Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils
Highlights
► Methane emission globally will increase with increasing fertilizer application. ► Methane production is generally stimulated by nitrogenous fertilizers. ► Methane oxidation is generally reduced by nitrogenous fertilizers. ► Microbial diversity composition and traits are mechanistically related to fertilizer effects. ► Nitrogen as resource for methane cycling microbes needs further attention.
Introduction
Next to CO2, CH4 is the most important greenhouse gas adding about 1/3 to the radiative forcing exerted by CO2 [1]. Compared to preindustrial values, methane concentration has doubled to a current value of 1.77 ppmv. After stabilization of atmospheric methane levels in the period 1990–2006, levels are increasing again since 2007 (see [2]) leading to intensified research efforts regarding variability in sources and sinks of atmospheric methane. The global CH4 budget is dominated by biogenic sources (natural wetlands 23%, rice fields 21%, ruminants and termites 20%, landfills and other waste treatment systems 10% [1]). Hence, wetlands (natural and rice cultivation) constitute almost half of all biogenic methane sources globally and have been suggested to be responsible for the recent increase in methane concentration, mainly due to warming of arctic wetlands [2, 3].
Methane is produced by methanogenic archaea under anaerobic conditions (flooded soils, sediments, landfills, etc.) converting acetate, methanol or hydrogen together with carbon dioxide to methane (see Figure 1) (reviewed by [4••, 5]). The methanogenic substrates are the results of fermentative degradation of organic matter (e.g. dead roots) or photosynthetates exuded by plant roots [4••, 6••], which makes plants and important regulating factor of methane formation in wetland soils and sediments [7]. Wetland plants are also a major conduit of methane to the atmosphere, facilitating diffusion of methane through their internal gas transport systems [7]. However, approx. 50% of the methane produced in wetlands is removed before it reaches the atmosphere by the activity of methane oxidizing bacteria (MOB) which utilize oxygen leaking from wetland plant roots or oxygen diffusing from the water layer into the surface soil or sediment. MOB oxidize methane with oxygen to carbon dioxide for their energy generation and utilize the methane carbon also for generating new biomass (reviewed by [4••, 8]). In contrast to the well investigated MOB from wetland (high methane) environments, atmospheric methane in upland soils (e.g. forest, grassland) is consumed by as yet unknown organisms, specialized to oxidize methane concentrations in the nm range utilizing high affinity enzyme systems (reviewed by [9••, 10•]). MOB in aerobic soils contribute 6% to the global methane sink [1].
The key role MOB have in balancing the global methane cycle initiated intensive research into this process and organisms involved. Since the observation of reduced methane uptake in N-fertilized forest soils [11], the effect of nitrogenous fertilizers on methane oxidation has been the most investigated regulating factor of aerobic methane oxidation (reviewed [12••, 13••, 14••]). However, the proposed mechanisms as operating in pure culture experiments cannot explain the contradictory results observed in natural systems. This is even more complicated in wetlands where methane emission is the balance of production and oxidation which both can be affected by nitrogenous fertilizer addition [4••]. However, knowledge on the operating mechanisms is necessary because to what extent nitrogen controls emission of methane to the atmosphere has been designated as one of the key knowledge gaps in soil carbon–nitrogen interactions [15•] in a world of ever-growing fertilizer use and atmospheric nitrogen deposition [16] affecting carbon degradation, fixation and feedback to the atmosphere. Next to this, global circulation models (GCMs) do not account for methane–N cycle interactions [17] due to the lack of mechanistic knowledge possibly leading to some of the inconsistencies in simulating global methane emissions.
This review will synthesize the effects of nitrogenous fertilizers on methane production, consumption and emission from wetland and upland soils and will reflect on underlying causes for the conflicting and inconsistent results obtained so far. The central focus will be on the underlying microbiology and speculating on the role of recent discoveries of novel organisms and pathways. Novel techniques assessing microbial gene and gene functions may help to incorporate microbial traits into process models which is necessary to simulate and predict effects of climate change on nitrogen–carbon cycle interactions and resulting balance between methane sources and sinks.
Section snippets
Fertilizer effects on methane cycling from wetland and upland ecosystems
The intensive use of nitrogenous fertilizers globally, and the anticipated increase of such to meet growing food demands due to continued population growth [16] has led to increased research effort into environmental impact of fertilizer use. The tight coupling between methane and nitrogen cycling and the associated implications for atmospheric methane concentrations has evoked numerous studies assessing fertilizer effects on methane emission, consumption and underlying microbial processes. For
Methanogens in wetlands
Explanations of effects of nitrogenous fertilizers on methanogensis are mainly focused on the direct inhibition by toxic intermediates of denitrification (see also Figure 1, Figure 3a), or the indirect inhibition by competing microbes or effects of plants increasing their biomass and subsequent carbon input into the soil. Many of these effects have been modeled in mechanistic process models to predict, for example, fertilizer effects on methane emission from rice paddies [19] or natural
Synthesis
It is obvious that interactions between the nitrogen and methane cycle are complex and far from understood. It is clear, however, that more top-down effect studies on the ecosystem level will only yield more evidence of phenomena we already know but which we cannot explain mechanistically. Figure 3 gives a schematic overview of the general ways in which N-fertilization can influence methane production and oxidation in wetlands and uplands. Decades of molecular biological community analyses have
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
This work was part of the European Science Foundation EUROCORES Programme EuroEEFG as supported by funds from the Netherlands Organisation for Scientific Research (NWO) (Grant number 855.01.150). This publication is publication nr. 5054 of the Netherlands Institute of Ecology.
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