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Infection and Immunity, July 1999, p. 3181-3187, Vol. 67, No. 7
0019-9567/99/$04.00+0

Effects of Environmental pH on Membrane Proteins in Borrelia burgdorferi

James A. Carroll,1,* Claude F. Garon,1 and Tom G. Schwan2

Rocky Mountain Laboratories Microscopy Branch1 and Laboratory of Microbial Structure and Function,2 Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, Hamilton, Montana 59840

Received 5 January 1999/Returned for modification 18 February 1999/Accepted 6 April 1999

Borrelia burgdorferi, the causative agent of Lyme disease, alternates between the microenvironments of the tick vector, Ixodes scapularis, and a mammalian host. The environmental conditions the spirochete encounters during its infectious cycle are suspected to differ greatly in many aspects, including available nutrients, temperature, and pH. Here we identify alterations in the membrane protein profile, as determined by immunoblotting and two-dimensional nonequilibrium pH gradient gel electrophoresis (2D-NEPHGE), that occur in virulent B. burgdorferi B31 as the pH of the medium is altered. Initial comparisons of cultures incubated at pHs 6.0, 7.0, and 8.0 yielded alterations in the expression of seven membrane proteins as determined by probing with hyperimmune rabbit serum. Six of these membrane proteins (54, 45, 44, 43, 35, and 24 kDa) were either present in increased amounts in or solely expressed by cultures incubated at pHs 6.0 and 7.0. The 24-kDa protein that decreased in expression at pH 8.0 was identified as outer surface protein C (OspC). In addition, a 42-kDa membrane protein increased in amount in cultures incubated at pH 8.0. Similar changes were observed with serum from a mouse infected by tick bite, with the recognition of two additional bands (48 and 46 kDa) unique to pHs 6.0 and 7.0. When membrane fractions were analyzed by 2D-NEPHGE, at least 37 changes in the membrane protein profile between cells incubated at pHs 6.0, 7.0, and 8.0 were observed by immunoblotting and silver staining. Environmental cues such as pH may prove important in the regulation of virulence determinants and factors necessary for the adaptation of B. burgdorferi to the tick or mammalian microcosm.


* Corresponding author. Mailing address: 903 South 4th St., Hamilton, MT 59840. Phone: (406) 363-9407. Fax: (406) 363-9371. E-mail: jcarroll{at}atlas.niaid.nih.gov.


Infection and Immunity, July 1999, p. 3181-3187, Vol. 67, No. 7
0019-9567/99/$04.00+0



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  • Babb, K., El-Hage, N., Miller, J. C., Carroll, J. A., Stevenson, B. (2001). Distinct Regulatory Pathways Control Expression of Borrelia burgdorferi Infection-Associated OspC and Erp Surface Proteins. Infect. Immun. 69: 4146-4153 [Abstract] [Full Text]  
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  • Ramamoorthy, R., Scholl-Meeker, D. (2001). Borrelia burgdorferi Proteins Whose Expression Is Similarly Affected by Culture Temperature and pH. Infect. Immun. 69: 2739-2742 [Abstract] [Full Text]  
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  • Haake, D. A. (2000). Spirochaetal lipoproteins and pathogenesis. Microbiology 146: 1491-1504 [Full Text]  
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