Singh, j s & strong, p j 2015 biologically derived fertilizer a multifaceted bio tool in methane mit by Food production & climate issues

Ecotoxicology and Environmental Safety 124 (2016) 267–276

Contents lists available at ScienceDirect

Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv

Review

Biologically derived fertilizer: A multifaceted bio-tool in methane mitigation Jay Shankar Singh a,n, P.J. Strong b a

Department of Environmental Microbiology, BB Ambedkar (Central) University, Lucknow 226025, Uttar Pradesh, India Centre for Solid Waste Bioprocessing, School of Civil Engineering, School of Chemical Engineering, University of Queensland, St. Lucia, Queensland 4072, Australia

art ic l e i nf o

a b s t r a c t

Article history: Received 19 August 2015 Received in revised form 14 October 2015 Accepted 15 October 2015

Methane emissions are affected by agricultural practices. Agriculture has increased in scale and intensity because of greater food, feed and energy demands. The application of chemical fertilizers in agriculture, particularly in paddy fields, has contributed to increased atmospheric methane emissions. Using organic fertilizers may improve crop yields and the methane sink potential within agricultural systems, which may be further improved when combined with beneficial microbes (i.e. biofertilizers) that improve the activity of methane oxidizing bacteria such as methanotrophs. Biofertilizers may be an effective tool for agriculture that is environmentally beneficial compared to conventional inorganic fertilizers. This review highlights and discusses the interplay between ammonia and methane oxidizing bacteria, the potential interactions of microbial communities with microbially-enriched organic amendments and the possible role of these biofertilizers in augmenting the methane sink potential of soils. It is suggested that biofertilizer applications should not only be investigated in terms of sustainable agriculture productivity and environmental management, but also in terms of their effects on methanogen and methanotroph populations. & 2015 Elsevier Inc. All rights reserved.

Keywords: Bioresource Compost GHG Methanotrophs Paddy ﬁelds Sequestration

Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Overview of ammonia and methane-oxidizing bacteria . . 3. Overview of N-fertilizers on methane ﬂux. . . . . . . . . . . . . 4. Improving soil/sediment fertility and mitigating methane 5. Conclusion and recommendations . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

......................... ......................... ......................... emissions using biofertilizers . ......................... ......................... .........................

1. Introduction Methane (CH4) is a potent greenhouse gas that contributes towards global warming and is the second most important greenhouse gas, after carbon dioxide (IPCC, 2007; Zhou et al., 2013). Although less abundant than CO2, CH4 has approximately n

Corresponding author. E-mail addresses: jayshankar_1@bbau.ac.in (J.S. Singh), pjstrong@gmail.com (P.J. Strong). http://dx.doi.org/10.1016/j.ecoenv.2015.10.018 0147-6513/& 2015 Elsevier Inc. All rights reserved.

. . . . . . .

267 268 269 270 273 274 274

twenty times the impact (Kirschke et al., 2013). Anthropogenic activities such as the use of fossil fuels, agriculture, livestock farming, landﬁlling and biomass burning, account for 63% (566 Tg CH4 yr 1) of global CH4 emissions (Bousquet et al., 2006; Kirschke et al., 2013). Therefore, increased anthropogenic activity affects the CH4 ﬂux and has a strong potential to impact climate change. Methanotrophs sequester atmospheric CH4 in soils and are predicted to consume between 10 to 40 Tg CH4 yr 1, trapping more than 50% of the CH4 produced in soils (IPCC, 2001; Reeburgh et al., 1993).

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Agricultural production is expected to double by 2050 to support a projected human population of 9 billion (Raja, 2013). Increased food requirements place greater pressure on agrarian practices, where crop yields and areas must increase to meet demand (Singh et al., 2011). Agricultural practices (including crop type, irrigation, organic amendments and fertilizer use) affect CH4 production and consumption as these microbially-mediated processes are regulated by the prevailing soil physico-chemical properties of agrarian soils and sediments (Zheng et al., 2010). Nitrogen (N) fertilizers are widely recognized as one of the key factors affecting CH4 oxidation in agricultural soils (Kravchenko et al., 2002; Seghers et al., 2003). While short-term use of N fertilizers may prevent enzymatic methane oxidation, long-term use affects soil microbial communities and can impact CH4 production or oxidation (Bodelier and Laanbroek, 2004; Ho et al., 2014). A greater understanding of the effects of N fertilizers in the microflora responsible for the methane sink in soils is crucial to predict future trends in CH4 emissions. Net CH4 flux within the soils of agricultural lands may be governed by microbial interactions and subsequent changes to CH4 producing and consuming microbial populations. Even in well-aerated agricultural soils, where low or negligible CH4 uptake capacity was assumed, research indicates that CH4 oxidation is more important than previously assumed (Ho et al., 2015). The rate of global methane emissions from agricultural activities will certainly increase further if production is increased and intensified and no mitigation strategies are adopted. Agriculture is essential for food security and economic returns, but must be environmentally sustainable. Rice paddies are a significant source of CH4, which is problematic as rice production alone is anticipated to increase from 600 million tonnes in 2000 to 930 million tonnes by 2030 (Kubo and Purevdorj, 2004). Although genetically modified rice strains that divert more carbon into the grains could potentially decrease CH4 emissions (Bodelier, 2015), the foreseeable future of increased rice production will require more fertilizers to provide nutrients. It is important to increase agricultural production without detriment to environmental quality and even simple strategies can have great benefit. Adopting alternate wetting and drying cycles in rice production has delivered promising results, with up to 30% less CO2-equivalent emissions (IRRI, 2015). Practices such as these may ameliorate problems of accelerated gas emissions resulting from N-fertilizer based agriculture. Another practice, where organic fertilizers are combined with microbial amendments (biofertilizers) is a promising alternative to inorganic fertilizers. Currently, there are few reports emphasising the prospective role of biofertilizers with regard to CH4 mitigation, and this review article presents biofertilizers as a possible means to improve CH4 mitigation in agricultural systems. It is pertinent as sustainable and efficient tools are required to mitigate CH4 emissions via natural soil micro-flora (which include methanotrophs), while simultaneously improving soil quality and crop yields.

