Science of the Total Environment 757 (2021) 143928

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Fundamentals and potential environmental significance of denitrifying

anaerobic methane oxidizing archaea
Jing Ding a,c, Raymond Jianxiong Zeng b,d,⁎
a
School of Environmental Science and Engineering, Suzhou University of Science and Technology, Suzhou, Jiangsu 215009, China
b
Center of Wastewater Resource Recovery, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, China
c
Jiangsu Provincial Key Laboratory of Environmental Science and Engineering, Suzhou University of Science and Technology, Suzhou, Jiangsu 215009, China
d
CAS Key Laboratory for Urban Pollutant Conversion, Department of Applied Chemistry, University of Science and Technology of China, Hefei 230026, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• The status of research on DAMO archaea

is summarized.
• Inocula and enrichment parameters are
important for the culture enrichment.
• Environmental significance of DAMO ar-
chaea has been neglected.
• Some conjectures about anaerobically
metabolizing archaea are proposed.

a r t i c l e i n f o a b s t r a c t

Article history: Many properties of denitrifying anaerobic methane oxidation (DAMO) bacteria have been explored since their
Received 14 September 2020 first discovery, while DAMO archaea have attracted less attention. Since nitrate is more abundant than nitrite
Received in revised form 1 November 2020 not only in wastewater but also in the natural environment, in depth investigations of the nitrate-DAMO process
Accepted 16 November 2020
should be conducted to determine its environmental significance in the global carbon and nitrogen cycles. This
Available online 3 December 2020
review summarizes the status of research on DAMO archaea and the catalyzed nitrate-dependent anaerobic
Editor: Yifeng Zhang methane oxidation, including such aspects as laboratory enrichment, environmental distribution, and metabolic
mechanism. It is shown that appropriate inocula and enrichment parameters are important for the culture en-
Keywords: richment and thus the subsequent DAMO activity, but there are still relatively few studies on the environmental
Denitrifying anaerobic methane oxidation distribution and physiological metabolism of DAMO archaea. Finally, some hypotheses and directions for future
(DAMO) research on DAMO archaea, anaerobic methanotrophic archaea, and even anaerobically metabolizing archaea are
DAMO archaea also discussed.
Laboratory enrichment © 2020 Elsevier B.V. All rights reserved.
Environmental significance
Metabolic mechanism

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Laboratory enrichment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

⁎ Corresponding author at: Center of Wastewater Resource Recovery, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, China.
E-mail address: rzeng@ustc.edu.cn (R.J. Zeng).

https://doi.org/10.1016/j.scitotenv.2020.143928
0048-9697/© 2020 Elsevier B.V. All rights reserved.
J. Ding and R.J. Zeng Science of the Total Environment 757 (2021) 143928

2.1. Inocula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.2. Enrichment parameters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.2.1. Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.2.2. pH value . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2.2.3. Medium component. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3. Environmental distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4. Metabolism and the environmental significance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.1. Metabolism and physiology of DAMO archaea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.2. Other potential pathways in ecosystems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
4.3. Speculations about various archaea conducting anaerobic metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Declaration of competing interest. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

