and enhanced greatly by oxygen depletion. Curli production appears to be a phase variable phenotype in EcO157, thus providing the entire EcO157 population a survival strategy by helping the pathogen to adapt rapidly to diverse habitats.
Technical Abstract: Curli are adhesive fimbriae of Enterobactericaeae and are involved in surface attachment, cell aggregation and biofilm formation. They also mediate host cell invasion and are potent inducers of the host inflammatory response. Here we report that curli variants are distributed widely in Enterohemorrhagic Escherichia coli O157:H7 (EcO157) strains. Curli variants derived from the same strain display distinct survival fitness: curli-producing (C+) variants grow much better in nutrient-limited conditions than curli deficient variants (C-) whereas C- variants are much more acid resistant than C+ variants. C+ variants are stronger biofilm producers in general; however, this characteristic is strain-specific and depends on growth conditions. Curli production appears a phase variable phenotype in EcO157. Investigation of environmental factors that trigger this phase switch reveals that, for variants derived from 2006 US spinach-outbreak strains, switch responds to starvation mostly, and is unidirectional, from C- to C+; for variants derived from 1993 hamburger-outbreak strains, switch responds to oxygen tension mostly, and is bidirectional. Identical DNA sequences for curli genes csgA, csgB, csgD and the putative promoters of the two curli operons were observed for all 24 EcO157 curli variants, however, frame-shift mutation were detected in the rpoS genes of 8 C+ variants derived from the 2006 US spinach-outbreak strains. Our data suggest that maintaining curli variants in an EcO157 population provides a survival strategy in which C+ variants are selected in a nutrients-limited environment whereas C- variants are selected in an acidic environment such as the stomach of an animal host including human.