Environmental Pollution 244 (2019) 127e134

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Environmental Pollution

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Anaerobic oxidation in agricultural soils-synthesis and prospective*

* San'an Nie a, Gui-Bing Zhu b, Brajesh Singh c, Yong-Guan Zhu d, a College of Life Sciences, Fujian Agriculture and Forest University, Fuzhou, 350002, China b Key Laboratory of Drinking Water Science and Technology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China c Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith South, NSW, 2751, Australia d Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China article info abstract

Article history: Denitrification is considered as the dominant (N) removing pathway, however, anaerobic Received 5 May 2018 oxidation of ammonium (anammox) also plays a significant part in N loss in agricultural ecosystems. Received in revised form Large N inputs into agricultural soils may stimulate the growth of anammox bacteria, resulting in high 19 September 2018 activity and diversity of anammox bacteria and subsequent more N loss. In some specific niches, like Accepted 10 October 2018 oxic-anoxic interface, three processes, nitrification, anammox and denitrification couple with each other, Available online 10 October 2018 and significant anammox reaction could be observed. Soil parameters like pH, dissolved oxygen, salinity, oxidation-reduction potential (ORP), and substrate concentrations impact the anammox process. Here Keywords: Anammox we summarize the current knowledge on anammox activity and contribution to N loss, abundance and N loss diversity of anammox bacteria, factors affecting anammox, and the relationship between anammox and Rhizosphere other N loss pathways in agricultural soils. We propose that more investigations are required for (1) the Oxic/anoxic interface role of anammox to N loss with different agricultural management strategies; (2) microscale research on Agricultural soils the coupling of nitrification-anammox-denitrification, that might be a very complex process but ideal model for further studies responsible for N cycling in terrestrial ecosystems; and (3) new methods to estimate differential contributions of anammox, codenitrification and denitrification in total N loss in agricultural ecosystems. New research will provide much needed information to quantify the contri- bution of anammox in N loss from soils at landscape, ecosystem and global scales. © 2018 Elsevier Ltd. All rights reserved.

1. Introduction et al., 2013). These studies reported that a wide range of N2 pro- duction (20e80%) and less than 25% of total N is lost through High inputs of N fertilizers into agricultural soils lead to various anammox from marine and freshwater ecosystems, respectively. environmental issues and multiple changes to ecosystems (Guo Subsequently, the anammox has been found in many soils, which et al., 2010). Heterotrophic denitrification has long been consid- included permafrost soil (Humbert et al., 2010), peat soil (Hu et al., ered as the sole pathway for N loss to the atmosphere (Vitousek and 2011a), upland arable soil (Shen et al., 2013; Shen et al., 2015; Shen Howarth, 1991) until the discovery of anammox, extending our et al., 2017), paddy soil (Bai et al., 2015b; Li et al., 2016; Sato et al., understanding of the global N cycle (Mulder et al., 1995; Van de 2012; Yang et al., 2015; Zhu et al., 2011a), rice rhizosphere (Nie Graaf et al., 1996). Since then, anammox has been reported in et al., 2015), and temperate forest soil (Xi et al., 2016). marine ecosystems (Dalsgaard et al., 2012; Kuypers et al., 2005; The genetic potential of anammox in the environment can be Kuypers et al., 2003; Thamdrup and Dalsgaard, 2002), freshwater determined by molecular methods. The anammox process is ecosystems (Dale et al., 2009; Erler et al., 2008; Trimmer et al., mediated by bacteria within the phylum (Jetten 2003; Wang et al., 2012a), and land-freshwater interfaces (Zhu et al., 2010). At least five genera have been identified with culture-independent methods, including “Candidatus Brocadia”, “Candidatus Kuenenia”, “Candidatus Anammoxoglobus”, “Candidatus * This paper has been recommended for acceptance by Dr. K. Hageman. Jettenia”, and “” (Schmid et al., 2005), which * Corresponding author. have been discovered in agricultural soils (Shen et al., 2013; Shen E-mail address: [email protected] (Y.-G. Zhu). https://doi.org/10.1016/j.envpol.2018.10.050 0269-7491/© 2018 Elsevier Ltd. All rights reserved. 