1. Introduction AOM is even found to couple with dissimilatory reduction of metals (in-
cluding Fe(III) and Mn(IV)) (Beal et al., 2009), in which ANME archaea
Anaerobic oxidation of methane (AOM) consumes approximately can oxidize methane solely and transfer electrons directly to metal com-
90% of the methane emitted from the ocean bed, and thus contributes pound (Cai et al., 2018; Ettwig et al., 2016; Leu et al., 2020; Yan et al.,
significantly to the control of the methane flux into the atmosphere 2018), or ANME archaea should be partnered with metal-reducing mi-
(Ding et al., 2016b). AOM can couple with several kinds of electron ac- croorganisms (MRM) to accept electrons and reduce metal oxides (He
ceptors as is first discovered for sulfates, and the process of sulfate- et al., 2018b). These three kinds of AOM process are illustrated in
dependent anaerobic methane oxidation (SAMO) is jointly catalyzed Fig. 1. The equations involved are as follows.
by the anaerobic methanotrophic (ANME) archaea and sulfate-
reducing bacteria (SRB), in which the ANME archaeon activates and me- CH4 þ SO2− − −
4 ! HCO3 þ HS þ H2 O SAMO
tabolizes methane through a “reversed methanogenesis” pathway,
leading to an intermediate that is scavenged as an electron donor by
5CH4 þ 8NO− þ
3 þ 8H ! 5CO2 þ 4N2 þ 14H2 O nitrate−dependent DAMO
the sulfate-reducing partner (Knittel and Boetius, 2009). Following the
investigations of SAMO, AOM coupling with nitrate/nitrite reduction
called denitrifying anaerobic methane oxidation (DAMO) was discov- 3CH4 þ 8NO− þ
3 þ 8H ! 3CO2 þ 4N2 þ 10H2 O nitrite−dependent DAMO
ered in 2006 after 16 months of laboratory enrichment
(Raghoebarsing et al., 2006). The enriched culture contains the uncul-
CH4 þ 8FeðOHÞ3 þ 15Hþ ! HCO−
3 þ 8Fe
2þ
þ 21H2 O Fe−dependent AOM
tured NC10 phylum bacteria (DAMO bacteria) and Methanosarcinales
archaeon (DAMO archaea) that is distantly related to marine
methanotrophic archaea (Raghoebarsing et al., 2006). Furthermore, CH4 þ 4MnO2 þ 7Hþ ! HCO−
3 þ 4Mn
2þ
þ 5H2 O Mn−dependent AOM

N2
Fe(III)/Mn(IV)

Fe/Mn

Fig. 1. Anaerobic methane oxidation coupling with various electron acceptors. a, AOM coupling with sulfate reduction; b, AOM coupling with denitrification; c, AOM coupling with metal
reduction.

