Anaerobic ammonium oxidation (anammox) in different natural ecosystems

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.

Full text

ICoN2and 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
The process of anammox (anaerobic ammonium oxidation),
which refers to the oxidation of ammonium coupled with
the reduction of nitrite under anoxic conditions, has been
predicted to be a more thermodynamically favourable
process than aerobic ammonium oxidation [1], yet the
anammox process was not discovered until nearly 20 years
later in a wastewater-treatment plant in The Netherlands
[2]. The process is mediated by anammox bacteria, a
deep-branching monophyletic group of bacteria within
the phylum Planctomycetes. To date, anammox bacteria
have not been cultured in the laboratory; however, at
least five genera and 13 species have been identified
using culture-independent molecular techniques. These taxa
include the following: Candidatus ‘Brocadia’ (Ca. ‘Brocadia
anammoxidans’ [3], Ca. ‘Brocadia fulgida’ [4] and Ca.
‘Brocadia sinica’ [5]); Candidatus ‘Kuenenia stuttgartiensis’
[6]; Candidatus ‘Scalindua’ (Ca. ‘Scalindua brodae’ [7], Ca.
‘Scalindua wagneri’ [7], Ca. ‘Scalindua sorokinii’ [8], Ca.
‘Scalindua arabica’ [9], Ca. ‘Scalindua sinooilfield’ [10] and
Ca. ‘Scalindua zhenghei’ [11]); Candidatus ‘Anammoxo-
globus’ (Ca. ‘Anammoxoglobus propionicus’ [12] and Ca.
Key words: anaerobic ammonium oxidation (anammox), ecological distribution, environmental
conditions, natural ecosystem, nitrogen loss.
Abbreviations used: anammox, anaerobic ammonium oxidation; DNRA, dissimilatory nitrite
reduction to ammonium; OMZ, oxygen minimum zone.
1To whom correspondence should be addressed (email pzheng@zju.edu.cn).
‘Anammoxoglobus sulfate’ [13]) and Candidatus ‘Jettenia
asiatica’ [14]. Henceforth, these genera will be referred to
simply as Brocadia,Kuenenia, Scalindua,Anammoxoglobus
and Jettenia respectively.
Anammox bacteria have been detected in various natural
habitats, such as anoxic marine sediments [15–17] and
water columns [18–20], freshwater sediments [21] and water
columns [22], terrestrial ecosystems [23,24] and some special
ecosystems, such as petroleum reservoirs [10]. All of the
available evidence indicates that the anammox process is
critically important in the marine nitrogen cycle, and the
relative contribution of the anammox process to the total
production of dinitrogen gas (N2) has been estimated to be
50% in the ocean [25]. In addition to marine environments,
anammox activity has been detected in natural freshwater
and terrestrial environments [22,24], indicating that the
anammox process may play an even more significant role
in the global nitrogen cycle than previously thought.
The ecological distribution of anammox bacteria and their
contribution to the nitrogen loss in natural ecosystems are
influenced by local environmental conditions: the organic
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
summarizes the recent findings concerning the distribution
of anammox bacteria, their contribution to N2production in
various natural habitats and the major factors influencing the
anammox process.
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Table 1 Ecological distribution of anammox bacteria and their contribution to N2production 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
Anoxic sediments
Dalsgaard and Thamdrup [26] first detected anammox
activities in the sediments of two continental shelf sites
of the Skagerrak in the Danish Belt seaway. Subsequently,
anammox activities were detected in various marine sediments
(Table 1). Although organisms belonging to the Brocadia and
Kuenenia genera were found in some coastal and estuarine
sediments [17,30,31], the majority of anammox bacteria in
marine sediments were affiliated with the Scalindua genus
and showed surprisingly low diversity [8,9,15,18,20]. The
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contribution of the anammox process to regional nitrogen
loss is highly variable in marine sediments (Table 1); indeed,
the reported amounts of N2production by the anammox
process have ranged from 20 to 80% in shelf and deep
sediments [26,32,33]. However, it has also been reported
that the anammox process contributed to less than 20%
of the N2production in shallow coastal and estuarine
sediments [16,17,27]. Therefore the relative contribution of
anammox to nitrogen loss is positively correlated with water
depth. Furthermore, the water depth and organic content are
negatively correlated because a larger fraction of the organic
matter is mineralized during transport to the sediment within
a deep water column. Thus the organic content of deep
sediment is low [29]. The higher electron donor (organic
matter) availability in organic-rich shallow sediments leads
to increased competition for NO2−between denitrifiers and
anammox bacteria. Yet anammox bacteria are slow-growing
organisms [25] and are less competitive for NO2−than the
denitrifiers in organic-rich shallow sediments. In electron-
donor-limited deep sediments, nitrate-reducing organisms
produce more NO2−for the anammox process owing to
the shortage of sufficient organic matter. In addition, the
relative importance of the anammox process is directly
related to the availability of NO3−[16,28]: a higher NO3−
concentration leads to a higher nitrate reduction rate and a
greater release of NO2−for anammox. The stability of the
environment may also be important for regulating the relative
importance of the anammox process [29], an effect that is
due to the low growth rate of the anammox bacteria. The
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
of anammox bacteria and their contribution to nitrogen
loss is correlated with the salinity [17,31]. Scalindua is
the most abundant genus in environments with higher salt
concentrations and the most halotolerant of the anammox
genera [34]. In addition, previous studies showed that higher
contributions of the anammox process to nitrogen loss were
found in environments with higher salinity [17] and that the
abundances of Brocadia and Kuenenia species were negatively
correlated with the salinity [17,31].
