Utilization of DNA as a Sole Source of Phosphorus, Carbon, and Energy by Shewanella spp.: Ecological and Physiological Implications for Dissimilatory Metal Reduction
- 15 February 2008
- journal article
- research article
- Published by American Society for Microbiology in Applied and Environmental Microbiology
- Vol. 74 (4), 1198-1208
- https://doi.org/10.1128/aem.02026-07
Abstract
The solubility of orthophosphate (PO 4 3− ) 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 Ca 2+ -independent DNA utilization, both CN32 and MR-1 required millimolar concentrations of Ca 2+ 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 Ca 2+ -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.Keywords
This publication has 49 references indexed in Scilit:
- Diversity and Metabolism of Marine Bacteria Cultivated on Dissolved DNAApplied and Environmental Microbiology, 2007
- Phosphate Starvation-Inducible Gene ushA Encodes a 5′ Nucleotidase Required for Growth of Corynebacterium glutamicum on Media with Nucleotides as the Phosphorus SourceApplied and Environmental Microbiology, 2005
- The SphS-SphR Two Component System Is the Exclusive Sensor for the Induction of Gene Expression in Response to Phosphate Limitation in SynechocystisOnline Journal of Public Health Informatics, 2004
- Is phosphorus limitation of planktonic heterotrophic bacteria and accumulation of degradable DOC a normal phenomenon in phosphorus-limited systems? A microcosm studyFEMS Microbiology Ecology, 2003
- The Phosphate Starvation Stimulon ofCorynebacterium glutamicumDetermined by DNA Microarray AnalysesJournal of Bacteriology, 2003
- Extracellular DNA Required for Bacterial Biofilm FormationScience, 2002
- Determination of dissolved deoxyribonucleic acid concentration in lake waterAquatic Microbial Ecology, 1996
- An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein databaseJournal of the American Society for Mass Spectrometry, 1994
- Biochemical and immunological characterization of the extracellular nucleases of group B streptococci.The Journal of Experimental Medicine, 1980
- Extracellular nuclease produced by a marine bacterium. II. Purification and properties of extracellular nuclease from a marine Vibrio sp.Canadian Journal of Microbiology, 1976