2. Overview of ammonia and methane-oxidizing bacteria The interaction between CH4 and nitrogen has been identiﬁed as one of the major gaps in carbon–nitrogen cycle interactions (Gardenas et al., 2011; Stein et al., 2012). So too is the interaction between the two pivotal functional groups: CH4 oxidizers and ammonia oxidizers. The two groups are proposed to have a common evolutionary history as the enzyme systems of CH4 and ammonium-oxidizers are similar and they occupy similar ecological niches (Holmes et al., 1995; Stein et al., 2012). To better understand the complex relationship between ammonia and methaneoxidizing bacteria, it is worth ﬁrst describing these microbes and

their key enzymes (Pandey et al., 2014). Autotrophic nitrifiers are responsible for the oxidation of ammonia to nitrite, which is a key process in the global cycling of nitrogen (Singh and Kashyap, 2006). Ammonia monooxygenase (AMO) is responsible for the first step, where ammonia is oxidized to hydroxylamine (Hollocher et al., 1981). The majority of known isolates of ammonia oxidizers or nitrifiers are β-Proteobacteria and consists of the genera Nitrosomonas, Nitrosospira, Nitrosovibrio and Nitrosolobus. The second group is γ-Proteobacteria that consists of two species of the genus Nitrosococcus and is exclusively marine (Coci et al., 2008). Methanotrophic bacteria can use methane as their sole carbon source and they serve as a global sink for methane. Methane monooxygenase is the key enzyme that is responsible for the first step, where CH4 is oxidized to methanol. Methanotrophs are traditionally classified as Type I (γ-Proteobacteria) or Type II (α-Proteobacteria), primarily according to their use of the ribulose monophosphate pathway (Type I) or serine (Type II) pathways for formaldehyde assimilation). They were further subdivided into a Type X group, which used the ribulose monophosphate pathway of the Type I methanotrophs, but also had capabilities associated with Type IIs. Methanotrophs are now predominantly classified according to whether they are γ-proteobacteria or α-proteobacteria; Type X are regarded as a subdivision of Type 1 as they are γ-proteobacteria. Verrucomicrobium (Methylacidiphilum and Methylacidimicrobium), a recently-discovered phylum that consists of thermophiles, has also been added to the group of known methane oxidising bacteria (Stein et al., 2012; Kalyuzhnaya et al., 2015; Strong et al., 2015). Methane monooxygenase and ammonia monooxygenase occur as particulate membrane-bound enzymes, although a soluble form of methane monooxygenase (sMMO) is synthesized in copperdeficient environments by some methanotrophs (Semrau et al., 2010). Both ammonia and methane monooxygenases have broad substrate ranges that include various hydrocarbons and halogenated hydrocarbons (Hyman et al., 1998; Vannelli et al., 1990). As both enzymes are capable of oxidising either ammonia or methane, methanotrophs and autotrophic nitrifiers are both participants in the global cycling of nitrogen and CH4. Genes encoding particulate methane monooxygenase (pMMO) and ammonia monooxygenase share high sequence identity and, despite their different physiological roles, appear to be evolutionarily-related enzymes (Holmes et al., 1995). Methanotrophs and autotrophic nitrifiers share many similarities and have several common key enzymes. In natural systems, the methanotrophs may play an important role in the N cycle, while the contribution of ammonia oxidizers to methanotrophy appears to be relatively minor. A similar trend was observed for rice crop soils. A study by Bodelier and Frenzel (1999) allowed for the discrimination methane and ammonia oxidation in using a competitive inhibitor (CH3F) and by differential recovery after inhibition by C2H2. By applying both assays to model microcosms the authors demonstrated a major contribution of methanotrophs to nitrification in the rhizosphere, while the contribution of nitrifiers to CH4 oxidation was insignificant. However, ammonia oxidizers may have a more important role in agricultural soils. Akiyama et al. (2014) measured N2O and CH4 fluxes after urea application in fields containing different soils and their results suggest that the ammonia oxidizers be more important to CH4 oxidation than previously considered, regarding agricultural soils treated with N fertilizers. Despite their clear overlapping abilities, the complex relationship and interactions between methanotrophs and ammonia oxidizers in the laboratory are not well understood. Zheng et al. (2014) assessed competition between methane and ammonia oxidizing bacteria and observed transfer of C from CH4 oxidation to other soil microbes, which was enhanced