128 S. Nie et al. / Environmental Pollution 244 (2019) 127e134 et al., 2015; Wang and Gu, 2013; Yang et al., 2015; Zhu et al., 2011a). anammox bacteria (Humbert et al., 2010; Zhu et al., 2010). Zhu et al. The functional hzs genes consisted of three subunits (hzsA, hzsB, (2011a) first reported anammox in a long-term fertilized paddy soil, and hzsC) were specific biomarkers for quantifying anammox bac- which showed 23% of fertilizer N was lost through anammox, and teria (Kartal et al., 2011; Strous et al., 2006). Diversity and func- corresponded to 76 g N m 2 yr 1 in the paddy soil. Shen et al. tional gene abundance of anammox bacteria are commonly served (2014) estimated that 50.7 g m 2 yr 1 of N loss could be attrib- as the microbial indicators in assessing biological N removal (Sims uted to the anammox process. On a larger scale, it was estimated et al., 2013). Recent studies have suggested that, compared to ho- that potentially a total of 2.50 1012 gNyr 1 was lost by anammox, mogenous water column environments, terrestrial soils have a equivalent to 10% of the amount of ammonia fertilizers in southern higher diversity and abundance of anammox bacteria caused by China (Yang et al., 2015). Specially, Zhu et al. (2015a) assessed that highly heterogeneous niches, which may supply sufficient aerobic- the loss of (1.1 ± 0.7) 1012 gNyr 1 can be related to anammox in anaerobic interfaces (Hu et al., 2011a; Humbert et al., 2010; Nie paddy ecosystems, which implied that 4.6% of the applied chemical et al., 2015). N fertilizer is lost by anammox. The substantial contribution of Nitrification, denitrification, codenitrification, and anammox anammox to N loss was due, at least in part to the high load of are assumed to be the microbial processes involving in N removal in fertilization. The significant N loss by anammox may fill the gap of agricultural soils (Hayatsu et al., 2008; Long et al., 2013; Philippot N loss in paddy fields that could not be explained other processes et al., 2007; Spott and Stange, 2011). Denitrification has been (Zhu, 2008). widely explored and is known to be a major producer of gaseous N The anammox activity and contribution to N loss in paddy until the discovery of anammox (Thamdrup, 2012; Xu et al., 2013). fields varied greatly both vertically and horizontally with different Growing evidence of anammox importance in soil N cycle requires soil depths and types. Potential anammox rates in paddy soil detailed examination. Anammox is a relatively novel N removal ranged between 0.5 and 2.9 nmol N g 1 h 1 (contributed 4e37% of pathway alternative to heterotrophic denitrification. High ammo- soil N2 production) with high load of slurry manure, nium concentrations were reported to stimulate anammox reaction 0.3e5.4 nmol N g 1 h 1 (1e5%) with high concentration of , 1 1 in the bioreactor (Kartal et al., 2008; Strous et al., 1998). In agri- 5.6e22.7 nmol N2 g h (8.7e29.8%) with long-term fertiliza- 1 1 cultural soils, correspondingly, a relatively high N input may tion, and 0.02e5.25 nmol N2 g h (0.4e15%) in typical paddy stimulate the growth of anammox bacteria (Humbert et al., 2010), soils, respectively (Table 1). þ resulting in an increase in N loss. Anammox in a rice-wheat rotation The NH4 /NO3 concentration could be the key factor regulating soil contributed 3.15e9.62% of total N emission but no significant anammox in the soil. Anammox bacteria can endure high ammo- difference among fertilization regimes was observed (Gu et al., nium concentrations (Furukawa et al., 2009; Gao and Tao, 2011; 2017). The relationships between anammox rates, associated Joss et al., 2009). In intensively fertilized paddy fields, there is a þ microbiota and management strategies such as types and rates of high concentration of NH4 in comparison to NO3 , the anammox þ fertilization remain poorly characterized. activity is positively correlated with NH4 concentration (Shen et al., The aerobic-anaerobic interfaces are often hotspots for anam- 2014; Zhu et al., 2011a; Zhu et al., 2015a). However, when ammo- mox. In terrestrial ecosystems, anammox hotspots have been nium is available at relatively low concentration, the anammox þ described at land-freshwater interface (Zhu et al., 2013), oxic- activity seems correlated with NO3 rather than NH4 (Sato et al., anoxic interface in wetland ecosystems (Zhu et al., 2010). As 2012; Yang et al., 2015). These can be partially explained by the anammox depends on the coexistence of both oxidized and mechanisms known as N regulation (Geisseler et al., 2010), where reduced N compounds, we propose, based on previous research ammonium availability is high, the acquisition of other alternative (Nie et al., 2015; Sato et al., 2012; Wang et al., 2012a; Zhu