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Infection and Immunity, July 2008, p. 2966-2977, Vol. 76, No. 7
0019-9567/08/$08.00+0     doi:10.1128/IAI.00323-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Serendipitous Discovery of an Immunoglobulin-Binding Autotransporter in Bordetella Species

Corinne L. Williams, Robert Haines, and Peggy A. Cotter^*

Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, California 93106-9610

Received 11 March 2008/ Returned for modification 10 April 2008/ Accepted 15 April 2008

We describe the serendipitous discovery of BatB, a classical-type Bordetella autotransporter (AT) protein with an 180-kDa passenger domain that remains noncovalently associated with the outer membrane. Like genes encoding all characterized protein virulence factors in Bordetella species, batB transcription is positively regulated by the master virulence regulatory system BvgAS. BatB is predicted to share similarity with immunoglobulin A (IgA) proteases, and we showed that BatB binds Ig in vitro. In vivo, a Bordetella bronchiseptica batB mutant was unable to overcome innate immune defenses and was cleared from the lower respiratory tracts of mice more rapidly than wild-type B. bronchiseptica. This defect was abrogated in SCID mice, suggesting that BatB functions to resist clearance during the first week postinoculation in a manner dependent on B- and T-cell-mediated activities. Taken together with the previous demonstration that polymorphonuclear neutrophils (PMN) are critical for the control of B. bronchiseptica in mice, our data support the hypothesis that BatB prevents nonspecific antibodies from facilitating PMN-mediated clearance during the first few days postinoculation. Neither of the strictly human-adapted Bordetella subspecies produces a fully functional BatB protein; nucleotide differences within the putative promoter region prevent batB transcription in Bordetella pertussis, and although expressed, the batB gene of human-derived Bordetella parapertussis (B. parapertussis_hu) contains a large in-frame deletion relative to batB of B. bronchiseptica. Taken together, our data suggest that BatB played an important role in the evolution of virulence and host specificity among the mammalian-adapted bordetellae.

Published ahead of print on 21 April 2008.

Editor: A. J. Bäumler

Present address: Department of Biological Sciences, Ventura College, 4667 Telegraph Rd., Ventura, CA 93003.