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Anaerobic oxidation () in different natural

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 as the electron acceptor under anoxic conditions, was an important discovery in the cycle. The reaction is mediated by a specialized group of planctomycete-like 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 . 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 , 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 (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

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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 [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) availability in organic-rich shallow sediments leads Namibian Sea [38,39]. Therefore anammox bacteria may be − to increased competition for NO2 between denitrifiers and dependent on the activity of aerobic ammonium oxidizers + anammox bacteria. Yet anammox bacteria are slow-growing under oxygen-limited conditions. The NH4 in the water − organisms [25] and are less competitive for NO2 than the column is released through the mineralization of organic denitrifiers in organic-rich shallow sediments. In electron- matter by both denitrifiers and DNRA organisms [20,37]. donor-limited deep sediments, -reducing organisms The availability of organic matter also acts as an important − − − produce more NO2 for the anammox process owing to factor controlling the release of NO2 from NO3 for the the shortage of sufficient organic matter. In addition, the anammox process. Lam et al. [20] showed that, in the OMZ relative importance of the anammox process is directly of Peru, anammox bacteria obtained at least 67% of their − − − related to the availability of NO3 [16,28]: a higher NO3 NO2 from nitrate reduction using organic matter as the − concentration leads to a higher nitrate reduction rate and a electron donors, whereas less than 33% of the NO2 was − greater release of NO2 for anammox. The stability of the derived from aerobic ammonium oxidation. Therefore the environment may also be important for regulating the relative availability of organic matter and its mineralization rate are importance of the anammox process [29], an effect that is important factors influencing the anammox process in marine due to the low growth rate of the anammox bacteria. The water columns. anammox process is only significant in stable environments that allow a prolonged period for the bacterial population to develop [29]. Recent studies have shown that the distribution Anammox in freshwater ecosystems of anammox bacteria and their contribution to nitrogen Although there is growing evidence for the widespread occur- loss is correlated with the salinity [17,31]. Scalindua is rence of anammox bacteria in marine environments, evidence the most abundant genus in environments with higher salt for the existence of anammox bacteria in natural freshwater concentrations and the most halotolerant of the anammox habitats is limited (Table 1). The first direct evidence of genera [34]. In addition, previous studies showed that higher anammox bacteria in freshwater ecosystems was provided contributions of the anammox process to nitrogen loss were by Schubert et al. [22], who have reported that the anammox found in environments with higher salinity [17] and that the process contributed to 9–13% of the N2 production and was abundances of Brocadia and Kuenenia species were negatively responsible for 0.2 Tg of the fixed inorganic nitrogen loss correlated with the salinity [17,31]. per year in Lake Tanganyika, the second largest freshwater body in the world. Temperature has been identified as an important factor influencing anammox activity in this Anoxic water columns freshwater ecosystem [22]. A higher relative contribution In 2003, two parallel studies demonstrated that anammox of the anammox process to nitrogen loss was reported in bacteria were responsible for a substantial portion of the a eutrophic freshwater lake, Lake Kitaura, in which up to nitrogen