2
J. Ding and R.J. Zeng
After the first discovery of DAMO process in the laboratory, it is
found that the amount of Methanosarcinales archaeon decreases with
enrichment time in subsequent upscaled enrichment culture and is no
longer detectable after incubation for 15 months (Ettwig et al., 2008).
The subsequent enrichment with only nitrite as electron acceptor con-
firms the DAMO activity of the NC10 phylum bacteria, showing that
the NC10 bacteria catalyze the anaerobic methane oxidation coupling
with nitrite reduction (Ettwig et al., 2009). The effects of nitrite and ni-
trate on DAMO microbes selection were then studied, and it was re-
vealed that the DAMO bacteria are more effective for nitrite reduction
than DAMO archaea (Hu et al., 2011). Henceforth, many studies have
been conducted on the DAMO bacteria, including the studies of labora-
tory enrichment and reactor performance (He et al., 2013; He et al.,
2015a; He et al., 2015c; He et al., 2015d; Hu et al., 2014a; Hu et al.,
2019; Jiang et al., 2018; Kampman et al., 2012; Kampman et al., 2018;
Luesken et al., 2011a; Luesken et al., 2011b; Ma et al., 2017), physiology
and metabolism (Ettwig et al., 2010; Guerrero-Cruz et al., 2019; Wu
et al., 2011; Wu et al., 2012a; Wu et al., 2015), primers design (Han
and Gu, 2013; He et al., 2016; Luesken et al., 2011c), and environmental
evaluation (Chen et al., 2015a; Chen et al., 2014; Chen et al., 2015b; Hu
et al., 2014b; Meng et al., 2016; Shen et al., 2015a; Shen et al., 2014a;
Shen et al., 2014b; Shen et al., 2014c; Wang et al., 2012; Yang et al.,
2017; Zhang et al., 2018). However, due to human activities such as
the generation of effluent from wastewater treatment plants (WWTP)
and agricultural runoff, nitrate becomes the main form of nitrogen ox-
ides in many natural environments (Ding et al., 2015). Despite the prev-
alence of nitrate in the natural environment, studies on the distribution
of DAMO archaea and on the significance of nitrate-DAMO process in
relevant environments have been scarce. Furthermore, since there is
less nitrite occurring in municipal and industrial wastewater, the
nitrate-DAMO is likely to be more significant than the nitrite-
dependent AOM in the actual wastewater treatment. Therefore, the
contributions of DAMO archaea and the nitrate-DAMO must be impor-
tant not only in the natural environment, but also in wastewater treat-
ment. Nevertheless, compared to the DAMO bacteria, the study of
DAMO archaeon has attracted less attention, possibly because com-
pared to DAMO bacteria, it is much more difficult to obtain enriched
DAMO archaea.
Investigations of DAMO bacteria have been summarized in several
review articles (Chen et al., 2016; He et al., 2018a; Shen et al., 2012;
Shen et al., 2015b), the potential of DAMO process in wastewater treat-
ment have also been discussed (van Kessel et al., 2018; Wang et al.,
2017a), and there is a publication introducing both the nitrate- and
nitrite-dependent anaerobic oxidation of methane (Welte et al., 2016).
However, more reviews especially targeting the DAMO archaea are
needed and meaningful. Therefore, the objective of this article is to sum-
marize the status of research on DAMO archaea and nitrate-dependent
anaerobic methane oxidation with regard to the following aspects: i.
laboratory enrichment; ii. environmental distribution; iii. metabolism
and environmental significance, in order to highlight the importance
of DAMO archaea. Some hypotheses and directions for future research
on DAMO archaea, ANME archaea, and even anaerobically metabolizing
archaea are also discussed.
2. Laboratory enrichment
2.1. Inocula
Obtaining a highly enriched DAMO culture is vital for DAMO studies
and inevitably requires a very long time. The selection of an appropriate
inoculum is highly important for the successful culture enrichment. Var-
ious inocula are used in DAMO bacteria enrichment such as sediments
from the ditches of agricultural land drainage (Ettwig et al., 2009;
Kampman et al., 2012), WWTP sludge (Luesken et al., 2011b), soil of
the peatland infiltrated with nitrate-enriched groundwater (Zhu et al.,
2012), and coastal sediment (He et al., 2015b). The effects of inoculum
3
Science of the Total Environment 757 (2021) 143928
on DAMO bacteria enrichment have been tested, and paddy field sam-