et al., N sources (i.e., NO3 or organic molecules) is suppressed (Geisseler 2013; Zhu et al., 2011a), that significant anammox occurs at oxic/ et al., 2010). We propose that anammox bacteria may use NO2 anoxic interfaces with intensive exchange of N compounds (Zhu produced by nitrification at high ammonium concentration et al., 2010). In agricultural ecosystems, these may include: the whereas prone to utilize NO2 from denitrification under low flooded water-soil table interface; the rhizosphere where oxygen ammonium availability condition. concentration is reduced in comparison to adjacent soil due to respiration of plant roots and microorganisms (Brune et al., 2000; 2.2. Anammox in arable upland soil Humbert et al., 2010). This could be the coupled area of nitrifica- tion-anammox-denitrification. The anammox process could also play an important role in N This article aims to provide a comprehensive review based on loss from arable upland soils. The potential anammox activity is previous and current studies on the role and characteristics of variable, from being essentially absent to being mainly responsible anammox process in agricultural soils, focusing on (1) activity and for N loss, with activities ranging from 0.12 to 46.4 nmol N g 1 h 1 contribution of anammox to N loss; (2) abundance and diversity of correspondingly contributing 1.4e77.9% of total N loss (Long et al., anammox bacteria cells; (3) factors affecting anammox and (4) 2013; Shen et al., 2015; Shen et al., 2017). These ranges were larger anammox characteristics in some microniches. Finally, we identify than that observed in flooded paddy soils (Bai et al., 2015b; Sato and recommend future research on anammox in order to better et al., 2012; Shen et al., 2014; Yang et al., 2015; Zhu et al., 2011a). understand mechanisms so as to harness it to reduce N loss and It was estimated that 29.5 g N m 2 yr 1 (Shen et al., 2017) and environmental footprint of agricultural ecosystems. 7.1e78.2 g N m 2 yr 1 (Shen et al., 2015) could be lost related to anammox in different vegetable fields. These findings suggest 2. Role of anammox to N loss in agricultural soils anammox could be a significant N removal pathway in one of the most productive agricultural soils. However, there is likely over- 2.1. Anammox in paddy soil estimation because the coexistence of codenitrification, which can 29 14 þ also generate N2 simultaneously from the addition of NH4 and 15 15 15 The anammox is responsible for a significant loss of N from NO3 / NO2 in N tracer incubation experiments (Long et al., fertilizers in paddy soils. The paddy fields are characterized by long 2013). As more there is increasing use of inorganic N in agricul- growth period, oxic/anoxic interfaces, and oxygen-limiting envi- tural fields, the accurate quantification of N removal processes is ronments. These conditions may provide favorable conditions for highly needed. Table 1 Anammox activity, gene abundance, contribution to N loss and dominant community in different agricultural soils.

Sample Sample site (No. Sampled environment Depth cm Anammox Highest Contribution No. Of copies Highest copies Candidatus genus Reference 1 Analyzed) activity activity to N loss (%) g Paddy soil Southern China (10) High load of slurry manure as 0-100 (10 cm 0.5 0e10 4e37 8.6 10 5 to 40e50 cm Brocadia (predominant), Kuenenia, (Zhu et al., 7 fertilizer intervals) e2.9 nmol N 1.1 10 (hzo) Anammoxoglobus and Jettenia 2011) 1 1 g h Paddy field Kanto plains of Japan High concentration of nitrate 0-20 (4 cm 0.04 0e4cm 1e5 d a e Brocadia(predominant), Kuenenia (Sato et al., (5) pouring intervals) e2.7 nmol N 2012) 1 1 g h 5 Paddy soil Zhejiang, China Long-term fertilization 0-10, 20e30, 5.6e22.7 nmol0-10, 20- 8.7e29.8 1.0 10 to 0e10 cm Brocadia (predominant), Kuenenia (Shen et al., 1 1 6 50e60, 90-100 2Ng h 30 2.0 10 (hzsA) 2014) Paddy soil China (3) Typical paddy soil 0-5, 5e20, 20 0.02 5e20 cm 0.4e12.2 2.7 10 3 to 20e40 cm Brocadia(predominant), Kuenenia, (Bai et al., e40, 40-60 e0.77 nmol N 2.7 106 (hzsB) Jettenia 2015b) 127 (2019) 244 Pollution Environmental / al. et Nie S. 1 1 g h Paddy soil Southern China (12) Typical paddy soil 0e20 0.27 e 0.6e15 1.2 10 4 to e Brocadia (predominant), Kuenenia (Yang et al., 4 e5.25 nmol N 9.65 10 2015) 1 1 g h (hzsB) Paddy soil China (65) Typical paddy soil 0e50 0.20 e 6.7e12.7 eee (Zhu et al., e4.83 nmol N 2015) 1 gh 5 Paddy soil Subtropical China (6) Long-term manure fertilizer 0-60 (10 cm eee2.0 10 to 40e50 cm Brocadia (predominant), Jettenia (Wang 6 intervals) 2.7 10 (hzsB) et al., 2012) Paddy soil China (10) Rice plantation areas 0-80 (20 cm eee3.8 