loss in the anoxic water columns of the Black Sea 40% of the N2 production was correlated to anammox − and Golfo Dulce, in which 10–35% of the total nitrogen activity [40]. A positive correlation between the NO3 loss was attributable to the anammox process [8,35]. Recent concentration and the relative importance of the anammox − studies indicated that the anammox process was responsible process was found in this lake, suggesting that the NO3 for a greater percentage (more than 50%) of the nitrogen concentration was the key factor for the development loss in marine water columns, especially in OMZs (oxygen of anammox bacterial populations and their activities in minimum zones) [18–20], and anammox bacteria were this freshwater habitat [40]. Anammox activities were also reported to be the dominant N2 producer in the OMZs of recently detected in ammonium-contaminated groundwater Namibia, Chile and Peru [18–20]. Denitrification was initially sites in Canada, where anammox activity was responsible for reported as the dominant driver of nitrogen loss in the OMZ 18–36% of the nitrogen loss [41]. Because the highest relative of the Arabian Sea [36]; however, a direct link between the contribution of the anammox process to nitrogen loss was

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found in sites with high concentrations of dissolved organic organic matter (e.g. humic acids) was identified as an + − matter, NH4 and NO3 , researchers hypothesized that important factor that influenced the distribution of anammox these factors influenced anammox activity [41]. In addition, bacteria (Brocadia and Jettenia) in peat soil [43]. anammox bacteria have also been detected in the sediments of the Xinyi River [21] and Lake Wintergreen [42]. Unlike marine environments, in which the anammox communities Anammox in special ecosystems were exclusively dominated by the Scalindua genus, different Anammox bacteria are active at 6–43◦C, with an optimal dominant anammox species have been observed in freshwater temperature of 35◦C in laboratory bioreactors [45]. However, ecosystems. In Lake Tanganyika and Lake Wintergreen, it was recently observed that this process also occurred at the Scalindua genus was the dominant anammox species 52◦C in hot springs [46], 72◦C in petroleum reservoirs [10] [22,42], whereas in the sediments of the Xinyi River, Lake and even at 85◦C in hydrothermal vents [47]. The dominant Kitaura and Canada’s groundwater environments, Brocadia anammox species in these high-temperature habitats were organisms were the most common representatives [21,40,41]. Brocadia or Kuenenia, but not Scalindua (Table 1). This result These findings suggest that freshwater environments are more is likely to be due to the higher optimal growth temperatures favourable for the growth of different groups of anammox of Brocadia and Kuenenia organisms (35◦C in bioreactors) bacteria than marine environments. compared with that of Scalindua organisms (12–15◦Cin marine ecosystems) [46]. The production of long-chain fatty acids in anammox bacteria at elevated temperatures Anammox in terrestrial ecosystems mediates their adaption to high-temperature environments Because anammox depends on the concomitant presence of [46]. The versatile of some anammox species oxidized and reduced inorganic nitrogen compounds under (such as Brocadia and Kuenenia) is critical for survival in anoxic conditions, the oxic/anoxic interfaces in terrestrial high-temperature habitats [10]. Byrne et al. [47] detected areas may provide suitable habitats for anammox bacteria the activity of anammox bacteria in a hydrothermal vent, [23]. However, little is known about the presence of anammox indicating that anammox may play an important role in the bacteria in terrestrial ecosystems (Table 1). Humbert et al. [23] nitrogen cycle in thermophilic and mesophilic environments. first reported the distribution of diverse anammox bacteria in Anammox bacteria were also detected in some marine agricultural and permafrost soils, which contained Brocadia, sponges, which are ancient animals [48,49]. The majority of Kuenenia, Scalindua and Jettenia. Four different anammox anammox sequences found in marine sponges were affiliated genera were also simultaneously detected in fertilized paddy with the Scalindua or Brocadia genus. Hoffmann et al. soil in Southern China [24], and three distinct anammox [48] detected the activity of anammox bacteria in marine genera were found together in nitrogen-loaded peat soil [43]. sponges and showed that anammox activity contributed to