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when urea was added. Their results suggest that methane as the C source provides a competitive advantage for the methane oxidizing bacteria and limits ammonia oxidizers, and that there is competition among the methanotrophs themselves (Type I outcompeted Type II in N-rich environments) - illustrating the complexity of individual microbial interactions in mixed cultures.

3. Overview of N-fertilizers on methane flux The type and availability of N in the soils/sediments is important as these factors directly affect the microbial communities, and may inhibit or stimulate methanotroph populations across agricultural and natural ecosystems. Generally, aerobic soils may be regarded as a CH4 sink, while wetland soils are regarded as a net source of atmospheric CH4. Numerous studies presumed adding mineral nitrogenous fertilizers inhibited CH4 oxidation and increased atmospheric CH4 emissions (Bodelier and Laanbroek, 2004). However, opinions differ regarding the influence of N fertilizers on the bacteria responsible for CH4 oxidation. This may be attributable to a number of reasons, including type of N, providing N in an N-limited system, and varying N2-fixing ability among methanotrophs (Bodelier and Laanbroek, 2004). Results from differing soil types and sediments and application units also compound discrepancies related to field observations, while a lack of data regarding copper availability can make conclusions regarding the effects of fertilizers on a methanotrophic community difficult (Semrau et al., 2010). The carbon and phosphate availability may also strongly impact outcomes related to N studies (Veraart et al., 2015). Reports regarding the effects of ammonium (NH4 þ ) based fertilizers on CH4 flux by methanotrophs are contradictory: researchers have observed inhibition (Hutsch et al., 1994), stimulation (Mohanty et al., 2006) or no effect (Delgado and Mosier, 1996). At the microbial community level, ammonium (NH4 þ ) based fertilizers have stimulated growth and activity of methanotrophs. Although methanotrophs and ammonia-oxidizers can oxidize either CH4 or NH4 þ , ammonia may inhibit CH4 oxidation at the biochemical level by outcompeting CH4 at the active site of the CH4 monooxygenase (Zheng et al., 2014; Stein et al., 2005). This was supported by earlier research indicating that CH4 oxidation in soils was inhibited when NH4 þ fertilizers were applied (King and Schnell, 1994; Gulledge et al., 1997). Contrasting these observations, CH4 oxidation in rice field sediments was enhanced after urea applications at higher doses (120 kg ha 1) of N (Prasanna et al., 2002). This may be due to increased Type I methanotrophs (Zheng et al., 2014), or even increased NH4 þ -oxidizers (Singh and Kashyap, 2007) or aerobic chemoautotrophic NH4 þ -oxidizers (Bedard and Knowles, 1989) outcompeting methanotrophs for the same ecological niche (Singh and Singh, 2012, 2013). While several studies observed that NO3 had a stronger inhibitory effect on methanotrophs than NH4 þ (Kightley et al., 1995; Wang and Ineson, 2003), reports generally recommend NO3 as the preferred N source for CH4 degradation (Le Mer and Roger, 2001; Mancinelli, 1995). In laboratory methanotroph culture and isolation media, NO3 is often used to provide N (Whittenbury et al., 1970). Supplying more inorganic–N has negatively affected methanotroph numbers across different soil treatments (Singh, 2010; Singh et al., 2010, 2011; Tiwari et al., 2015). Ammonia concentrations greater than 200 μg N g 1 dry weight solid significantly inhibited methane oxidation activity in paddy soils. Phylogenetic analyses demonstrated that the abundance of Type I methanotrophs (γ-proteobacteria) increased in soil microcosms amended with nitrogenous fertilizers, compared to Type II methanotrophs (α-proteobacteria) that were dominant in native soil. Interestingly, although CH4 oxidation activity significantly decreased with

