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Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores

Abstract

Nitrogen fixation, the reaction that transforms atmospheric nitrogen into bioavailable ammonia and is responsible for the supply of nitrogen to Earth’s ecosystems, is mediated by the enzyme nitrogenase. This reaction requires molybdenum (Mo) or vanadium (V) in addition to iron (Fe) (refs 1, 2). Therefore, the availability of these trace metals may control the Earth’s nitrogen cycle3,4. Many bacteria release strong iron-binding compounds (siderophores) for iron acquisition5,6, but the effect of these compounds on Mo and V availability to nitrogen-fixing organisms is not well understood. Here, we show that the siderophores produced in cultures of Azotobacter vinelandii while fixing atmospheric nitrogen under limitation by Mo or V form strong complexes with molybdate and vanadate, and that these complexes are available for uptake. We also show that addition of these siderophores rapidly reverses the effect of other natural binding compounds that make Mo and V unavailable for uptake. Our results resolve the long-standing debate regarding the existence of bacterial ‘molybdophores’7,8,9, as well as the corollary question regarding ‘vanadophores’. We conclude that the production of strong binding compounds may be a widespread strategy for metal acquisition by bacteria, implying that the availability of Mo and V may be critical for the nitrogen cycle of terrestrial ecosystems.

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Figure 1: Effect of Mo, Fe and V on the growth and production of catechol siderophores by A. vinelandii under diazotrophic conditions.
Figure 2: Complexation of Mo, V and Fe by catechol siderophores in cultures of A. vinelandii (strain OP).
Figure 3: Short-term uptake of the Mo and V complexes with protochelin, azotochelin and DFB by A. vinelandii.
Figure 4: Effect of azotochelin on V uptake in the presence of other vanadium ligands by A. vinelandii (mutant strain CA11.70).

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Acknowledgements

The authors wish to thank S. Brantley, T. M. Loveless and P. E. Bishop for providing the wild-type strain OP and the mutant strains CA11.70 and F196. We are also grateful to François M. M. Morel for useful discussions and his support throughout this work. We thank D. Little and E. Chan for their help with mass spectrometry. This work was supported by grants from the NSF (CHE-0221978, Center for Environmental Bioinorganic Chemistry and DEB-0614116), as well as fellowships from the French Department of Education to J.P.B and from the Camille and Henry Dreyfus Postdoctoral Program in Environmental Chemistry to T.W.

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Correspondence to A. M. L. Kraepiel.

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Bellenger, J., Wichard, T., Kustka, A. et al. Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nature Geosci 1, 243–246 (2008). https://doi.org/10.1038/ngeo161

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