These results suggest a higher diversity of anammox bacteria 1.25% of the N2 production; in addition, the in terrestrial ecosystems than usually observed in aquatic and denitrification processes were also found in the marine habitats and may be mediated by the larger variety of suitable sponges, and the related and complex interactions of these niches for anammox bacteria in terrestrial habitats [23]. nitrogen-cycling processes were mainly controlled by the + The dominant anammox species in the reported terrestrial metabolic waste products (e.g. NH4 and organic matter) of environments were affiliated with the Brocadia and Kuenenia the sponge host. Therefore the anammox process in marine + genera [23,24,44], demonstrating that Brocadia and Kuenenia sponges was largely influenced by the amount of NH4 and organisms exhibited a better adaptation capacity in these organic matter produced by the sponge host. ecosystems [23]. Brocadia and Kuenenia organisms possess a more mixotrophic metabolism than previously thought [4,12,44]. These microbes use ferrous iron and a variety of Conclusions and outlook organic compounds, such as formate, acetate, propionate With the current knowledge of the anammox process in and methylamines, as electron donors [4,12,44] and employ natural ecosystems, it is clear that anammox bacteria have ferric iron and manganese oxides as electron acceptors a widespread distribution in various natural habitats. Among during their metabolic activities [44]. Therefore the versatile the anammox bacteria that have been described to date, metabolism of Brocadia and Kuenenia organisms may be Scalindua organisms appear to be the most widespread the main reason for their better adaptation in heterogeneous anammox species in natural ecosystems. However, Brocadia terrestrial environments. Anammox activity was reported and Kuenenia species appear to be more likely to live in

to account for 4–37% of the soil N2 production in a freshwater and terrestrial ecosystems. The published data fertilized paddy soil, and the substantial contribution of have indicated that anammox activity was responsible for anammox to nitrogen loss in the paddy field was related 50% of the marine nitrogen loss and may also play an + to the high concentrations of NH4 that were introduced important role in the nitrogen cycle of freshwater and by the fertilization [24]. Moreover, Hu et al. [43] obtained terrestrial ecosystems. In contrast with marine ecosystems, an enriched anammox culture from a nitrogen-loaded peat the detection of anammox bacteria, the measurement of soil and showed a significant amount of anammox activity. anammox activity and elucidation of environmental factors In controlled environments, the presence of slowly released influencing the anammox process are still lacking for

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freshwater and terrestrial environments. Therefore more 13 Liu, S.T., Yang, F.L., Gong, Z, Meng, F.F., Chen, H.H., Quan, Z.X. and studies on the anammox process in a broader range of Furukawa, K. (2008) Application of anaerobic ammonium-oxidizing consortium to achieve completely autotrophic ammonium and sulfate freshwater and terrestrial habitats are required to obtain removal. Biores. Technol. 99, 6817–6825 a better comprehension of the ecological distribution of 14 Quan, Z.X., Rhee, S.K., Zuo, J.E., Yang, Y., Bae, J.W., Park, J.R., Lee, S.T. and anammox bacteria and their potential importance in marine Park, Y.H. (2008) Diversity of ammonium-oxidizing bacteria in a granular ecosystems as natural ecosystems. In addition, further study sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ. Microbiol. 