Anoxic water columns
In 2003, two parallel studies demonstrated that anammox
bacteria were responsible for a substantial portion of the
nitrogen loss in the anoxic water columns of the Black Sea
and Golfo Dulce, in which 10–35% of the total nitrogen
loss was attributable to the anammox process [8,35]. Recent
studies indicated that the anammox process was responsible
for a greater percentage (more than 50%) of the nitrogen
loss in marine water columns, especially in OMZs (oxygen
minimum zones) [18–20], and anammox bacteria were
reported to be the dominant N2producer in the OMZs of
Namibia, Chile and Peru [18–20]. Denitrification was initially
reported as the dominant driver of nitrogen loss in the OMZ
of the Arabian Sea [36]; however, a direct link between the
DNRA (dissimilatory nitrite reduction to ammonium) and
the anammox process through the 15NO2−signal-mediated
production of 15N15 N was easily mistaken as a signature for
denitrification [37]. This finding indicates that anammox–
DNRA coupling, rather than denitrification, was responsible
for the massive nitrogen loss in the OMZ of the Arabian Sea.
As observed in marine sediments, the dominant anammox
species in marine water columns is closely related to the
Scalindua genus (Table 1). However, the factors influencing
the anammox process in marine water columns are not
well known. Recent findings have indicated that aerobic
ammonium oxidizers provided NO2−and created anoxic
microenvironments for the anammox bacteria through the
consumption of oxygen in the OMZs of the Black Sea and
Namibian Sea [38,39]. Therefore anammox bacteria may be
dependent on the activity of aerobic ammonium oxidizers
under oxygen-limited conditions. The NH4+in the water
column is released through the mineralization of organic
matter by both denitrifiers and DNRA organisms [20,37].
The availability of organic matter also acts as an important
factor controlling the release of NO2−from NO3−for the
anammox process. Lam et al. [20] showed that, in the OMZ
of Peru, anammox bacteria obtained at least 67% of their
NO2−from nitrate reduction using organic matter as the
electron donors, whereas less than 33% of the NO2−was
derived from aerobic ammonium oxidation. Therefore the
availability of organic matter and its mineralization rate are
important factors influencing the anammox process in marine
water columns.
Anammox in freshwater ecosystems
Although there is growing evidence for the widespread occur-
rence of anammox bacteria in marine environments, evidence
for the existence of anammox bacteria in natural freshwater
habitats is limited (Table 1). The first direct evidence of
anammox bacteria in freshwater ecosystems was provided
by Schubert et al. [22], who have reported that the anammox
process contributed to 9–13% of the N2production and was
responsible for 0.2 Tg of the fixed inorganic nitrogen loss
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
freshwater ecosystem [22]. A higher relative contribution
of the anammox process to nitrogen loss was reported in
a eutrophic freshwater lake, Lake Kitaura, in which up to
40% of the N2production was correlated to anammox
activity [40]. A positive correlation between the NO3−
concentration and the relative importance of the anammox
process was found in this lake, suggesting that the NO3−
concentration was the key factor for the development
of anammox bacterial populations and their activities in
this freshwater habitat [40]. Anammox activities were also
recently detected in ammonium-contaminated groundwater
sites in Canada, where anammox activity was responsible for
18–36% of the nitrogen loss [41]. Because the highest relative
contribution of the anammox process to nitrogen loss was
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found in sites with high concentrations of dissolved organic
matter, NH4+and NO3−, researchers hypothesized that
these factors influenced anammox activity [41]. In addition,
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
were exclusively dominated by the Scalindua genus, different
dominant anammox species have been observed in freshwater
ecosystems. In Lake Tanganyika and Lake Wintergreen,
the Scalindua genus was the dominant anammox species
[22,42], whereas in the sediments of the Xinyi River, Lake
Kitaura and Canada’s groundwater environments, Brocadia
organisms were the most common representatives [21,40,41].
These findings suggest that freshwater environments are more
favourable for the growth of different groups of anammox
bacteria than marine environments.
