Anaerobic Ammonium Oxidation (Anammox) in Different Natural Ecosystems

ICoN2 and the NCycle16 1811 Anaerobic ammonium oxidation (anammox) in different natural ecosystems Bao-lan Hu, Li-dong Shen, Xiang-yang Xu and Ping Zheng1 Department of Environmental Engineering, Zhejiang University, Hangzhou 310058, China Abstract Anammox (anaerobic ammonium oxidation), which is a reaction that oxidizes ammonium to dinitrogen gas using nitrite as the electron acceptor under anoxic conditions, was an important discovery in the nitrogen cycle. The reaction is mediated by a specialized group of planctomycete-like bacteria that were first discovered in man-made ecosystems. Subsequently, many studies have reported on the ubiquitous distribution of anammox bacteria in various natural habitats, including anoxic marine sediments and water columns, freshwater sediments and water columns, terrestrial ecosystems and some special ecosystems, such as petroleum reservoirs. Previous studies have estimated that the anammox process is responsible for 50% of the marine nitrogen loss. Recently, the anammox process was reported to account for 9– 40% and 4–37% of the nitrogen loss in inland lakes and agricultural soils respectively. These findings indicate the great potential for the anammox process to occur in freshwater and terrestrial ecosystems. The distribution of different anammox bacteria and their contribution to nitrogen loss have been described in different natural habitats, demonstrating that the anammox process is strongly influenced by the local environmental conditions. The present mini-review summarizes the current knowledge of the ecological distribution of anammox bacteria, their contribution to nitrogen loss in various natural ecosystems and the effects of major influential factors on the anammox process. Introduction ‘Anammoxoglobus sulfate’ [13]) and Candidatus ‘Jettenia The process of anammox (anaerobic ammonium oxidation), asiatica’ [14]. Henceforth, these genera will be referred to which refers to the oxidation of ammonium coupled with simply as Brocadia, Kuenenia, Scalindua, Anammoxoglobus the reduction of nitrite under anoxic conditions, has been and Jettenia respectively. predicted to be a more thermodynamically favourable Anammox bacteria have been detected in various natural process than aerobic ammonium oxidation [1], yet the habitats, such as anoxic marine sediments [15–17] and anammox process was not discovered until nearly 20 years water columns [18–20], freshwater sediments [21] and water later in a wastewater-treatment plant in The Netherlands columns [22], terrestrial ecosystems [23,24] and some special [2]. The process is mediated by anammox bacteria, a ecosystems, such as petroleum reservoirs [10]. All of the deep-branching monophyletic group of bacteria within available evidence indicates that the anammox process is the phylum Planctomycetes. To date, anammox bacteria critically important in the marine nitrogen cycle, and the have not been cultured in the laboratory; however, at relative contribution of the anammox process to the total least five genera and 13 species have been identified production of dinitrogen gas (N2) has been estimated to be using culture-independent molecular techniques. These taxa 50% in the ocean [25]. In addition to marine environments, include the following: Candidatus ‘Brocadia’ (Ca. ‘Brocadia anammox activity has been detected in natural freshwater anammoxidans’ [3], Ca. ‘Brocadia fulgida’ [4] and Ca. and terrestrial environments [22,24], indicating that the ‘Brocadia sinica’ [5]); Candidatus ‘Kuenenia stuttgartiensis’ anammox process may play an even more significant role [6]; Candidatus ‘Scalindua’ (Ca. ‘Scalindua brodae’ [7], Ca. in the global nitrogen cycle than previously thought. ‘Scalindua wagneri’ [7], Ca. ‘Scalindua sorokinii’ [8], Ca. The ecological distribution of anammox bacteria and their ‘Scalindua arabica’ [9], Ca. ‘Scalindua sinooilfield’ [10] and contribution to the nitrogen loss in natural ecosystems are Ca. ‘Scalindua zhenghei’ [11]); Candidatus ‘Anammoxo- influenced by local environmental conditions: the organic − globus’ (Ca. ‘Anammoxoglobus propionicus’ [12] and Ca. content [26,27], NOx concentration [28], environmental stability [29], salinity [16,17] and temperature [22] have been described as key influencing factors. The present mini-review Key words: anaerobic ammonium oxidation (anammox), ecological distribution, environmental summarizes the recent findings concerning the distribution conditions, natural ecosystem, nitrogen loss. of anammox bacteria, their contribution to N2 production in Abbreviations used: anammox, anaerobic ammonium oxidation; DNRA, dissimilatory nitrite reduction to ammonium; OMZ, oxygen minimum zone. various natural habitats and the major factors influencing the 1 To whom correspondence should