10, 3130–3139 will enhance our understanding of the influential factors that 15 Schmid, M.C., Risgaard-Petersen, N., van de Vossenberg, J., Kuypers, control anammox activity in natural environments. M.M.M., Lavik, G., Petersen, J., Hulth, S., Thamdrup, B., Canfield, D., Dalsgaard, T. et al. (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ. Microbiol. 9, 1476–1484 Funding 16 Rich, J.J., Dale, O.R., Song, B. and Ward, B.B. (2008) Anaerobic ammonium oxidation (Anammox) in Chesapeake Bay sediments. Our research was supported by the National Hi-Tech Research Microb. Ecol. 55, 311–320 and Development Program of China (863) [grant number 17 Dale, O.R., Tobias, C.R. and Song, B. (2009) Biogeographical distribution 2006AA06Z332] and the Fundamental Research Funds for the Central of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Universities [grant number 2010QNA6017]. Fear River Estuary. Environ. Microbiol. 11, 1194–1207 18 Kuypers, M.M.M., Lavik, G., Wobken, ¨ D., Schmid, M.C., Fuchs, B.M. and Amann, R. (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. U.S.A. 102, 6478–6483 References 19 Thamdrup, B., Dalsgaard, T., Jensen, M.M., Ulloa, O., Farias, L. and 1 Broda, E. (1977) Two kinds of missing in nature. Z. Allg. Escribano, R. (2006) Anaerobic ammonium oxidation in the Microbiol. 17, 491–493 oxygen-deficient waters off northern Chile. Limnol. Oceanogr. 51, 2 Mulder, A., van de Graaf, A.A., Robertson, L.A. and Kuenen, J.G. (1995) 2145–2156 Anaerobic ammonium oxidation discovered in a denitrifying fluidized 20 Lam, P., Lavik, G., Jensen, M.M., van de Vossenberg, J., Schmid, M.C., bed reactor. FEMS Microbiol. Ecol. 16, 177–184 Woebken, D., Gutierrez, ´ D., Amann, R., Jetten, M.S.M. and Kuypers, 3 Strous, M., Fuerst, J.A., Kramer, E.H.M., Logemann, S., Muyzer, G., van de M.M.M. (2009) Revising the nitrogen cycle in the Peruvian oxygen Pas-Schoonen, K.T., Webb, R.I., Kuenen, J.G. and Jetten, M.S.M. (1999) minimum zone. Proc. Natl. Acad. Sci. U.S.A. 106, 4752–4757 Missing identified as new planctomycete. Nature 400, 21 Zhang, Y., Ruan, X.H., Op den Camp, H.J.M., Smits, T.J.M., Jetten, M.S.M. 446–449 and Schmid, M.C. (2007) Diversity and abundance of aerobic and 4 Kartal, B., van Niftrik, L.A., Rattray, J., van de Vossenberg, J., Schmid, anaerobic ammonium-oxidizing bacteria in freshwater sediments of the M.C., Damste, ´ J.S.S., Jetten, M.S.M. and Strous, M. (2008) Candidatus Xinyi River (China). Environ. Microbiol. 9, 2375–2382 ‘Brocadia fulgida’: an autofluorescent anaerobic ammonium oxidizing 22 Schubert, C.J., Durisch-Kaiser, E., Wehrli, B., Thamdrup, B., Lam, P. and bacterium. FEMS Microbiol. Ecol. 63, 46–55 Kuypers, M.M.M. (2006) Anaerobic ammonium oxidation in a tropical 5 Hu, B.L., Zheng, P., Tang, C.J., Chen, J.W., van der Biezen, E., Zhang, L., Ni, freshwater system (Lake Tanganyika). Environ. Microbiol. 8, 1857–1863 B.J., Jetten, M.S.M., Yan, J., Yu, H.Q. and Kartal, B. (2010) Identification 23 Humbert, S., Tarnawski, S., Fromin, N., Mallet, M.P., Aragno, M. and and quantification of anammox bacteria in eight nitrogen removal Zopfi, J. (2010) Molecular detection of anammox bacteria in terrestrial reactors. Water Res. 44, 5014–5020 ecosystems: distribution and diversity. ISME J. 4, 450–454 6 Schmid, M.C., Twachtmann, U., Klein, M., Strous, M., Juretschko, S., Jetten, 24 Zhu, G.B, Wang, S., Wang, Y., Wang, C., Risgaard-Petersen, N., Jetten, M.S.M., Metzger, J.W., Schleifer, K.H. and Wagner, M. (2000) Molecular M.S.M. and Yin, C.Q. (2011) Anaerobic ammonia oxidation in a fertilized evidence for genus level diversity of bacteria capable of catalyzing paddy soil. ISME J., doi:10.1038/ismej.2011.63 anaerobic ammonium oxidation. Syst. Appl. Microbiol. 