104 to 20-40; 40 Brocadia (predominant), Kuenenia (Bai et al., intervals) 1.6 107 (hzsB) e60 cm 2015a) Paddy soil Typical albic soil of With 1, 4, 9 years of rice cultivation 0-5, 20-25 eeee 4-year paddy Scalindua (Wang and Northeast China (6) history soil Gu, 2013) 6 Paddy soil Hunan, China (2) Pot experiment Rhizosphere 0.08 e 2e41 3.7 10 to rhizosphere Kuenenia (predominant), Brocadia (Nie et al., 7 and bulk soil e0.64 nmol N2 1.4 10 (hzsA) 2015) g 1 h 1 Paddy soil Hunan, China (10) Pot experiment Rhizosphere 0.27 Tillering e 4.8 10 5 to rhizosphere at Brocadia (predominant), Kuenenia, (Li et al., 6 e and bulk soil e0.71 nmol N stage 5.3 10 (hzsB) tillering stage Anammoxoglobus, Jettenia and Scalindua 2016) 134 1 1 g h Vegetable Southeastern China Typically applied as ammonium 0-100 (10 cm 2.2e35 nmol N10 1.4e18.4 7.8 10 4 to 0e40 cm Brocadia(predominant), Kuenenia, (Shen et al., 1 1 6 soil (10) nitrate, or ammonium sulphate intervals) g h e30 cm 1.1 10 (hzsA) Jettenia 2017) Vegetable Southeastern China High load of N and periodic water 10e20 4.2 e 5.9e20.5 2.8 10 5 to e Brocadia (predominant), Kuenenia, (Shen et al., soil (5) saturation e46.4 nmol N 3.0 106 (hzsA) Anammoxoglobus, Jettenia 2015) 1 1 g h Arable soil China (32) Dry farmland soil 0e10 eee6.3 104 to e Brocadia (predominant), Kuenenia, (Shen et al., 3.7 106 (hzsA) Anammoxoglobus and Jettenia 2013) Arable soil United States (6) Inorganic fertilizers for 5 years 0e30 0.12 e 32.1e77.9 5.0 10 3 to e Jettenia (Long et al., e6.15 nmol N 1.6 105 (hzo) 2013) 1 1c g h Rice-wheat Jiangsu, China Rice-wheat crop rotation for 5 0e20 0.68 CF 3.15e9.56 1.82-10 5-4.63- PMCF Brocadia (predominant), Scalindua, (Gu et al., 6 rotation years e2.08 nmol N treatment 10 (hzsB) treatment Jettenia 2017) 1 1c soil g h a Data not available. 129 130 S. Nie et al. / Environmental Pollution 244 (2019) 127e134

Generally, in the vegetable field, the nitrate concentration is 3. Diversity and abundance of anammox bacteria relatively much higher than that in the flooded paddy soils, even higher than the concentration of ammonium. Both nitrification and 3.1. Diversity and dominant groups denitrification may occur significantly in vegetable soil (Zhu et al., 2011b). Therefore, the substrates for anammox bacteria cannot be A higher biodiversity of anammox bacteria in soil ecosystems a limiting factor. In summary, in vegetable soils, anammox activity than marine (Amano et al., 2007; Woebken et al., 2008)andfresh- has much heterogeneity, due to intensive management measures, water ecosystems (Jetten et al., 2003; Schubert et al., 2006) has been such as frequent fertilization, temporal patterns of flooding, and observed, due to micro-niches in soil which may support diverse repetitive tillage. physiological feature of the anammox bacteria (Hu et al., 2011a; Humbert et al., 2010). The community structure of anammox bac- teria in soil differed with soil depth (Bai et al., 2015b; Shen et al., 2.3. Anammox in special sites 2017; Zhu et al., 2011a), fertilization pattern (Gu et al., 2017; Hui et al., 2017; Shen et al., 2013), land use (Zhou et al., 2017), and 2.3.1. Rhizosphere plant cultivation history (Wang and Gu, 2013). These indicate that Significant anammox reaction in rice rhizosphere was observed both local soil conditions and human activities can affect the dis- due to the typical oxic-anoxic interface, which is the major site of tribution of anammox bacteria. It was shown that Candidatus Bro- coupled nitrification-denitrification (Nie et al., 2015). The specific cadia was the most commonly dominant anammox groups in soils anammox cells in rhizosphere were examined by catalyzed re- (Table 1), suggesting “Brocadia” has developed a better ability of porter depositionefluorescence in situ hybridization (CARD-FISH) adaptation in terrestrial ecosystems. Indeed, “Brocadia” shows a and the occurrence of anammox was unraveled (Nie et al., 2015). diverse metabolism (Gori et al., 2011). This genus is capable of using Moreover, the anammox activity, contribution, and functional gene alternative electron donors (e.g., short-chain organic acids) as well as abundance were all significantly higher in the rhizosphere than the linking the oxidation of acetate to CO2 with the reduction of NO2 to bulk soil (Nie et al., 2015). The reason was that there were high N2 (Kartal et al., 2008). The “Kuenenia” was the second common ammonium (32.0e39.3 mg kg 1) and (9.1e10.1 mg kg 1) anammox genus in agricultural environments (Bai et al., 2015a; Shen concentrations in the rhizosphere, where both partial denitrifica- et al., 2013). The “Kuenenia” bacteria may be better adapted than