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Journal of Bacteriology, December 2004, p. 8164-8171, Vol. 186, No. 24
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.24.8164-8171.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Pyruvate Oxidase Is a Determinant of Avery's Rough Morphology

Aimee E. Belanger,* Melissa J. Clague, John I. Glass,{dagger} and Donald J. LeBlanc{ddagger}

Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana

Received 13 July 2004/ Accepted 10 September 2004

In pioneering studies, Avery et al. identified DNA as the hereditary material (A. T. Avery, C. M. MacLeod, and M. McCarty, J. Exp. Med. 79:137-158, 1944). They demonstrated, by means of variation in colony morphology, that this substance could transform their rough type 2 Streptococcus pneumoniae strain R36A into a smooth type 3 strain. It has become accepted as fact, from modern textbook accounts of these experiments, that smooth pneumococci make capsule, while rough strains do not. We found that rough-to-smooth morphology conversion did not occur in rough strains R36A and R6 when the ability to synthesize native type 2 capsule was restored. The continued rough morphology of these encapsulated strains was attributed to a second, since-forgotten, morphology-affecting mutation that was sustained by R36A during strain development. We used a new genome-PCR-based approach to identify spxB, the gene encoding pyruvate oxidase, as the mutated locus in R36A and R6 that, with unencapsulation, gives rise to rough colony morphology, as we know it. The variant spxB allele of R36A and R6 is associated with increased cellular pyruvate oxidase activity relative to the ancestral strain D39. Increased pyruvate oxidase activity alters colony shape by mediating cell death. R36A requires a wild-type spxB allele for the expression of smooth type 2 morphology but not for the expression of smooth type 3 morphology, the phenotype monitored by Avery et al. Thus, the mutated spxB allele did not impact their use of smooth morphology to identify the transforming principle.

* Corresponding author. Mailing address: Elanco Animal Health, Eli Lilly and Company, 2001 West Main St., Drop Code 21, Greenfield, IN 46140. Phone: (317) 277-1622. Fax: (317) 277-4755. E-mail: belangerae{at}lilly.com.

{dagger} Present address: Institute for Biological Energy Alternatives, Rockville, MD 20850.

{ddagger} Present address: Antibacterial Molecular Sciences, Pfizer Global Research and Development, Ann Arbor, MI 48105.

Journal of Bacteriology, December 2004, p. 8164-8171, Vol. 186, No. 24
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.24.8164-8171.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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  • Lanie, J. A., Ng, W.-L., Kazmierczak, K. M., Andrzejewski, T. M., Davidsen, T. M., Wayne, K. J., Tettelin, H., Glass, J. I., Winkler, M. E. (2007). Genome Sequence of Avery's Virulent Serotype 2 Strain D39 of Streptococcus pneumoniae and Comparison with That of Unencapsulated Laboratory Strain R6. J. Bacteriol. 189: 38-51 [Abstract] [Full Text]  


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