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increasing nitrification activity, there was no statistically significant relationship between pmoA (pMMO) and amoA (ammonia monooxygenase) gene abundance (Alam and Jia, 2012), indicating that either pMMO genes were present and not expressed, or that the enzymes were expressed and not functional/inhibited. Neither group can flourish solely by oxidizing the other's substrate, but methanotrophs can oxidize NH4, while ammonia-oxidizers can oxidize CH4 (Bedard and Knowles 1989; Bodelier and Frenzel, 1999). However, consistent responses to these compounds in the environment have failed to emerge, as ammonia availability has both inhibited (King and Schnell, 1994) and stimulated (Bodelier et al., 2000) methane oxidation. Similarly, methanotrophs may contribute to (Bodelier and Frenzel, 1999), or suppress nitrification (Megraw and Knowles, 1987; Roy and Knowles, 1994). The C/N ratio of organic amendments may also affect the soil methane sink as long-term applications affect the size of the microbial community and its diversity. Wheat and maize straw amendments have high C/N ratios (97 and 25 respectively) and did not inhibit methanotrophs, while sugar beet and potato leaf amendments with low C/N ratios (13.5 and 11.3 respectively) inhibited CH4 oxidation (Hutsch, 1998). Degradation of substrates with low C/N ratios can increase soil NH4 þ content and thereby potentially inhibit methanotroph activity (Singh, 2013b). Soil amendments with high C/N ratios may promote N immobilization and consequently lower soil NH4 þ levels (Boeckx et al., 1998), but it is likely that they provide insufficient easily-accessible N for bacterial proliferation, and favour the growth of microbes such as fungi, which are capable of degrading recalcitrant carbon sources. In addition, the role of P and its effects on the N and methane cycle and interactions between microbial community members is also poorly understood. A recent study by Kalyuzhnaya et al. (2013) illustrated a novel mode of CH4 utilization coupled with a highly efficient pyrophosphate-mediated glycolytic pathway. Phosphate is clearly another key element that displays differing correlation to CH4 oxidation activity in different environments and little is known about the effects of P on methanotroph community structure and its consequences for methane consumption (Veraart et al., 2015), which adds another variable to already complex interactions between CH4 and N. Even after years of study, the interactions between the N and CH4 cycles are complex and our understanding is far from complete (Bodelier, 2011). A synopsis of the varying results that different N-sources have on CH4 oxidation activity has been illustrated in Table 2. Although many studies related to the possible underlying mechanisms for nitrogen regulation of methane oxidation in soils and sediments have been reviewed (Bodelier, 2011; Bodelier and Laanbroek, 2004), the role and the consequences of interactions between methanotrophs and ammonia oxidizers regarding C and N cycling has been investigated infrequently in complex natural ecosystems (Stein et al., 2012). Extensive research combining community structure, individual genomes, protein expression, functional capability and fluctuations in response to agricultural inputs are necessary. As such, there are still questions to be resolved in relation to the impact of N fertilizers on CH4 dynamics across different ecosystems:

For a given ecosystem under various constraints, which type of

soil methanotrophic community is more sensitive to N fertilizers, and why? Under what set of constraints does their shift in relative abundance lower total CH4 oxidation? What is the rate of CH4 oxidation by ammonia-oxidizing bacteria compared to methanotrophs in organic or inorganic N-amended soils? How do these rates (and microbial communities) vary in N-sufﬁcient or N-deﬁcient environments? How are the two enzymatic systems of the ammonia-oxidizing and methane-oxidizing bacteria interrelated and how do these

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Table 1 Overview of biofertilizers and their mode of activity. Biofertilizers

Beneﬁcial role

Diazotrophs (predominantly N2-ﬁxing bacteria) Azotobacter, Azospirrilum, Ochrobactrum, etc. Nitrifying bacteria

Decreases CH4 emission due to enhancing O2 diffusion in ﬂooded Pingak et al. (2014), soils via stimulation of root growth and hairs Bhardwaj et al. (2014)

Nitrosomonas Cyanobacteria (Blue Green Algae)

Anabaena, Aphanotheca, Aulosira, Gleotrichia, Lyngbya, Nostoc, Oscillatoria, Plectonema, Scytonema, Synechocystis, Tolypothrix, etc. Azolla (Plantae: Salviniaceae) (Association with Anabaena azollae)

References

Consume CH4 at the expense of methanotrophs in urea fertilized Bedard and Knowles (1989) soils Enhances CH4 oxidation rate by releasing plenty O2 during photosynthesis and make the ﬂooded paddy ﬁeld oxygenated

Rai et al. (2000), Prasanna et al. (2002), Pingak et al. (2014), Singh (2014)

Accelerates CH4 oxidation rate due to enhancing the dissolved O2 Prasanna et al. (2002) concentration in the ﬂooded paddy soils

substrates affect community abundance?

What is the effect of C type, N abundance, and phosphate availability on the community structure and function and what is the effect on methane ﬂux?