tion and nitrification could occur and provide nitrite for anammox “Scalindua” to low salinity environments (Dale et al., 2009)whichis bacteria. The significant differences in anammox activities and common in agricultural ecosystems. However, “Jettenia”, “Anam- contributions to N2 production between rhizosphere and the bulk moxoglobus” and “Scalindua” could only be detected in certain soil soil are similar to the land-freshwater interfaces, which could types (Long et al., 2013; Wang and Gu, 2013) or particular depth (Zhu provide a hotspot for anammox (Zhu et al., 2013). The dynamics of et al., 2011a). The diversity and distribution of anammox bacterial anammox in the rhizosphere can vary due to plant growth stages. Li communities in soils have yet to be further investigated. It is et al. (2016) reported that anammox activities in rice rhizosphere essential to explore whether different anammox bacteria demand showed a temporal shift. Nevertheless, more specific research on specific niche conditions for their existence and function in the soil. the anammox process along the redox gradient (such as rhizo- sphere, soil profile from surface layer) in agricultural soils are 3.2. Abundance of anammox bacteria required for thorough understanding of the coupled nitrification- anammox-denitrification in these oxic-anoxic interfaces, which is The abundance of anammox bacteria based on functional gene ubiquitous (Jones and Hinsinger, 2008) and plays a vital part in N copy numbers in agricultural soils represent large variation ranges cycling (Jackson et al., 2012; Richardson et al., 2009). (Table 1). Anammox bacteria are absent in soils with low N contents (Humbert et al., 2010). However, depending on fertilization inputs into the soil, a relatively high content of N may stimulate the 2.3.2. Surface soil growth of anammox bacteria. The preferred habitats for anammox Basically, anammox rates in the surface layer are higher in paddy bacteria were deeper paddy soil (Bai et al., 2015a; Bai et al., 2015b; soils, but lower in arable upland layer, while both compared with Wang et al., 2012b; Zhu et al., 2011a), surface and subsurface soil in the subsurface layer. In flooded paddy soils, the highest anammox vegetable field (Shen et al., 2015; Shen et al., 2017), in which highest activity was found in the surface layer (Sato et al., 2012; Shen et al., numbers were present (Table 1). 2014; Zhu et al., 2011a). The long and stable flooded conditions Generally, the gene abundance of anammox bacteria is posi- provide anaerobic conditions, adequate substrates, and energy flow tively associated with the activity. Quantitative PCR of the func- for anammox bacteria in surface soils. However, in arable upland tional gene further confirmed the presence of anammox bacteria in fields, such as vegetable soil, though with high nutrients for different agricultural soils (Table 1). Most research showed anam- anammox, intermittent flooding implies the surface soil involve in mox activity was positively related to the abundance of functional alternating aerobic-anaerobic conditions. Such unstable conditions genes in typical paddy soils (Yang et al., 2015), vertical soil cores may not be suitable for the growth and metabolism of anammox (Shen et al., 2017), and vegetable fields (Shen et al., 2015). However, bacteria. The anammox bacteria in the surface layer is likely this is not conclusive, as some research showed that the anammox impacted by supply patterns (continuous and intermittent) of ox- bacterial abundance was not linked to the activity (Bai et al., 2015b; ygen. It is important to investigate anammox process that experi- Shen et al., 2014; Wang et al., 2012a). Anammox activity in the ence oxic/anoxic conditions such as alternative wetting and drying surface layer was very low in vegetable soil or even undetectable in in agricultural soils. paddy soil, but a relatively high abundance of anammox bacteria In summary, there were differences of anammox rates and and a detectable level of them could be observed, respectively (Bai contributions from studied soils. All findings indicated that anam- et al., 2015b; Shen et al., 2017). Therefore, the surface soil might mox can be a crucial N loss pathway in agriculture soils. The provide a niche for anammox bacteria but may not be suitable for accumulated research into anammox implied that the microbes the function. This may indicate that anammox bacteria can tolerant responsible for nitrite-dependent anaerobic ammonium in agri- relatively high oxygen (Kalvelage et al., 2011) but remain largely cultural soils can be varied greatly with their activities and con- dormant cells, thus no or very little function. The specific effects of tributions to N loss with field types and/or soil depths. oxygen on anammox need to be further explored. S. Nie et al. / Environmental Pollution 244 (2019) 127e134 131

