This Article Full Text Full Text (PDF) Supplemental material Other Versions of this Article: JB.01292-06v1 189/3/918    most recent 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 Kalscheuer, R. Articles by Steinbüchel, A. Search for Related Content PubMed PubMed Citation Articles by Kalscheuer, R. Articles by Steinbüchel, A.

 Previous Article  |  Next Article 

Journal of Bacteriology, February 2007, p. 918-928, Vol. 189, No. 3
0021-9193/07/$08.00+0     doi:10.1128/JB.01292-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Analysis of Storage Lipid Accumulation in Alcanivorax borkumensis: Evidence for Alternative Triacylglycerol Biosynthesis Routes in Bacteria ^,

Rainer Kalscheuer ,^1,, Tim Stöveken,^1, Ursula Malkus,² Rudolf Reichelt,² Peter N. Golyshin,³ Julia S. Sabirova,³ Manuel Ferrer,⁴ Kenneth N. Timmis,³ and Alexander Steinbüchel^1*

Institut für Molekulare Mikrobiologie und Biotechnologie,¹ Institut für Medizinische Physik und Biophysik, Universitätsklinikum, Westfälische Wilhelms-Universität, Münster, Germany,² Department of Environmental Microbiology, HZI-Helmholtz Centre for Infection Research, Braunschweig, Germany,³ Institute of Catalysis, CSIC, Cantoblanco, Madrid, Spain⁴

Received 15 August 2006/ Accepted 13 November 2006

Marine hydrocarbonoclastic bacteria, like Alcanivorax borkumensis, play a globally important role in bioremediation of petroleum oil contamination in marine ecosystems. Accumulation of storage lipids, serving as endogenous carbon and energy sources during starvation periods, might be a potential adaptation mechanism for coping with nutrient limitation, which is a frequent stress factor challenging those bacteria in their natural marine habitats. Here we report on the analysis of storage lipid biosynthesis in A. borkumensis strain SK2. Triacylglycerols (TAGs) and wax esters (WEs), but not poly(hydroxyalkanoic acids), are the principal storage lipids present in this and other hydrocarbonoclastic bacterial species. Although so far assumed to be a characteristic restricted to gram-positive actinomycetes, substantial accumulation of TAGs corresponding to a fatty acid content of more than 23% of the cellular dry weight is the first characteristic of large-scale de novo TAG biosynthesis in a gram-negative bacterium. The acyltransferase AtfA1 (ABO_2742) exhibiting wax ester synthase/acyl-coenzyme A:diacylglycerol acyltransferase (WS/DGAT) activity plays a key role in both TAG and WE biosynthesis, whereas AtfA2 (ABO_1804) was dispensable for storage lipid formation. However, reduced but still substantial residual TAG levels in atfA1 and atfA2 knockout mutants compellingly indicate the existence of a yet unknown WS/DGAT-independent alternative TAG biosynthesis route. Storage lipids of A. borkumensis were enriched in saturated fatty acids and accumulated as insoluble intracytoplasmic inclusions exhibiting great structural variety. Storage lipid accumulation provided only a slight growth advantage during short-term starvation periods but was not required for maintaining viability and long-term persistence during extended starvation phases.

Published ahead of print on 22 November 2006.

Supplemental material for this article may be found at http://jb.asm.org/.

R.K. and T.S. contributed equally to this work.

Present address: Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY 10461.

This article has been cited by other articles:

• Alvarez, A. F., Alvarez, H. M., Kalscheuer, R., Waltermann, M., Steinbuchel, A. (2008). Cloning and characterization of a gene involved in triacylglycerol biosynthesis and identification of additional homologous genes in the oleaginous bacterium Rhodococcus opacus PD630. Microbiology 154: 2327-2335 [Abstract] [Full Text]  
• Arabolaza, A., Rodriguez, E., Altabe, S., Alvarez, H., Gramajo, H. (2008). Multiple Pathways for Triacylglycerol Biosynthesis in Streptomyces coelicolor. Appl. Environ. Microbiol. 74: 2573-2582 [Abstract] [Full Text]  
• Holtzapple, E., Schmidt-Dannert, C. (2007). Biosynthesis of Isoprenoid Wax Ester in Marinobacter hydrocarbonoclasticus DSM 8798: Identification and Characterization of Isoprenoid Coenzyme A Synthetase and Wax Ester Synthases. J. Bacteriol. 189: 3804-3812 [Abstract] [Full Text]