This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hasona, A. Articles by Shanmugam, K. T. Search for Related Content PubMed PubMed Citation Articles by Hasona, A. Articles by Shanmugam, K. T.

 Previous Article  |  Next Article 

Journal of Bacteriology, November 2004, p. 7593-7600, Vol. 186, No. 22
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.22.7593-7600.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Pyruvate Formate Lyase and Acetate Kinase Are Essential for Anaerobic Growth of Escherichia coli on Xylose

Adnan Hasona, Youngnyun Kim, F. G. Healy, L. O. Ingram, and K. T. Shanmugam^*

Department of Microbiology and Cell Science, University of Florida, Gainesville, Florida 32611

Received 21 May 2004/ Accepted 16 August 2004

During anaerobic growth of bacteria, organic intermediates of metabolism, such as pyruvate or its derivatives, serve as electron acceptors to maintain the overall redox balance. Under these conditions, the ATP needed for cell growth is derived from substrate-level phosphorylation. In Escherichia coli, conversion of glucose to pyruvate yields 2 net ATPs, while metabolism of a pentose, such as xylose, to pyruvate only yields 0.67 net ATP per xylose due to the need for one (each) ATP for xylose transport and xylulose phosphorylation. During fermentative growth, E. coli produces equimolar amounts of acetate and ethanol from two pyruvates, and these reactions generate one additional ATP from two pyruvates (one hexose equivalent) while still maintaining the overall redox balance. Conversion of xylose to acetate and ethanol increases the net ATP yield from 0.67 to 1.5 per xylose. An E. coli pfl mutant lacking pyruvate formate lyase cannot convert pyruvate to acetyl coenzyme A, the required precursor for acetate and ethanol production, and could not produce this additional ATP. E. coli pfl mutants failed to grow under anaerobic conditions in xylose minimal medium without any negative effect on their survival or aerobic growth. An ackA mutant, lacking the ability to generate ATP from acetyl phosphate, also failed to grow in xylose minimal medium under anaerobic conditions, confirming the need for the ATP produced by acetate kinase for anaerobic growth on xylose. Since arabinose transport by AraE, the low-affinity, high-capacity, arabinose/H⁺ symport, conserves the ATP expended in pentose transport by the ABC transporter, both pfl and ackA mutants grew anaerobically with arabinose. AraE-based xylose transport, achieved after constitutively expressing araE, also supported the growth of the pfl mutant in xylose minimal medium. These results suggest that a net ATP yield of 0.67 per pentose is only enough to provide for maintenance energy but not enough to support growth of E. coli in minimal medium. Thus, pyruvate formate lyase and acetate kinase are essential for anaerobic growth of E. coli on xylose due to energetic constraints.

Florida Agricultural Experiment Station Journal Series no. R-10339.

Present address: Department of Oral Biology, University of Florida, Gainesville, FL 32610.

Present address: Department of Biology, Trinity University, San Antonio, TX 78212.

This article has been cited by other articles:

• Murarka, A., Dharmadi, Y., Yazdani, S. S., Gonzalez, R. (2008). Fermentative Utilization of Glycerol by Escherichia coli and Its Implications for the Production of Fuels and Chemicals. Appl. Environ. Microbiol. 74: 1124-1135 [Abstract] [Full Text]  
• Kim, Y., Ingram, L. O., Shanmugam, K. T. (2007). Construction of an Escherichia coli K-12 Mutant for Homoethanologenic Fermentation of Glucose or Xylose without Foreign Genes. Appl. Environ. Microbiol. 73: 1766-1771 [Abstract] [Full Text]