Review PaperNitrification and nitrifiers in acidic soils
Introduction
Acidic soils (defined as pH < 5.5) occupy 30% of the world's ice-free land and mainly support forest, woodland and grassland, with a minor fraction used for arable crops (Vonuexkull and Mutert, 1995). Nitrification is a crucial step in nitrogen biogeochemical cycling and plant nutrition in soil-plant ecosystems. Nitrification in soil is generally considered to be a two-step process where ammonia is first oxidized to nitrite by ammonia oxidizers, and subsequently to nitrate by nitrite-oxidizing bacteria (NOB). However, the recent discovery of some species of Nitrospira capable of complete ammonia oxidation (comammox) in water systems (Daims et al., 2015, van Kessel et al., 2015) and detection in soil (Pjevac et al., 2017) indicates that this process could also be relevant. Nitrification can lead to nitrate leaching, losses of nitrogen-based fertilizers and the increased emission of the greenhouse gas nitrous oxide (Wrage et al., 2001). In particular, nitrification in acidic soils can lead to further acidification and aluminum toxicity (He et al., 2012). It was previously assumed that nitrification was relatively low in acidic soils since the availability of the substrate ammonia (NH3) for the ammonia monoxygenase (AMO) enzyme of ammonia oxidizers would be limited and all isolated bacterial ammonia oxidizers did not grow in standard laboratory medium with a pH < 5.5 (De Boer and Kowalchuk, 2001). However, many recent studies have suggested that nitrification can occur at pH values as low as 3.0 (Norton and Stark, 2011) and that rates of nitrification based on mineralized organic nitrogen can be equal or even greater than that typically found in neutral pH soils (Booth et al., 2005).
There are probably three breakthrough discoveries that have promoted scientific interest and discussion on nitrification mechanisms in acidic soils. Firstly, in the 1980s, acidic forest soils in northwestern Europe were found to have a high potential for nitrate production (Vanbreemen and Vandijk, 1988) and subsequently resulted in increased public concern regarding the potentially damaging effects of nitrate leaching and pollution. Secondly, Stark and Hart (1997) used the 15N isotope-dilution technique in intact soil cores to measure gross nitrification and microbial assimilation in a large number of acidic forest soils. They demonstrated that standard measurements of net nitrification could be significantly lower than gross nitrification rates determined using 15N-based measurements and that microbial communities play an important role in promoting nitrate loss in acidic soil ecosystems. Thirdly, homologues of bacterial AMO-encoding genes were found in metagenomic fragments of uncultured archaea (Schleper et al., 2005, Venter et al., 2004) followed by the isolation of Nitrosopumilus maritimus (Könneke et al., 2005), confirming the potential for ammonia oxidation by organisms belonging to the (then-described) mesophilic crenarchaeota, and subsequently termed ammonia-oxidizing archaea (AOA). These organisms were found to be functionally important in soils and sediments (Leininger et al., 2006, Schleper and Nicol, 2010), especially in acidic soil ecosystems (Prosser and Nicol, 2008, Yao et al., 2011b). The discovery of obligately acidophilic AOA in these soils indicated that they possess specific adaptations allowing them to grow at low pH (Lehtovirta-Morley et al., 2011, Lehtovirta-Morley et al., 2014).
Since the turn of the century there has been a continual increase in the number of studies examining nitrification and nitrifiers in acidic soils. The majority of studies have focused on the distinct ecological niches of ammonia oxidizing bacteria and archaea, their relative importance to autotrophic nitrification and their environmental drivers (Erguder et al., 2009, Hu et al., 2014, Yao et al., 2013, Zhalnina et al., 2012). Some studies report on the methodology for the measurement of nitrification, the functioning of isolated microorganisms and the mechanisms responsible for nitrification.
Section snippets
Detection of nitrification rates
Accurate determination of nitrification rates is essential to understanding nitrogen-cycling processes. Nitrification rates have been measured using a wide variety of methods, such as the laboratory incubation of soils (e.g. in potential nitrification assays), the use of 15N tracers to determine changes in pools of ammonium and nitrate, and the use of inhibitors to differentiate the relative contribution of different microbial groups to ammonia oxidation (Hart et al., 1994b, Liu et al., 2015a,
Relationship between environmental factors and nitrification activity
As previously mentioned, soil pH and substrate concentration (usually NH3) are the two most important environmental factors which influence soil nitrification rate (Allen et al., 2005, Sahrawat, 2008, Yao et al., 2013). It was assumed that the absence of net nitrification in highly acidic soils was due to the exponential decrease in substrate availability (NH3 + H+ ↔ NH4+; pKa = 9.25) with decreasing pH (De Boer and Kowalchuk, 2001, Norton and Stark, 2011). However, high nitrification can occur
Conclusion and perspectives
The evidence for the high rates of nitrification in acidic soils is now well documented. Substrate concentration, nitrifier community composition and contributors to activity contrast between acidic and neutral/alkaline soil systems (Fig. 1). AOA generally make a much greater contribution than AOB to ammonia oxidation in acidic soils, although some acid-tolerant or uncultured acidophilic AOB may also contribute to ammonia oxidation. In nitrogen-limited systems, especially in natural forest
Acknowledgements
This work was supported by the National Natural Science Foundation of China (41525002, 41471206), the National Key R & D Program of China (2017YFD0200102), the Strategic Priority Research Program of China Academy of Sciences (XDB15020301), and Ningbo Municipal Science and Technology Bureau (2015C10031). GWN is funded by the AXA Research Fund.
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