ples are considered to be excellent inocula for DAMO bacteria enrich-
ment that were superior to methanogenic sludge and freshwater
sediment, according to the results of DAMO activity test and molecular
detection (He et al., 2015a). Even though it has not been evaluated,
the choice of an appropriate inoculum should also be highly important
for enriching the mixed DAMO culture containing both DAMO archaea
and bacteria. The first mixed DAMO culture is enriched from the inocu-
lum of anoxic sediment taken from a canal, the total denitrification rate
of which is 28.8 ± 2 μmol N2 h−1 (part of the rate is caused by organic
compounds) (Raghoebarsing et al., 2006). This canal is a freshwater
habitat receiving agriculture runoff that contains nitrate concentrations
of up to 1 mM and saturated methane. Then an enriched culture is ob-
tained with mixed inocula containing the sediments from a local fresh-
water lake, return sludge and anaerobic digester sludge from WWTP, in
which the denitrification rate in the 35 °C reactor after day 220 achieves
to 2.0 mmol L−1 NO− 3 day
−1
(Hu et al., 2009). Similarly, a DAMO co-
culture is enriched using methanogenic sludge mixed with activated
sludge obtained from the local WWTP (Ding et al., 2014). They observed
DAMO activity after about 5 months' enrichment, and found that the ob-
tained mixed culture contained not only DAMO microbes, but also
anammox bacteria; the highest rate of nitrate reduction in the culture
is 4.84 mmol L−1 day−1, and the highest ammonium removal rate is
4.07 mmol L−1 day−1. The surface sediment of a local freshwater river
is also used for operating a hollow-fiber membrane biofilm reactor,
obtaining the maximal removal rates of nitrate and ammonium of
5.57 mmol L−1 day−1 and 1.86 mmol L−1 day−1 (Ding et al., 2017b).
Freshwater lake sediment, paddy soil, mixed with methanogenic sludge
from a local WWTP have been used as inocula to enrich DAMO culture
for the removal of nitrate with methane as the electron donor; the nitro-
gen removal rate of about 1.57 mmol NO− 3 L
−1
day−1 is obtained that is
considered as the highest rate observed in the literatures under the
same conditions (Li et al., 2018). Moreover, mixed inocula including
river sediment from Hangzhou of China, activated sludge and digested
sludge from the Qige WWTP have also been used in a DAMO reactor,
to study the short- and long-term effects of nitrite on DAMO organisms
(Lou et al., 2019). In sum up, it can be seen that mixed inocula are often
used in DAMO enrichment in order to provide more potential original
microbial sources for the reactor start-up. And the nitrate removal
rates in above cultures are different in some extent, but all in the milli-
molar level. This difference in DAMO enrichment may be partly caused
by the operation conditions; and may also be caused by the original in-
oculum, which actually have not been intensively studied and con-
cluded. The effects of the inoculum types on the culture enrichment
may depend on the nitrogen and carbon contents in the sampling
sites, and also on the soil and sediment properties such as temperature,
pH, salinity, dissolved oxygen, and even water moisture content and po-
rosity; the original microbial composition in the inoculum should also
affect the enrichment culture. Therefore, in addition to the above-
mentioned work, detailed studies should be conducted in future re-
search to precisely identify the effects and reasons of the inoculum
type on DAMO culture enrichment. The inocula used to enrich the
DAMO culture are summarized in Table 1.
2.2. Enrichment parameters
2.2.1. Temperature
In addition to inoculum selection, appropriate enrichment parame-
ters are also highly important for DAMO culture enrichment. The first
co-culture containing both DAMO archaea and DAMO bacteria is ob-
tained at temperature of 25 °C (Raghoebarsing et al., 2006). Afterwards,
the enrichment temperature is modified to 30 °C, leading to the disap-
pearance of DAMO archaea and sole catalysis of DAMO bacteria in the
system (Ettwig et al., 2008). For cultures that only contain DAMO bacte-
ria, most of the subsequent enrichments are carried out at approxi-
mately 30 °C (Ettwig et al., 2009; He et al., 2015a; He et al., 2015c; Hu
J. Ding and R.J. Zeng Science of the Total Environment 757 (2021) 143928

