Unraveling possible mechanisms - PNAS

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Sep 28, 2010 - studies of the biospheric sources and molecular mechanisms of ... 1Present address: Max Planck Institute of Molecular Plant Physiology, 14476 ...
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Kudzu invasion leads to NOx increase and ozone pollution: Unraveling possible mechanisms The article by Hickman et al. (1) presents very interesting data showing that the invasive nitrogen-fixing legume kudzu (Pueraria montana) exhibits strong biospheric impacts. This species has been known for many years as a plant enriching soil with nitrogen, protecting it from weathering and preventing erosion (for this purpose it was introduced in the United States from Japan in the 1950s). However, its mainly vegetative extensive spreading (60,000 ha annually in the southern United States) results in increased nitrogen oxides (NOx), in particular nitric oxide (NO), emissions, leading to a rise in tropospheric ozone levels. The production of NO caused by this plant is a consequence of increasing nitrogen input and cycling in soils. The authors do not discuss in detail possible mechanisms of NO formation related to kudzu invasion. The clarification of these mechanisms represents an important task that will lead to quantitative evaluations of the sources of NOx and O3 greenhouse gases. Here we briefly discuss possible sources of NOx formation to outline future directions of research. A possibility can be explored that the process of nitrogen fixation, resulting in ammonium accumulation in roots, leads to oxygen depletion in soil via stimulation of respiration by NH4+ (2). Under resulting anaerobic conditions, nitrate and nitrite can be used as terminal acceptors to produce NO species by the microbes. To date, only the contribution of soil bacteria (both denitrifying and oxidizing ammonia) has been considered as a significant source of NOx. Recent studies show that plant roots are capable of production of NOx in significant quantities under anoxic conditions (3). The main compartment conferring this reaction is mitochondria (descendants of prokaryotes) that can use nitrite in the absence of oxygen to produce NO (3), whereas other NOx can be byproducts of this reaction. Although the input of this process to formation of NOx in soils has to be

www.pnas.org/cgi/doi/10.1073/pnas.1009093107

quantified, it likely represents a minor source of NOx as compared with bacteria. Different bacteria are involved in the nitrogen cycle, which includes oxidation of ammonia to nitrates and reduction of nitrates to nitrite, nitrogen gas, and ammonium. Both oxidation of ammonia and reduction of nitrate/nitrite form NOx as byproducts of corresponding reactions. The anaerobic environment stimulates NOx production, not only during denitrification but also in the process of ammonia oxidation by Planctomycetes and even Nitrosomonas (4). Because the emissions of nitrous oxides in production and use of agro-biofuels can potentially negate global warming reduction (5), it is extremely important to understand all possible (including microbial and plant) sources of NOx and to quantify their biospheric impact. The article by Hickman et al. represents an important step in this direction. It shows that invasive plants, without proper nitrogen management, can be an important source of NOx formation and ozone pollution. The fundamental studies of the biospheric sources and molecular mechanisms of NOx production will result in proper quantification of the level of contribution of active nitrogen species and ozone in the global warming potential. Kapuganti J. Guptaa,1 and Abir U. Igamberdievb,2 Julius-von-Sachs-Institut für Biowissenschaften, 97082 Würzburg, Germany; and bDepartment of Biology, Memorial University of Newfoundland, St. John’s, NL, Canada A1B 3X9 a

1. Hickman JE, Wu S, Mickley LJ, Lerdau MT (2010) Kudzu (Pueraria montana) invasion doubles emissions of nitric oxide and increases ozone pollution. Proc Natl Acad Sci USA 107:10115–10119. 2. Hachiya T, et al. (2010) Ammonium-dependent respiratory increase is dependent on the cytochrome pathway in Arabidopsis thaliana shoots. Plant Cell Environ, 10.1111/ j.1365-3040.2010.02189.x. 3. Planchet E, Kaiser WM (2006) Nitric oxide production in plants: Facts and fictions. Plant Signal Behav 1:46–51. 4. Kampschreur MJ, et al. (2006) Role of nitrogen oxides in the metabolism of ammoniaoxidizing bacteria. Biochem Soc Trans 34:179–181. 5. Crutzen PJ, Mosier AR, Smith KA, Winiwarter W (2008) N2O release from agro-biofuel production negates global warming reduction by replacing fossil fuels. Atmos Chem Phys Discuss 7:11191–11205.

Author contributions: K.J.G. and A.U.I. wrote the paper. The authors declare no conflict of interest. 1

Present address: Max Planck Institute of Molecular Plant Physiology, 14476 Golm, Germany.

2

To whom correspondence should be addressed. E-mail: [email protected].

PNAS | September 28, 2010 | vol. 107 | no. 39 | E153