23, 93–106 25 Jetten, M.S.M., van Niftrik, L.A., Strous, M., Kartal, B., Keltjens, J.T. and Op 7 Schmid, M.C., Walsh, K., Webb, R.I., Rijpstra, W.I., van de Pas-Schoonen, den Camp, H.J.M. (2009) Biochemistry and molecular biology of K., Verbruggen, M.J., Hill, T., Moffett, B., Fuerst, J., Schouten, S. et al. anammox bacteria. Crit. Rev. Biochem. Mol. Biol. 44, 65–84 (2003) Candidatus ‘Scalindua brodae’, sp. nov., Candidatus ‘Scalindua 26 Dalsgaard, T. and Thamdrup, B. (2002) Production of N2 through wagneri’, sp. nov., two new species of anaerobic ammonium oxidizing anaerobic ammonium oxidation coupled to nitrate reduction in marine bacteria. Syst. Appl. Microbiol. 26, 529–538 sediments. Appl. Environ. Microbiol. 68, 1312–1318 8 Kuypers, M.M.M., Sliekers, A.O., Lavik, G., Schmid, M.C., Jørgensen, B.B., 27 Trimmer, M., Nicholls, J.C. and Deflandre, B. (2003) Anaerobic Kuenen, J.G., Damste, ´ J.S.S., Strous, M. and Jetten, M.S.M. (2003) ammonium oxidation measured in sediments along the Thames Estuary, Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. United Kingdom. Appl. Environ. Microbiol. 69, 6447–6454 Nature 422, 608–611 28 Risgaard-Petersen, N., Meyer, R.L., Schmid, M.C., Jetten, M.S.M., 9 Woebken, D., Lam, P., Kuypers, M.M.M., Naqvi, S.W., Kartal, B., Strous, Enrich-Prast, A., Rysgaard, S. and Revsbech, N.P. (2004) Anaerobic M., Jetten, M.S.M., Fuchs, B.M. and Amann, R. (2008) A microdiversity ammonia oxidation in an estuarine sediment. Aquat. Microb. Ecol. 36, study of anammox bacteria reveals a novel 293–304 phylotype in marine oxygen minimum zones. Environ. Microbiol. 10, 29 Dalsgaard, T., Thamdrup, B. and Canfield, D.E. (2005) Anaerobic 3106–3119 ammonium oxidation (anammox) in the marine environment. Res. 10 Li, H., Chen, S., Mu, B.Z. and Gu, J.D. (2010) Molecular detection of Microbiol. 156, 457–464 anaerobic ammonium-oxidizing (anammox) bacteria in 30 Amano, T., Yoshinaga, I., Okada, K., Yamagishi, T., Ueda, S., Obuchi, A., high-temperature petroleum reservoirs. Microb. Ecol. 60, 771–783 Sako, Y. and Suwa, Y. (2007) Detection of anammox activity and 11 Hong, Y.G., Li, M., Cao, H.L. and Gu, J.D. (2011) Residence of diversity of anammox bacteria-related 16S rRNA genes in coastal marine habitat-specific anammox bacteria in the deep-sea subsurface sediment in Japan. Microbes Environ. 22, 232–242 sediments of the South China Sea: analyses of marker gene abundance 31 Li, M., Cao, H.L., Hong, Y.G. and Gu, J.D. (2011) Seasonal dynamics of with physical chemical parameters. Microb. Ecol. 62, 36–47 anammox bacteria in estuarial sediment of the Mai Po Nature Reserve 12 Kartal, B., Rattray, J., van Niftrik, L.A., van de Vossenberg, J., Schmid, revealed by analyzing the 16S rRNA and hydrazine oxidoreductase (hzo) M.C., Webb, R.I., Schouten, S., Fuerst, J.A., Damste, ´ J.S.S., Jetten, M.S.M. genes. Microbes Environ. 26, 15–22 and Strous, M. (2007) Candidatus ‘Anammoxoglobus propionicus’ a new 32 Engstrom, ¨ P., Penton, C.R. and Devol, A.H. (2009) Anaerobic ammonium propionate oxidizing species of anaerobic ammonium oxidizing bacteria. oxidation in deep-sea sediments off the Washington margin. Limnol. Syst. Appl. Microbiol. 30, 39–49 Oceanogr. 54, 1643–1652

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33 Trimmer, M. and Nicholls, J.C. (2009) Production of nitrogen gas via 44 Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., anammox and denitrification in intact sediment cores along a Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P. et al. (2006) continental shelf to slope transect in the North Atlantic. Limnol. Deciphering the evolution and metabolism of an anammox bacterium Oceanogr. 54, 577–589 from a community . Nature 440, 790–794 34 Terada, A., Zhou, S. and Hosomi, M. (2011) Presence and detection of 45 Kuenen, J.G. and Jetten, M.S.M. (2001) Extraordinary anaerobic anaerobic ammonium-oxidizing (anammox) bacteria and appraisal of ammonium oxidizing bacteria. ASM News 67, 456 anammox process for high-strength nitrogenous wastewater treatment. 