4. Improving soil/sediment fertility and mitigating methane emissions using biofertilizers The abundance, community composition and activity of methane oxidizing bacteria in agro-ecosystems, is crucial to the stability and efficiency of the CH4 sink in disturbed soils (Singh, 2011). Restorative practices that increase the population size of an efficient methane-oxidizing community in disturbed ecosystems (natural and agriculture lands) would significantly improve CH4 sequestration (Kizilova et al., 2013). Among options worth considering is the use of organic fertilizers in conjunction with beneficial microbes (Singh et al., 2010; Singh, 2013b). Organic fertilizers have a biological origin and, under various definitions, may include peat, composted plant waste (green waste), animal manure and poultry litter mixed with sawdust, biosolids from waste activated sludge or anaerobic digester sludge, animal slaughter wastes from meat processing, fish meal or even worm-castings, seaweed extracts and wood ash. Biofertilizers are organic fertilizers amended with organisms capable of beneficial functions such as photosynthesis or N2-fixation. These biofertilizers may use microorganisms such as cyanobacteria/blue green algae (Shukia et al., 2008; Singh, 2014), diazotrophs (Kennedy et al., 2004; Singh, 2013a), Azolla and mycorrhizae (Nadeem et al., 2014) to improve crop yields and decrease the amount of N fertilizer required. Biofertilizers could be crucial to sustainably improving soil conditions for agriculture to improve crop yields (Singh et al., 2011; Lakshmi et al., 2012; Bhardwaj et al., 2014), as well as lowering CH4 emissions (Table 1). Applying these organic fertilizers containing active microbes to degraded agriculture soils may not only conserve the methanotrophs still present, but improve the population density and diversity of methane-oxidizing bacteria (Seneviratne and Kulasooriya, 2013; Singh, 2015a). A conceptual model supporting biofertilizers as a green technology to lower chemical fertilizer use and improve methane mitigation has been proposed (Fig. 1). A large portion of CH4 is consumed by methanotrophs at anoxic–oxic interfaces such as the soil or root surfaces of aquatic plants (Conrad, 1996). Soil oxygen levels are significant for methane-oxidation (Mancinelli, 1995) as most methane oxidizers are obligate aerobes (Prasanna et al., 2002), and grow preferentially in relatively oxygen-rich environments such as surface soils or paddy rhizospheres. The methanotroph population size drastically

declines in dry land paddy soil over periods of heavy rainfall due to lack of O2 (Wilshusena et al., 2004; Singh et al., 2010). Light regimes in deep water photosynthesis allows for oxygenation of the sediments, promoting methane oxidation (King, 1990; King et al., 1990, King and Schnell, 1994). Oxygen also potentially prevents the growth of methanogens which produce CH4, as they are obligate anaerobes. Applying biofertilizers that contain aerobic photosynthetic organisms, such as cyanobacteria or Azolla, has improved and sustained oxygenation of flooded paddy soils (Lakshmanan et al., 1994; Mandal, 1961; Prasanna et al., 2002: Fig. 2). Azolla, a N2-fixing aquatic pteridophyte symbiotically associated with Anabaena azollae, is widely exploited as an efficient bio-fertilizer in rice paddy ecosystems (Yadav et al., 2014). The biomass may be free-floating or associated with the soil surface, and can provide sufficient aeration to the soils of flooded paddy agro-ecosystem to enable CH4 oxidation (Prasanna et al., 2002; Lakshmanan et al., 1994). Similarly, the beneficial role of cyanobacteria regarding CH4 mitigation was demonstrated for soils from rice fields treated with combinations of urea, Azolla and cyanobacteria (Prasanna et al., 2002: Fig. 2). Among the cyanobacteria, Synechocystis sp. are one of the most beneficial for lowering CH4 emission from soils, presumably aiding methane oxidation via oxygenation during photosynthesis (Umorin and Ermolaev, 1986; Prasanna et al., 2002: Fig. 3). Applying diazotrophs (Ochrobactrum anthropi, Azotobacter and Azospirillum) have also lowered methane emissions from paddy fields (Pingak et al., 2014). Among these diazotrophs, Ochrobactrum anthropi produces nitrous oxide reductase, an enzyme that converts N2O to N2, that may then be converted into plant-accessible nitrogen by N2-fixing soil micro-flora (Zumft, 1997). Azospirillum, a free-living aerobic diazotroph, can thrive under waterlogged conditions and improves its hosts ability to exchange gases (including O2) in the rhizospheric region by increasing the number of host plant lateral roots and root hairs (Sahoo et al., 2014). Inoculating Azospirillum to rice plant roots may lower CH4 emissions by stimulating extensive root growth and consequently increasing O2 exchange and CH4 oxidation in the rhizosphere. Nitrogen-fixing bacteria increase N availability to paddy crops (Cassman et al., 1998). Rhizobia (Rosch et al., 2002), methanotrophs (Knief et al., 2003; Hackl et al., 2004) and Archaea (Kemnitz et al., 2005) play important roles in C and N cycles in soils.The majority of the Type II methanotrophs (α-Proteobacteria: Methylocystis, Methylocella, Methylocapsa, and Methylosinus spp.) are capable of fixing N2, while some of the Type I methanotrophs (γProteobacteria: Methylosoma, Methylosphaera, and Methylococcus spp.) can fix N2 under low O2 tension (Aumen et al., 2001;