Anammox in terrestrial ecosystems
Because anammox depends on the concomitant presence of
oxidized and reduced inorganic nitrogen compounds under
anoxic conditions, the oxic/anoxic interfaces in terrestrial
areas may provide suitable habitats for anammox bacteria
[23]. However, little is known about the presence of anammox
bacteria in terrestrial ecosystems (Table 1). Humbert et al. [23]
first reported the distribution of diverse anammox bacteria in
agricultural and permafrost soils, which contained Brocadia,
Kuenenia,Scalindua and Jettenia. Four different anammox
genera were also simultaneously detected in fertilized paddy
soil in Southern China [24], and three distinct anammox
genera were found together in nitrogen-loaded peat soil [43].
These results suggest a higher diversity of anammox bacteria
in terrestrial ecosystems than usually observed in aquatic
habitats and may be mediated by the larger variety of suitable
niches for anammox bacteria in terrestrial habitats [23].
The dominant anammox species in the reported terrestrial
environments were affiliated with the Brocadia and Kuenenia
genera [23,24,44], demonstrating that Brocadia and Kuenenia
organisms exhibited a better adaptation capacity in these
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
organic compounds, such as formate, acetate, propionate
and methylamines, as electron donors [4,12,44] and employ
ferric iron and manganese oxides as electron acceptors
during their metabolic activities [44]. Therefore the versatile
metabolism of Brocadia and Kuenenia organisms may be
the main reason for their better adaptation in heterogeneous
terrestrial environments. Anammox activity was reported
to account for 4–37% of the soil N2production in a
fertilized paddy soil, and the substantial contribution of
anammox to nitrogen loss in the paddy field was related
to the high concentrations of NH4+that were introduced
by the fertilization [24]. Moreover, Hu et al. [43] obtained
an enriched anammox culture from a nitrogen-loaded peat
soil and showed a significant amount of anammox activity.
In controlled environments, the presence of slowly released
organic matter (e.g. humic acids) was identified as an
important factor that influenced the distribution of anammox
bacteria (Brocadia and Jettenia) in peat soil [43].
Anammox in special ecosystems
Anammox bacteria are active at 6–43◦C, with an optimal
temperature of 35◦C in laboratory bioreactors [45]. However,
it was recently observed that this process also occurred at
52◦C in hot springs [46], 72◦C in petroleum reservoirs [10]
and even at 85◦C in hydrothermal vents [47]. The dominant
anammox species in these high-temperature habitats were
Brocadia or Kuenenia, but not Scalindua (Table 1). This result
is likely to be due to the higher optimal growth temperatures
of Brocadia and Kuenenia organisms (35◦C in bioreactors)
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
mediates their adaption to high-temperature environments
[46]. The versatile metabolism of some anammox species
(such as Brocadia and Kuenenia) is critical for survival in
high-temperature habitats [10]. Byrne et al. [47] detected
the activity of anammox bacteria in a hydrothermal vent,
indicating that anammox may play an important role in the
nitrogen cycle in thermophilic and mesophilic environments.
Anammox bacteria were also detected in some marine
sponges, which are ancient animals [48,49]. The majority of
anammox sequences found in marine sponges were affiliated
with the Scalindua or Brocadia genus. Hoffmann et al.
[48] detected the activity of anammox bacteria in marine
sponges and showed that anammox activity contributed to
1.25% of the N2production; in addition, the nitrification
and denitrification processes were also found in the marine
sponges, and the related and complex interactions of these
nitrogen-cycling processes were mainly controlled by the
metabolic waste products (e.g. NH4+and organic matter) of
the sponge host. Therefore the anammox process in marine
sponges was largely influenced by the amount of NH4+and
organic matter produced by the sponge host.
Conclusions and outlook
With the current knowledge of the anammox process in
natural ecosystems, it is clear that anammox bacteria have
a widespread distribution in various natural habitats. Among
the anammox bacteria that have been described to date,
Scalindua organisms appear to be the most widespread
anammox species in natural ecosystems. However, Brocadia
and Kuenenia species appear to be more likely to live in
freshwater and terrestrial ecosystems. The published data
have indicated that anammox activity was responsible for
50% of the marine nitrogen loss and may also play an
important role in the nitrogen cycle of freshwater and
terrestrial ecosystems. In contrast with marine ecosystems,
the detection of anammox bacteria, the measurement of
anammox activity and elucidation of environmental factors
influencing the anammox process are still lacking for
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freshwater and terrestrial environments. Therefore more
studies on the anammox process in a broader range of
freshwater and terrestrial habitats are required to obtain
a better comprehension of the ecological distribution of
anammox bacteria and their potential importance in marine
ecosystems as natural ecosystems. In addition, further study
will enhance our understanding of the influential factors that
control anammox activity in natural environments.
Funding
Our research was supported by the National Hi-Tech Research
and Development Program of China (863) [grant number
2006AA06Z332] and the Fundamental Research Funds for the Central
Universities [grant number 2010QNA6017].
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Received 17 August 2011
doi:10.1042/BST20110711
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