46 Jaeschke, A., Op den Camp, H.J.M., Harhangi, H.R., Klimiuk, A., Hopmans, Clean Technol. Environ. Policy, doi:10.1007/s10098-011-0355-3 E.C., Jetten, M.S.M., Schouten, S. and Damste, ´ J.S.S. (2009) 16S rRNA 35 Dalsgaard, T., Canfield, D.E., Petersen, J., Thamdrup, B. and gene and lipid biomarker evidence for anaerobic ammonium-oxidizing Acuna-Gonz ˜ alez, ´ J. (2003) N2 production by the anammox reaction in the bacteria (anammox) in California and Nevada hot springs. FEMS anoxic water column of Golfo Dulce, Costa Rica. Nature 422, 606–608 Microbiol. Ecol. 67, 343–350 36 Ward, B.B., Devol, A.H., Rich, J.J., Chang, B.X., Bulow, S.E., Naik, H., 47 Byrne, N., Strous, M., Crepeau, ´ V., Kartal, B., Birrien, J.L., Schmid, M.C., Pratihary, A. and Jayakumar, A. (2009) Denitrification as the dominant Lesongeur, F. and Godfroy, A. (2009) Presence and activity of anaerobic nitrogen loss process in the Arabian Sea. Nature 461, 78–81 ammonium-oxidizing bacteria at deep-sea hydrothermal vents. ISME J. 37 Jensen, M.M., Lam, P., Revsbech, N.P., Nagel, B., Gaye, B., Jetten, M.S.M. 3, 117–123 and Kuypers, M.M.M. (2011) Intensive nitrogen loss over the Omani 48 Hoffmann, F., Radax, R., Woebken, D., Holtappels, M., Lavik, G., Rapp, Shelf due to anammox coupled with dissimilatory nitrite reduction to H.T., Schlappy, ¨ M.L., Schleper, C. and Kuypers, M.M.M. (2009) Complex ammonium. ISME J. 5, 1660–1670 nitrogen cycling in the sponge Geodia barrette.Environ.Microbiol.11, 38 Lam, P., Jensen, M.M., Lavik, G., McGinnis, D.F., Muller, ¨ B., Schubert, C.J., 2228–2243 Amann, R., Thamdrup, B. and Kuypers, M.M.M. (2007) Linking 49 Mohamed, N.M., Saito, K., Tal, Y. and Hill, R.T. (2010) Diversity of aerobic crenarchaeal and bacterial nitrification to anammox in the Black Sea. and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J. 4, Proc. Natl. Acad. Sci. U.S.A. 104, 7104–7109 38–48 39 Woebken, D., Fuchs, B.M., Kuypers, M.M.M. and Amann, R. (2007) 50 Brandsma, J., van de Vossenberg, J., Risgaard-Petersen, N., Schmid, M.C., Potential interactions of particle-associated anammox bacteria with Engstrom, ¨ P., Eurenius, K., Hulth, S., Jaeschke, A., Abbas, B., Hopmans, bacterial and archaeal partners in the Namibian upwelling system. Appl. E.C. et al. (2011) A multi-proxy study of anaerobic ammonium oxidation Environ. Microbiol. 73, 4648–4657 in marine sediments of the Gullmar Fjord, Sweden. Environ. Microbiol. 40 Yoshinaga, I., Amano, T., Yamagishi, T., Okada, K., Ueda, S., Sako, Y. and Rep. 3, 360–366 Suwa, Y. (2011) Distribution and diversity of anaerobic ammonium 51 Dang, H.Y., Chen, R.P., Wang, L., Guo, L.Z., Chen, P.P., Tang, Z.W., Tian, F., oxidation (anammox) bacteria in the sediment of a eutrophic freshwater Li, S.Z. and Klotz, M.G. (2010) Environmental factors shape sediment lake, Lake Kitaura, Japan. Microbes Environ. 26, 189–197 anammox bacterial communities in hypernutrified Jiaozhou Bay, China. 41 Moore, T.A., Xing, Y.P., Lazenby, B., Lynch, M.D.J., Schiff, S., Robertson, Appl. Environ. Microbiol. 76, 7036–7047 W.D., Timlin, R., Lanza, S., Ryan, M.C., Aravena, R. et al. (2011) 52 Hong, Y.G., Yin, B. and Zheng, T.L. (2011) Diversity and abundance of Prevalence of anaerobic ammonium-oxidizing bacteria in contaminated anammox bacterial community in the deep-ocean surface sediment groundwater. Environ. Sci. Technol. 45, 7217–7225 from equatorial Pacific. Appl. Microbiol. Biotechnol. 89, 1233–1241 42 Penton, C.R., Devol, A.H. and Tiedje, J.M. (2006) Molecular evidence for 53 Amano, T., Yoshinaga, I., Yamagishi, T., Thuoc, C.V., Thu, P.T., Ueda, S., the broad distribution of anaerobic ammonium-oxidizing bacteria in Kato, K., Sako, Y. and Suwa, Y. (2011) Contribution of anammox bacteria freshwater and marine sediments. Appl. Environ. Microbiol. 72, to benthic nitrogen cycling in a mangrove forest and shrimp ponds, 6829–6832 Haiphong, Vietnam. Microbes Environ. 26,1–6 43 Hu, B.L., Rush, D., van der Biezen, E., Zheng, P., van Mullekom, M., Schouten, S., Damste, ´ J.S.S., Smolders, A.J.P., Jetten, M.S.M. and Kartal, B. (2011) New anaerobic, ammonium-oxidizing community enriched from Received 17 August 2011 peat soil. Appl. Environ. Microbiol. 77, 966–971 doi:10.1042/BST20110711

C The Authors Journal compilation C 2011 Biochemical Society