Table 2 N addition and its effect on methane oxidation. Methane oxidation

Remarks

Soil types

References

NH4 þ

Inhibited

Literature review of various soil types

Le Mer and Roger (2001)

NH4 þ

Inhibited

Methane oxidation potential of upland soils is reduced by cultivation, especially by ammonium N-fertiliser application Factors that favour CH4 emission from cultivated wetlands are mostly submersion and organic matter addition. Intermittent drainage and utilization of the sulphate forms of N-fertilisers reduce CH4 emission Highest consumption rates in rice paddy fields, swamps, landfills Aerobic soils have low CH4 oxidation activities and microbes mostly uncharacterized. Methane oxidation by aerobic upland soils rarely exceeds 0.1 mg CH4 m 2 ha–1 Forest soils are the most active, followed by grasslands and cultivated soils Strong inhibition increased with increasing methane concentration Authors proposed nitrite formation from methanotrophic ammonium oxidation accounted for most of the inhibition CH4 fluxes were sensitive primarily to landscape position and biogeochemical disturbances. N fertilization inhibited CH4 consumption in the upland birch/aspen and floodplain spruce sites, but not in the upland spruce site.

Soils

King and Schnell (1994)

Inhibited, or no effect

NH4 þ NH4 þ NH4 þ NH4 þ NH4 þ

Inhibited No effect No effect Stimulated Inhibited, or no effect

NH4 þ

Inhibited

NH4 þ

Inhibited

NH4 þ

Stimulated or inhibited No effect Inhibited

NH4

NH4 þ NH4 þ

Forests: Floodplain alder and white spruce Upland sites had similar CH4 oxidation rates ( 0.5 mg C m 2 d 1), while the floodplain sites had lower rates (0–0.3 mg Upland birch/aspen and C m 2 d 1). white spruce Paper birch (Betula papyrifera) stand exhibited a delayed inhibition response that became severe (60–70%) by the third season Upland coniferous forests (paper birch and white spruce) CH4 flux was not affected in a white spruce (Picea glauca) stand In laboratory incubations, (NH4)2SO4 had no effect on CH4 oxidation rates in either soil þ NH4 stimulated activity and growth of methane-oxidizing bacteria Root zone of rice plants Sediment pore water with NH4 þ concentrations o4 mM had no effect on CH4 oxidation. Littoral sediment NH4 þ concentrations between 4 and 10 mM NH4 þ reduced CH4 oxidation rates by 30%. CH4 oxidation decreased at Z 4 mM NH4 þ , completely inhibited at 420 mM NH4 þ CH4 oxidizing activity was 3 magnitudes greater than NH4 þ oxidizing activity Ammonium inhibited methane oxidation by all samples Intertidal freshwater marshes Inhibition depended on methane and ammonium concentrations. Increasing ammonium concentrations resulted in greater inhibition, and increasing methane concentrations resulted in less All N, P, and K treatments significantly decreased CH4 oxidation Paddy soil Authors concluded that methanotrophic population size and diversity is not enough to evaluate the soil CH4 sink accurately Stimulated at low concentrations ( N 1 g m 2) Peat Inhibited at high concentrations (N 10 g m 2) Nutrient and liming had no effect on rates of CH4 production or CH4 consumption Peat Long term application of (NH4)2SO4, completely inhibited CH4 oxidation, even when lime was applied to maintain a soil pH of Arable wheat field 6. Permanent grassland Long term application of NaNO3 caused no decline in CH4 oxidation compared to unfertilized grassland at the same pH Fallow (110 years) site Generally no significant effect, only inhibitory at high concentrations (1200 ppm dry mass) Landfill

NO3 Various N: NO3, NH4 and NO2 Various N salts and Urea NO3NO3NO3 or NH4 þ

No effect Inhibited, or no effect Stimulated

NH4NO3

Inhibited

urea

Stimulated

Urea Manure Urea

Stimulated growth Inhibited No effect

Negative relationship of methanotroph population with NH4 þ -N No effect of urea applied at 90 kg N h 1

Urea

No effect

No signiﬁcant difference after urea application at 120 kg N ha 1

Inhibited Inhibited Inhibited

Amendment with most N salts improved methane oxidation, except for urea Methane oxidation highest with NPK fertilizer CH4 oxidation was lowered by the addition of NO3 (86%), glucose (83%) and a combination of the two (99.4%) Inhibited activity by 33% NO3 had a very strong inhibitory effect compared to NH4 þ