4. Factors affecting anammox diversity of anammox bacteria compared with low salinity soils (Bai et al., 2015b; Wang and Gu, 2014). High soil salinity corresponded to In agricultural soils, the factors most likely affecting anammox high anammox activity and functional gene abundance in paddy process are inorganic N (ammonium, nitrate, and nitrite), dissolved soils (Bai et al., 2015b) and promoted anammox bacterial diversity in oxygen and/or ORP. Recently, soil pH, salinity, and root metabolism mangrove sediments (Wang and Gu, 2014). The genus of Scalindua is have also been indicated as important factors regulating anammox highly related to the salinity level while Brocadia and Kuenenia are (Bai et al., 2015b; Li et al., 2016; Wang and Gu, 2014). associated with low salinity (Amano et al., 2007; Dale et al., 2009). These studies suggest that soil salinity is essential for governing the 4.1. Ammonium, nitrate and nitrite activity and community structure of anammox bacteria. High salinity may suggest higher concentration of exchangeable ammonium and Anammox activity is correlated to the concentration of ammo- nitrite with stimulation of anammox bacteria (Rysgaard et al., 1999). nium, nitrate, and nitrite in the soil (Hu et al., 2011b). These inor- Significant knowledge and mechanistic gaps exist for the role of ganic N compounds had great impacts on anammox bacteria (Li salinity in altering anammox in agricultural soils. et al., 2016; Shen et al., 2014; Shen et al., 2015; Shen et al., 2017; Zhu et al., 2011a). In agricultural soils, nitrite is reliant on nitrate 4.3. Dissolved oxygen and ORP reduction by denitrification or ammonia oxidation, both are thought to play a crucial role on anammox (Naeher et al., 2015; Van Anammox occurred in oxygen-limited ecosystems and could be de Graaf et al., 1996). reversibly inhibited by oxygen (Strous et al., 1997). Generally, ox- The relative concentration of ammonium to nitrite and/or ni- ygen concentration and ORP in soil shift gradually with depth trate can impact the anammox activity. In agricultural soils, N-rich profiles. In agricultural soils, the relatively high oxygen concen- fertilizers are intensively used. The value of exchangeable ammo- trations in the surface layer were caused by air pervasion (Maier, nium in paddy soils could be much higher (sometimes 1e2 orders 1998). Low detection frequency of anammox bacteria in the sur- of magnitude) than nitrate or nitrite (Li et al., 2016; Nie et al., 2015; face paddy soil (0e5 cm) mainly attributed to the inhibition of Yang et al., 2015; Zhu et al., 2011a). Additionally, the organic N in dissolved oxygen (Bai et al., 2015b). These distinctly differed from the soil has to be mineralized to ammonium prior to usage by anammox reaction detected in the water-sediment interface (Zhu microorganisms (Geisseler et al., 2010). Therefore, generally nitrate et al., 2013). The possible reason could be the degradation of or/and nitrite rather than ammonium is the limiting factor for organic matter, which is higher in the surface sediment than in anammox in paddy soil. In vegetable fields, however, the content of paddy soil, resulting in oxygen depletion. Moreover, less negative nitrite or/and nitrate could be higher than (or similar with) ORP condition limit ferrous ion and organic compounds which are ammonium due to nitrification, which could supply enough nitrite electron donors for anammox bacteria (Kartal et al., 2007b; Kartal to sustain anammox (Jetten et al., 1998; Zhu et al., 2013). Therefore, et al., 2008; Strous et al., 2006). A low supply of ferrous has a it is envisaged that these inorganic N compounds may not limit negative effect on the growth of anammox bacteria (Huang et al., anammox. Furthermore, ammonium concentration had some cor- 2014). So far, most research into anammox sampled surface soil relations with anammox community structure (Bai et al., 2015a; cores with 10 cm, which probably overestimate the activity of Shen et al., 2013; Yang et al., 2015), but how ammonium can anammox. A more specified sampling should be adopted, especially affect the composition and diversity of anammox bacteria is poorly in the upper surface layer. Moreover, the moisture, alternation of characterized. drying and wetting, degradable organic matters, aeration, all of which have significant effects on ORP should be considered in the 4.2. Soil pH and salinity future research.

