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      The Effect of Nitrogen Enrichment on C 1-Cycling Microorganisms and Methane Flux in Salt Marsh Sediments

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          Abstract

          Methane (CH 4) flux from ecosystems is driven by C 1-cycling microorganisms – the methanogens and the methylotrophs. Little is understood about what regulates these communities, complicating predictions about how global change drivers such as nitrogen enrichment will affect methane cycling. Using a nitrogen addition gradient experiment in three Southern California salt marshes, we show that sediment CH 4 flux increased linearly with increasing nitrogen addition (1.23 μg CH 4 m −2 day −1 for each g N m −2 year −1 applied) after 7 months of fertilization. To test the reason behind this increased CH 4 flux, we conducted a microcosm experiment altering both nitrogen and carbon availability under aerobic and anaerobic conditions. Methanogenesis appeared to be both nitrogen and carbon (acetate) limited. N and C each increased methanogenesis by 18%, and together by 44%. In contrast, methanotrophy was stimulated by carbon (methane) addition (830%), but was unchanged by nitrogen addition. Sequence analysis of the sediment methylotroph community with the methanol dehydrogenase gene ( mxaF) revealed three distinct clades that fall outside of known lineages. However, in agreement with the microcosm results, methylotroph abundance (assayed by qPCR) and composition (assayed by terminal restriction fragment length polymorphism analysis) did not vary across the experimental nitrogen gradient in the field. Together, these results suggest that nitrogen enrichment to salt marsh sediments increases methane flux by stimulating the methanogen community.

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          Responses of extracellular enzymes to simple and complex nutrient inputs

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            Nitrogen as a regulatory factor of methane oxidation in soils and sediments.

            The oxidation of methane by methane-oxidising microorganisms is an important link in the global methane budget. Oxic soils are a net sink while wetland soils are a net source of atmospheric methane. It has generally been accepted that the consumption of methane in upland as well as lowland systems is inhibited by nitrogenous fertiliser additions. Hence, mineral nitrogen (i.e. ammonium/nitrate) has conceptually been treated as a component with the potential to enhance emission of methane from soils and sediments to the atmosphere, and results from numerous studies have been interpreted as such. Recently, ammonium-based fertilisation was demonstrated to stimulate methane consumption in rice paddies. Growth and activity of methane-consuming bacteria in microcosms as well as in natural rice paddies was N limited. Analysing the available literature revealed that indications for N limitation of methane consumption have been reported in a variety of lowland soils, upland soils, and sediments. Obviously, depriving methane-oxidising bacteria of a suitable source of N hampers their growth and activity. However, an almost instantaneous link between the presence of mineral nitrogen (i.e. ammonium, nitrate) and methane-oxidising activity, as found in rice soils and culture experiments, requires an alternative explanation. We propose that switching from mineral N assimilation to the fixation of molecular nitrogen may explain this phenomenon. However, there is as yet no experimental evidence for any mechanism of instantaneous stimulation, since most studies have assumed that nitrogenous fertiliser is inhibitory of methane oxidation in soils and have focused only on this aspect. Nitrogen as essential factor on the sink side of the global methane budget has been neglected, leading to erroneous interpretation of methane emission dynamics, especially from wetland environments. The purpose of this minireview is to summarise and balance the data on the regulatory role of nitrogen in the consumption of methane by soils and sediments, and thereby stimulate the scientific community to embark on experiments to close the existing gap in knowledge.
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              A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission.

              Anthropogenic nitrogen (N) enrichment of ecosystems, mainly from fuel combustion and fertilizer application, alters biogeochemical cycling of ecosystems in a way that leads to altered flux of biogenic greenhouse gases (GHGs). Our meta-analysis of 313 observations across 109 studies evaluated the effect of N addition on the flux of three major GHGs: CO(2), CH(4) and N(2)O. The objective was to quantitatively synthesize data from agricultural and non-agricultural terrestrial ecosystems across the globe and examine whether factors, such as ecosystem type, N addition level and chemical form of N addition influence the direction and magnitude of GHG fluxes. Results indicate that N addition increased ecosystem carbon content of forests by 6%, marginally increased soil organic carbon of agricultural systems by 2%, but had no significant effect on net ecosystem CO(2) exchange for non-forest natural ecosystems. Across all ecosystems, N addition increased CH(4) emission by 97%, reduced CH(4) uptake by 38% and increased N(2)O emission by 216%. The net effect of N on the global GHG budget is calculated and this topic is reviewed. Most often N addition is considered to increase forest C sequestration without consideration of N stimulation of GHG production in other ecosystems. However, our study indicated that although N addition increased the global terrestrial C sink, the CO(2) reduction could be largely offset (53-76%) by N stimulation of global CH(4) and N(2)O emission from multiple ecosystems.
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                Author and article information

                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbio.
                Frontiers in Microbiology
                Frontiers Research Foundation
                1664-302X
                04 January 2012
                19 March 2012
                2012
                : 3
                : 90
                Affiliations
                [1] 1simpleDepartment of Ecology and Evolutionary Biology, University of California Irvine Irvine, CA, USA
                [2] 2simpleDivision of Planning, Science and Resource Management, Santa Monica Mountain National Recreation Area, U.S. National Park Service Thousand Oaks, CA, USA
                [3] 3simpleIFEVA, Facultad de Agronomía, CONICET – Universidad de Buenos Aires Buenos Aires, Argentina
                Author notes

                Edited by: Paul Bodelier, Netherlands Institute of Ecology, Netherlands

                Reviewed by: Marina Kalyuzhnaya, University of Washington, USA; Hinsby Cadillo-Quiroz, Arizona State University, USA; Zhongjun Jia, Chinese Academy of Sciences, China

                *Correspondence: Irina C. Irvine, Division of Planning, Science and Resource Management, Santa Monica Mountains National Recreation Area, U.S. National Park Service, 401 West Hillcrest Drive, Thousand Oaks, CA 91360, USA. e-mail: irina_irvine@ 123456nps.gov

                This article was submitted to Frontiers in Terrestrial Microbiology, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2012.00090
                3307020
                22470369
                4ac01fbb-3694-42dd-b4c3-1e2a74fdb675
                Copyright © 2012 Irvine, Vivanco, Bentley and Martiny.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                History
                : 07 December 2011
                : 23 February 2012
                Page count
                Figures: 3, Tables: 1, Equations: 0, References: 56, Pages: 10, Words: 7998
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                nitrogen gradient,mxaf,methane flux,nutrient limitation,methylotrophy,methanotrophy,acetate,methanogenesis

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