Landﬁll Temperate-forest soils Temperate-forest soils Coniferous forest soil

Decreased methane oxidation capacity by 64% Enriched culture from landfill Inhibition by a nonspecific ionic effect rather than by specific inhibition soils Soil cores from plots that were treated with urea alone at 60, 90 and 120 kg N ha 1 oxidized methane more rapidly than did Rice soils 1 the core samples from plots treated with urea alone at 30 kg N ha Stimulated growth of Type 1s: Methylmicrobium and Methylocaldum Paddy soil

Gulledge et al. (1997)

Bodelier et al. (2000) Bosse et al. (1993)

Van der Nat et al. (1997)

Zheng et al. (2013) Keller et al. (2006) Keller et al. (2005) Hutsch et al. (1994)

Huber-Humer et al. (2011) Jugnia et al. (2012) Fender et al. (2012) Steudler et al. (1989) Wang and Ineson (2003) Kightley et al. (1995), Prasanna et al. (2002) Noll et al. (2008) Singh et al. (2010) Delgado and Mosier, 1996 Akiyama et al. (2014)

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Paddy soils Agriculture soil Spring barley Brassica cultivation. Soil types: Low-humic Andosol, yellow soil and grey lowland soil

Gulledge and Schimel (2000)

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Fertilizer

Inhibited No effect Various N

Inhibited Stimulated

Stimulated Various N

Various N

Inhibited, or no effect Urea and NH4 þ

Large applications ( 4100 kg N ha 1) inhibited CH4 oxidation in soils Small applications ( o 100 kg N ha 1) stimulated CH4 oxidation in soils

Deciduous forest Natural grassland Fertilized pasture Non-wetland soils. Analysis of literature

Aronson and Helliker (2010)

Boeckx and Van Cleemput, 1996

Mohanty et al. (2006) Rice ﬁeld and forest soils

Soil cores from:

Alam and Jia (2012) Paddy soil

Paddy soil Stimulated Urea

Urea stimulated methane oxidation 6-fold Ammonia oxidation was suppressed by CH4 CH4 partially inhibited the growth of Nitrosospira and Nitrosomonas in urea-amended microcosms, as well as growth of nitrite-oxidizing bacteria Ammonia and urea concentrations greater than 200 μg N g 1 dry weight solid was inhibitory, no difference with urea concentrations o 200 μg N g 1 dry weight Type I methanotrophs population increased in response to N fertilizers. Methane oxidation activity negatively correlated with nitriﬁcation activity in the presence of urea or ammonium Type I stimulated growth and methane consumption. Type I active in forest soils (Methylomicrobium /Methylosarcina related) differed from the active species in rice ﬁeld soils (Methylobacter/Methylomonas related) Methylocystis (Type II) species were inhibited by fertilization Different fertilizers added over a 10 year period prior to the study had no effect on methane oxidation of arable soil. Typical rates were: Deciduous forest soil (5.1 g CH4 ha 1 day 1) Natural grassland (3.5 g CH4 ha 1 day 1) Fertilized pasture (1.6 g CH4 ha 1 day 1) Arable soils with different fertilizer treatments (1.7–1.8 g CH4 ha–1 day 1)

Soil types Remarks Methane oxidation Fertilizer

Table 2 (continued )

Zheng et al. (2014)

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References

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Karthikeyan et al., 2014). There is little information on the diversity and interactions of Rhizobia, methanotrophs and Archaea with respect to tropical soils. Comprehensive field research regarding these microbes' relationships could impact agricultural land management practices and improve CH4 mitigation in the tropics (Butler and Laurance, 2008; Malhi et al., 2008). In addition to methanotrophs, other bacteria also contribute to CH4 oxidation. Some microbes involved in the oxidation of methanol, also degrade CH4 at concentrations below 10% (Huang et al., 2011). Some of these methylotrophs are even capable of plant growth promotion. Jhala et al. (2014) reported methane degradation enzymes and genes within known plant growth promoting bacteria identified from wetland paddy agro-ecosystems. Plant growth promoting strains of Paenibacillus illinoisensis, Bacillus aerius, B. subtilis and Rhizobium sp. contained the pmoA gene (encodes a subunit pMMO), while strains of Bacillus megaterium, P. illinoisensis, Methylobacterium extrorquens and Rhizobium sp. contained the mmoX gene (encodes a subunit of the hydroxylase of sMMO). Nitrosomonas spp. are nitrifying bacteria that obtain electrons for energy from oxidizing ammonia to nitrite. Although they fix carbon dioxide, their ammonia oxidase enzyme is not specific and can also oxidize CH4 - albeit at oxidation rates less than 5% of pure methanotroph cultures (Hanson and Hanson, 1996; Bodelier and Frenzel, 1999). Besides beneficial microbes, other amendments to organic fertilizers may facilitate the growth of methane oxidizing bacteria. Saline conditions in paddy soils can lower the activity and size of methane-oxidizing communities (Tilak et al., 2005). Organic amendments are traditional practices for reclaiming such soils (Supparattanapan et al., 2009), while pyrite is recommended for reclaiming saline, sodic or usar land soils, and boosts the soil properties of saline paddy fields in tropical regions (Pandey et al., 2005). Field studies have confirmed that farmyard manure in conjunction with pyrite can increase the number of methanotrophs in salinity-affected paddy fields (Singh et al., 2010). In salinity-disturbed paddy soils, combining long-term organic amendments with pyrite or fly ash appears to be an effective strategy for sustaining crops and increasing methanotroph activity. Similarly, short-term field experiments indicate scope for using fly ash in combination with organic manure (press mud) to increase methanotroph numbers in dry-tropical nutrient-poor saline soils (Singh and Pandey, 2013). Here, changes to the soil physicochemical properties due to the amendments are pivotal to enhanced soil methane oxidation. An alternative strategy to improve methane oxidation in saline soils could include seeding with salttolerant methanotrophs. Halophilic methanotrophs belonging to the genus Methylmicrobium are known (Kalyuzhnaya et al., 2008) and the population size and efficiency of these methanotrophs could be one of the factors governing CH4 consumption in saline soils (Khmelenina et al., 2000; Carini et al., 2005). Given the interaction of various microbes with the bacteria that are capable of degrading methane, it is imperative to understand the influence of organic and chemical fertilizers on soil and sediment microbial communities. The research would better determine the effects of modern agricultural practices, such as the shift towards organic amendments, as well as the use of enriched microbial cultures in the amendments. Microbial eco-genomics has advanced tremendously over recent time and is now a significantly cheaper, quicker and more robust technology. These advances allow researchers to qualify and quantify individual species that are able to oxidize methane, or that interact with these microbes, and determine which genes are up- or downregulated under specific conditions. Understanding the interactions of various microorganisms and how their metabolic capabilities relate to different forms of C, N and oxygen tension may allow for more generalized operating procedures to improve CH4

