Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils

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Recent dynamics and uncertainties in global methane budgets necessitate research of controls of sources and sinks of atmospheric methane. Production of methane by methanogenic archaea in wetlands is a major source while consumption by methane oxidizing bacteria in upland soils is a major sink. Methane formation as well as consumption is affected by nitrogenous fertilizers as has been studied intensively. This review synthesizes the results of these studies which are contradictory and await mechanistic explanations. These can be found in the community composition and the traits of the microbes involved in methane cycling. Molecular microbial investigations, use of stable isotope labeling techniques, discoveries and isolation of new species and pathways offer new insight into interactions between nitrogen and methane cycling.

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.

References (65)

  • M. Jahn et al.

    Global climate change and its impacts on the terrestrial Arctic carbon cycle with special regards to ecosystem components and the greenhouse-gas balance

    J Plant Nutr Soil Sci

    (2010)
  • R. Conrad

    Microbial ecology of methanogens and methanotrophs

    (2007)
  • J.P. Megonigal et al.

    Anaerobic metabolism: linkages to trace gases and aerobic processes

  • Y.H. Lu et al.

    In situ stable isotope probing of methanogenic archaea in the rice rhizosphere

    Science

    (2005)
  • H.J. Laanbroek

    Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review

    Ann Bot

    (2010)
  • J.D. Semrau et al.

    Methanotrophs and copper

    FEMS Microbiol Rev

    (2010)
  • P.F. Dunfield

    The soil methane sink

  • S. Kolb

    The quest for atmospheric methane oxidizers in forest soils

    Environ Microbiol Rep

    (2009)
  • P.A. Steudler et al.

    Influence of nitrogen-fertilization on methane uptake in temperate forest soils

    Nature

    (1989)
  • L.L. Liu et al.

    A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission

    Ecol Lett

    (2009)
  • E.L. Aronson et al.

    Methane flux in non-wetland soils in response to nitrogen addition: a meta-analysis

    Ecology

    (2010)
  • R. Wania et al.

    Implementation and evaluation of a new methane model within a dynamic global vegetation model: LPJ-WHyMe v1.3.1

    Geosci Model Dev

    (2010)
  • Z.C. Cai et al.

    Effects of nitrogen fertilization on CH4 emissions from rice fields

    Soil Sci Plant Nutr

    (2007)
  • T. Fumoto et al.

    Revising a process-based biogeochemistry model (DNDC) to simulate methane emission from rice paddy fields under various residue management and fertilizer regimes

    Global Change Biol

    (2008)
  • P.L.E. Bodelier et al.

    Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots

    Nature

    (2000)
  • A.S.K. Chan et al.

    Methane oxidation and production activity in soils from natural and agricultural ecosystems

    J Environ Qual

    (2001)
  • J. Tang et al.

    Quantifying wetland methane emissions with process-based models of different complexities

    Biogeosciences

    (2010)
  • S. Sakai et al.

    Methanocella arvoryzae sp nov., a hydrogenotrophic methanogen isolated from rice field soil

    Int J Syst Evol Microbiol

    (2010)
  • L.Q. Wu et al.

    Composition of archaeal community in a paddy field as affected by rice cultivar and N fertilizer

    Microb Ecol

    (2009)
  • D.Y. Liu et al.

    Relation between methanogenic archaea and methane production potential in selected natural wetland ecosystems across China

    Biogeosciences

    (2011)
  • R. Conrad et al.

    Soil type links microbial colonization of rice roots to methane emission

    Global Change Biol

    (2008)
  • D. Morozova et al.

    Stress response of methanogenic archaea from Siberian permafrost compared with methanogens from nonpermafrost habitats

    FEMS Microbiol Ecol

    (2007)
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