Anammox bacteria are influenced by soil pH and salinity, they 4.4. Rhizosphere effect favor neutral to slightly alkaline environments in bioreactors (pH 7e8.5) (Jetten et al., 2001; Mulder et al., 1995; Yamamoto et al., Few studies have addressed the anammox process in the 2008). The abundance and activity of anammox bacteria were rhizosphere, due to the complexity and difficulty in sampling the higher in the alkaline soils than acidic soils (Bai et al., 2015b). rhizosphere (Youssef and Chino, 1988). During flooding, some Microcosm incubation experiment showed a significant inhibition herbaceous plants are able to transport oxygen into the rhizosphere of anammox bacteria growth under strong alkaline condition (pH and the oxygen profile appears to regulate gradients of electron 3þ þ 9) (Wang and Gu, 2014), indicating high pH (>8.5) is unlikely to be acceptors (e.g., NO3 ,Fe ) and reduced compounds (e.g., NH4 , þ suitable for anammox bacteria. Many metal ions are unavailable at Fe2 )(Maier, 1998). These gradients are important for modulating high pH, which are electron donors (such as ferrous, manganous) the diversity and distribution of microorganisms in terrestrial for anammox bacteria. Surprisingly, anammox bacteria were also ecosystems. found in low pH sediments and paddy soils (Shan et al., 2018; Wang The anammox bacteria can use organic substrate selectively. and Gu, 2014; Zhu et al., 2015b). These findings indicate that Microbial growth in the rhizosphere is strongly influenced by root anammox bacteria can also adapt to low pH environments. Addi- exudates (i.e., sugars, amino acids, and organic acids) (Lynch and tionally, a higher diversity of anammox bacteria could be observed Whipps, 1991). Some organic substrates can inhibit anammox under both acid and alkaline conditions (Bai et al., 2015b; Wang and (Van de Graaf et al., 1996), while some organic acids (e.g., acetate Gu, 2014). Soil pH is important in shaping anammox bacterial and propionate) can be used as supplementary carbon (C) source community, as it generally affects ammonium availability (Bai et al., (Guven et al., 2005). Glucose, formate, and alanine have little in- 2015a; Yang et al., 2015), which affects anammox community fluence on the anammox process (Guven et al., 2005), yet succinate structure (Bai et al., 2015a; Shen et al., 2013; Yang et al., 2015). in rhizosphere was significantly correlated with anammox cell Anammox bacteria adapt to a wide range of salinity in the natural abundance (Li et al., 2016). More concerted research is needed to environments (Koop-Jakobsen and Giblin, 2009; Wang and Gu, address the relationship between anammox and root exudates. 2014). The salinity is substantially lower in agricultural soils The oxic/anoxic interface formed by oxygen releasing from roots (<8dsm 1)(Pitman and Lauchli,€ 2002) than in seawater (averaged may provide appropriate habitats for anammox bacteria. It was 35‰)(Wang et al., 2012a). High salinity promotes the growth and reported that the rice rhizosphere is a hotspot for anammox 132 S. Nie et al. / Environmental Pollution 244 (2019) 127e134 bacteria and activity (Nie et al., 2015). The positive effects can be interpreted by the transiently stimulated nitrite produced by nitrification as well as denitrification, which have been reported in marine (Kuypers et al., 2005), freshwater (Wang et al., 2012a) and soil (Zhu et al., 2011a). Moreover, the anammox process might be influenced by root exudates (Li et al., 2016). These findings implied that the root metabolism should be considered for evaluating the anammox process. Still, there are many gaps in our understanding of anammox process influenced by rhizosphere, which is the main area of co-occurrence of nitrification, denitrification, DNRA, and Fig. 2. The combination of anammox, denitrification and DNRA. Revised from Guven anammox (Fig. 1). et al. (2005).