be addressed (email [email protected]). anammox process. C C Biochemical Society Transactions www.biochemsoctrans.org Biochem. Soc. Trans. (2011) 39, 1811–1816; doi:10.1042/BST20110711 The Authors Journal compilation 2011 Biochemical Society 1812 Biochemical Society Transactions (2011) Volume 39, part 6 Table 1 Ecological distribution of anammox bacteria and their contribution to N2 production in various natural habitats ND, no data. Location 16S rRNA affiliation Contribution (%) Reference(s) Marine sediments Skagerak (North Sea) ND 24–67 [26] Thames Estuary (U.K.) ND 1–8 [27] Randers Fjord (Denmark) Scalindua 5–24 [28] Greenland Sea (Greenland) Scalindua >19 [15] Disko Bay (Greenland) Scalindua ND [15] Cascadia Basin (U.S.A) ND 40–42 [32] Gullmarsfjorden (Sweden) ND 23–47 [14,50] Barents Sea (Greenland) Scalindua ND [15] Golfo Dulce (Costa Rica) Scalindua ND [15] Young Sound (Greenland) Scalindua ND [15] North Sea (North of the Friesian Front) Scalindua ND [15] Yodo Estuary (Japan) Scalindua, Brocadia, Kuenenia 1–2 [30] Chesapeake Bay (U.S.A.) Scalindua 0–22 [16] Cape Fear River Estuary (U.S.A.) Scalindua, Brocadia, Kuenenia, Jettenia 4–17 [17] North Atlantic ND 33–65 [33] Jiaozhou Bay (China) Scalindua ND [51] Mai Po Marshes (Hong Kong) Scalindua, Kuenenia ND [31] South China Sea (China) Scalindua ND [11] Equatorial Pacific Scalindua ND [52] Haiphong (Vietnam) Scalindua, Brocadia, Kuenenia <2 [53] Marine water columns Golfo Dulce (Costa Rica) Scalindua 19–35 [35] Black Sea Scalindua 10–15 [8,38] Namibian waters Scalindua Approximately 100 [18,39] Peruvian waters Scalindua Approximately 100 [20] Northern Chile Scalindua Approximately 100 [19] Arabian Sea Scalindua <13 [36,37] Freshwater ecosystems Lake Tanganyika (Kigoma) Scalindua 9–13 [22] Wintergreen Lake (U.K.) Scalindua ND [42] Xinyi River (China) Brocadia ND [21] Groundwater (Canada) Scalindua, Brocadia, Kuenenia, Jettenia 18–36 [41] Lake Kitaura (Japan) Brocadia, Kuenenia, Anammoxoglobus <40 [40] Terrestrial ecosystems Various terrestrial habitats (Switzerland) Scalindua, Brocadia, Kuenenia, Jettenia ND [23] Peat soil (The Netherlands) Brocadia, Kuenenia, Jettenia ND [43] Paddy soil (Southern China) Brocadia, Kuenenia, Jettenia, Anammoxoglobus 4–37 [24] Special ecosystems Hot springs (U.S.A.) Brocadia, Kuenenia ND [46] Hydrothermal vents (Mid-Atlantic Ridge) Scalindua, Kuenenia ND [47] Marine sponge (Norway) Scalindua 0–1 [48] Marine sponge (U.S.A.) Brocadia ND [49] Petroleum reservoirs (China) Scalindua, Brocadia, Kuenenia, Jettenia ND [10] Anammox in marine ecosystems anammox activities were detected in various marine sediments (Table 1). Although organisms belonging to the Brocadia and Anoxic sediments Kuenenia genera were found in some coastal and estuarine Dalsgaard and Thamdrup [26] first detected anammox sediments [17,30,31], the majority of anammox bacteria in activities in the sediments of two continental shelf sites marine sediments were affiliated with the Scalindua genus of the Skagerrak in the Danish Belt seaway. Subsequently, and showed surprisingly low diversity [8,9,15,18,20]. The C The Authors Journal compilation C 2011 Biochemical Society ICoN2 and the NCycle16 1813 contribution of the anammox process to regional nitrogen DNRA (dissimilatory nitrite reduction to ammonium) and 15 − loss is highly variable in marine sediments (Table 1); indeed, the anammox process through the NO2 signal-mediated 15 15 the reported amounts of N2 production by the anammox production of N N was easily mistaken as a signature for process have ranged from 20 to 80% in shelf and deep denitrification [37]. This finding indicates that anammox– sediments [26,32,33]. However, it has also been reported DNRA coupling, rather than denitrification, was responsible that the anammox process contributed to less than 20% for the massive nitrogen loss in the OMZ of the Arabian Sea. of the N2 production in shallow coastal and estuarine As observed in marine sediments, the dominant anammox sediments [16,17,27]. Therefore the relative contribution of species in marine water columns is closely related to the anammox to nitrogen loss is positively correlated with water Scalindua genus (Table 1). However, the factors influencing depth. Furthermore, the water depth and organic content are the anammox process in marine water columns are not negatively correlated because a larger fraction of the organic well known. Recent findings have indicated that aerobic − matter is mineralized during transport to the sediment within ammonium oxidizers provided NO2 and created anoxic a deep water column. Thus the organic content of deep microenvironments for the anammox bacteria through the sediment is low [29]. The higher electron donor (organic consumption of oxygen in the OMZs of the Black Sea and matter)

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