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Applied and Environmental Microbiology, February 2008, p. 1198-1208, Vol. 74, No. 4
0099-2240/08/$08.00+0     doi:10.1128/AEM.02026-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Utilization of DNA as a Sole Source of Phosphorus, Carbon, and Energy by Shewanella spp.: Ecological and Physiological Implications for Dissimilatory Metal Reduction{triangledown}

Grigoriy E. Pinchuk,1 Christine Ammons,2 David E. Culley,1 Shu-Mei W. Li,1 Jeff S. McLean,1 Margaret F. Romine,1 Kenneth H. Nealson,2 Jim K. Fredrickson,1 and Alexander S. Beliaev1*

Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99352,1 Department of Earth Sciences, University of South California, Los Angeles, California 900892

Received 4 September 2007/ Accepted 13 December 2007

The solubility of orthophosphate (PO43–) in iron-rich sediments can be exceedingly low, limiting the bioavailability of this essential nutrient to microbial populations that catalyze critical biogeochemical reactions. Here we demonstrate that dissolved extracellular DNA can serve as a sole source of phosphorus, as well as carbon and energy, for metal-reducing bacteria of the genus Shewanella. Shewanella oneidensis MR-1, Shewanella putrefaciens CN32, and Shewanella sp. strain W3-18-1 all grew with DNA but displayed different growth rates. W3-18-1 exhibited the highest growth rate with DNA. While strain W3-18-1 displayed Ca2+-independent DNA utilization, both CN32 and MR-1 required millimolar concentrations of Ca2+ for growth with DNA. For S. oneidensis MR-1, the utilization of DNA as a sole source of phosphorus is linked to the activities of extracellular phosphatase(s) and a Ca2+-dependent nuclease(s), which are regulated by phosphorus availability. Mass spectrometry analysis of the extracellular proteome of MR-1 identified one putative endonuclease (SO1844), a predicted UshA (bifunctional UDP-sugar hydrolase/5' nucleotidase), a predicted PhoX (calcium-activated alkaline phosphatase), and a predicted CpdB (bifunctional 2',3' cyclic nucleotide 2' phosphodiesterase/3' nucleotidase), all of which could play important roles in the extracellular degradation of DNA under phosphorus-limiting conditions. Overall, the results of this study suggest that the ability to use exogenous DNA as the sole source of phosphorus is widespread among the shewanellae, and perhaps among all prokaryotes, and may be especially important for nutrient cycling in metal-reducing environments.

* Corresponding author. Mailing address: Biological Sciences Division, Pacific Northwest National Laboratory, P.O. Box 999, MS: P7-54, Richland, WA 99352. Phone: (509) 376-4183. Fax: (509) 376-4909. E-mail: alex.beliaev{at}pnl.gov

{triangledown} Published ahead of print on 21 December 2007.

Applied and Environmental Microbiology, February 2008, p. 1198-1208, Vol. 74, No. 4
0099-2240/08/$08.00+0     doi:10.1128/AEM.02026-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Pinchuk, G. E., Rodionov, D. A., Yang, C., Li, X., Osterman, A. L., Dervyn, E., Geydebrekht, O. V., Reed, S. B., Romine, M. F., Collart, F. R., Scott, J. H., Fredrickson, J. K., Beliaev, A. S. (2009). Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization. Proc. Natl. Acad. Sci. USA 106: 2874-2879 [Abstract] [Full Text]  


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