5. The relationship between anammox, DNRA, denitrification, of soil microbial N cycling, more precise quantifications of the and codenitrification anammox which can distinguish the production of N2 from code- nitrification are considered necessary. The bacterial and fungal The linkage between anammox and dissimilatory nitrate contributions to produced N2 may be differentiated with antibiotic reduction to ammonium (DNRA) could serve as a signature for inhibition. The contributions of anammox, codenitrification, and denitrification. DNRA is thought to occur under specific conditions denitrification to total N emission may be differentiated by oper- 2 (i.e., low ORP and available NO3 ), which has some similarity to ating 15N isotope-tracing measurements combined with antibiotic denitrification (Silver et al., 2001; Zumft, 1997). Recent studies inhibition (Long et al., 2013). Future research is warranted to showed that DNAR may play important role in paddy soil (0e20 cm address the contribution of codenitrification to the N2 production depth) and upland soil (below 80 cm depth) (Shan et al., 2016; Zhu as well as to develop and verify new methods to distinguish this et al., 2018). Some anammox cells (i.e., Kuenenia stuttgartiensis)are contribution from anammox. þ capable of DNRA, reducing NO3 to NH4 (Kartal et al., 2007a). Regardless of whether DNRA is functioned by anammox bacteria or þ alternate microorganisms, DNRA might supply NH4 for anammox 6. Conclusions and perspectives þ (Fig. 2, b). As DNRA-derived NH4 is ultimately lost as N2, the whole process is adequately concealed as denitrification (Fig. 2, a). Thus an It has become increasingly clear that the microbial N cycling in even bigger portion of N loss from agricultural ecosystems may be agricultural soils is considerably more complex than previously evaluated by anammox. The coupled DNRAeanammox is difficult thought. N loss from terrestrial ecosystems is no longer synony- to distinguish from denitrification in most conventional isotope- mous with denitrification. Many other processes are potentially tracing analyses (Fig. 2). Therefore, it is important to identify the responsible for N removal. New evidence has been made available different products formed during these nitrate removal processes. on of N2 production via anaerobic ammonium oxidation coupled to Future research is required to address how tightly DNRA and iron (III) reduction (termed Feammox) (Ding et al., 2014) and anammox are coupled and whether this interaction occurs and nitrite-dependent anaerobic methane-oxidizing (termed n-damo) contributes to N loss. (Shen et al., 2014; Wang et al., 2012b) in terrestrial ecosystems. The contribution of anammox and denitrification to N loss can However, few measurements with the magnitude of contribution of 15 be quantified by N isotope-tracing techniques. Nevertheless, the process to soil systems have been investigated. Nevertheless, codenitrification may obscure estimation of the contribution as it we conclude that about 5e10% of the applied fertilizers may be lost 29 45 14 þ can also produce N2 by reducing N2O generated by using NH4 through the anammox process. As it has been investigated that 13% 15 and NO2 in the isotope-tracing analysis. Currently, the anammox of total N fertilizers applied on agricultural soils remain unac- 15 contribution to total N loss could be overestimated by the N tracer counted for (Zhu, 2008), anammox could partly explain this fate 29 technique. Furthermore, both bacteria and fungi can produce N2 (Fig. 3). as the end product of codenitrification. For a better understanding The fact that N loss is often concentrated around oxic-anoxic interfaces, suggests aerobic and anaerobic N metabolisms may co-

Fig. 3. Schematic representation of N transformation above, below and across the oxic- Fig. 1. Co-occurrence of nitrification, denitrification, DNRA and anammox in oxic/ reduced interface in Chinese agricultural soil. A hypothesis based on Zhu (2008). N loss anoxic rhizosphere. is highlighted in red to emphasize the concerned pathway within N cycling. S. Nie et al. / Environmental Pollution 244 (2019) 127e134 133 exist over a wide variety of oxygen concentration. This appears to Oceanogr. 57, 1331e1346. be of particular importance for N loss, seriously challenging our Ding, L.J., An, X.L., Li, S., Zhang, G.L., Zhu, Y.G., 2014. Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chro- current knowledge of organic matter remineralization. The oxic/ nosequence. Environ. Sci. Technol. 48, 10641e10647. anoxic interfaces in the agricultural soils are often hotspots for Erler, D.V., Eyre, B.D., Davison, L., 2008. 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