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Fig. 1. A conceptual model illustrating improved methanotrophic diversity and CH4 sink potential with the use of bio-fertilizers.

oxidation via biofertilizers. The beneﬁts would include increased crop yields coupled to lowered use of inorganic fertilizers, improved waste biomass reuse, and, ultimately less global atmospheric CH4.

5. Conclusion and recommendations

Fig. 2. Methane emitted from paddy ﬁeld soils that had been treated with urea, urea þ a cyanobacterial mixture, Azolla, or Azolla þ a cyanobacterial mixture (modiﬁed from Prasanna et al. (2002)).

Fig. 3. Methane uptake efﬁciency of different cyanobacteria inoculated paddy soils (modiﬁed from Prasanna et al. (2002)).

The long-term use of organic fertilizers with microbial amendments (biofertilizers) in agricultural management may be an ecologically-beneficial strategy to improve crop yields, while simultaneously decreasing CH4 emissions. It may not only conserve the methane-oxidizing populations present, but improve the population density and diversity. This could significantly enhance the robustness and the potential of the CH4 sink in agricultural soils. Cyanobacteria, Azolla, and fungal mycorrhizae serve as model organisms for biofertilizer systems. They are efficient microbes that contain novel genes for stress tolerance that could enhance the robustness of the microbial community (including the methane-oxidizing bacteria), thereby improving environmental remediation. Applying biofertilizers in agriculture may be considered as an emerging tool to boost methane-oxidizing bacteria within microbial communities. Biofertilizers seem an achievable and cost-effective prospect, but an integrated approach is required to combine the organic substrate and biological amendments for efficient gains (Singh, 2015b). Biofertilizers certainly hold promise as a new tool for tropical agriculture that overcomes many of the inorganic fertilizer shortcomings. Although biofertilizers have tremendous potential to enrich the soils, their direct and indirect effects with regard to the soil CH4 sink potential is yet to be fully elucidated, optimized and beneficially exploited. The impact of biofertilizers with regard to microbial CH4 oxidation under field conditions requires further study. Exploring the synergistic performance of biofertilizers with naturally-occurring microbial communities under field conditions

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could lead to better strategies for controlling methane ﬂux, especially in stressed agriculture soils. We now have advanced affordable technologies available to respond to questions regarding CH4 sequestration efﬁciencies within dynamic and varied systems. Given the implication of methane in global warming and climate change, it is relevant to explore potential mechanisms by which to conserve, stimulate or increase the effective populations of methane-sequestering microbes.

Acknowledgements JSS thanks Prof. R.C. Sobti (Hon’ble VC, BBAU, Lucknow, India) for his constant support and encouragement, Prof. S.P. Singh (Dept. of Botany, Banaras Hindu University, Varanasi, India) for suggestions and refinement and gratefully acknowledges financial support from UGC grant no. BSR Project [F.20-1/2012(BSR)/20-4(15)], New Delhi, Govt. of India. PJS gratefully acknowledges financial support from Remondis, the School for Civil Engineering grant no. DP 140104572 at UQ and the Australian Research Commission (DP 140104572).

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