Table 1 operational activities of nitrate-DAMO are evaluated from gradual

Inocula used to enrich DAMO microbes. cooling (30–20 °C) to ambient temperatures (13–38 °C) (Li et al.,
Inoculum Enriched microbes References 2020). Under the stepwise cooling conditions (from 30 to 20 °C),
Anoxic canal sediment DAMO archaea and Raghoebarsing
DAMO activity is inhibited firstly, but then be adjusted rapidly and
DAMO bacteria et al. (2006) shows similar level at 20 and 30 °C. However, under ambient tempera-
Mixed inocula: freshwater lake DAMO archaea and Hu et al. (2009) ture conditions (13–38 °C, 230 days), the nitrate removal rate at the end
sediments, anaerobic digester DAMO bacteria of the test is clearly lower than that at the beginning of the test, and the
sludge, and return sludge
DAMO archaea abundantly enriched in the stepwise cooling tempera-
Mixed inocula: methanogenic DAMO archaea, DAMO Ding et al. (2014)
sludge and activated sludge bacteria, and anammox ture condition disappear after operation at ambient temperature for a
bacteria long time. It is concluded that the long-term temperature fluctuation in-
Surface sediment from a local DAMO archaea, DAMO Ding et al. (2017b) hibit the DAMO activity irreversibly. Similarly, tolerance of the DAMO
freshwater river bacteria, and anammox co-culture to temperatures as low as 10 °C is also observed; the total ni-
bacteria
Mixed inocula: freshwater lake DAMO archaea and Li et al. (2018)
trogen removal efficiency maintained at 90–94% during the tempera-
sediment, paddy soil, DAMO bacteria ture decrease from 25 to 10 °C (Liu et al., 2020b). Thus, the survey of
methanogenic sludge the literature shows that the temperature is mostly controlled at
Mixed inocula: river sediment, DAMO archaea and Lou et al. (2019) 30–35 °C in laboratory studies, but operation at lower temperature
activated sludge, and digested DAMO bacteria
around 20 °C and even 10 °C is also feasible, and can be economic if
sludge from WWTP
Sediments from ditche draining DAMO bacteria Ettwig et al. adopted in practical use.
agricultural land (2009); Kampman On the whole, it seems that DAMO bacteria are mesophilic and often
et al. (2012) enriched at ambient temperature. Comparatively, it is known that ar-
WWTP sludges DAMO bacteria Luesken et al. chaea are often found living in various extreme natural environments,
(2011b)
such as hot springs, salt lakes, strong acid/alkaline conditions, etc.
Peatland DAMO bacteria Zhu et al. (2012)
Coastal sediment DAMO bacteria He et al. (2015b) DAMO archaea are mostly enriched at medium temperature in labora-
Methanogenic sludge DAMO bacteria He et al. (2015a) tory studies, but operation at low temperature is also feasible, providing
Paddy soil DAMO bacteria He et al. (2015a) a potential that DAMO archaea may also be active in some disadvan-
Freshwater sediment DAMO bacteria He et al. (2015a)
taged conditions (not only the low temperature), which expands the
environmental significance and application potential of DAMO archaea
and the nitrate-dependent DAMO process. However, deeper studies of
et al., 2014a; Jiang et al., 2018; Kampman et al., 2012; Kampman et al., the effects of temperature on the physiology of DAMO microbes,
2018; Wang et al., 2019b), but in some cases they are also carried out nitrate-DAMO activity, and the competition between DAMO archaea
at 20–25 °C (He et al., 2015b; Luesken et al., 2011b; Zhu et al., 2012). and DAMO bacteria should be conducted. The temperatures used in
The short- and long-term effects of environmental conditions on the studies on enrichment of DAMO culture performed to date are sum-
DAMO bacteria enrichment are also evaluated (He et al., 2015d). The ef- marized in Table 2.
fects of different temperatures (15, 20, 25, 30, 35, 40 and 45 °C) on the
nitrite-dependent DAMO activity are investigated, and it is found that 2.2.2. pH value
with increasing temperature the DAMO activity first increases at the The first co-culture containing both DAMO archaea and DAMO bac-
temperatures below 35 °C, and then decreases at the temperatures teria is obtained with pH between 7.0 and 7.5 (Raghoebarsing et al.,
higher than 35 °C. Combining with the results of long-term experi- 2006). Then in the adjacent study, the pH value is modified to 7.3–7.6,
ments, the optimum temperature is identified as 35 °C, which shows in which the DAMO archaea disappear and only DAMO bacteria function
that DAMO bacteria are mesophilic. in the system (Ettwig et al., 2008). The effects of different pH values (6.0,
However, for the co-culture including both DAMO archaea and 6.5, 7.0, 7.5, 8.0, 8.5 and 9.0) on the nitrite-dependent DAMO activity are
DAMO bacteria, detailed investigations about the effects of environmen- also investigated, and it is found that with increasing pH, the DAMO ac-
tal factors on the microbial culture and DAMO activity have not been tivity first increases when pH lower than 7.5, and then decreases when
carried out, even though such studies are also needed. The DAMO co- pH higher than 7.5. The optimum pH is identified as approximately 7.6
culture is once attempted to be enriched under the temperatures of when combining the long-term experiments results. And actually, the
35 °C and 22 °C, and it is found that the 35 °C enrichment contains literature survey shows that pH is almost fixed at approximately 7.5 in
both DAMO archaea and DAMO bacteria, while the 22 °C enrichment all DAMO enrichments, and it can be shown that DAMO bacteria may
contains only DAMO bacteria but no DAMO archaea, suggesting that be favored in weakly alkaline conditions. However, for the co-culture in-
high temperature may be favorable for the enrichment of archaea- cluding both DAMO archaea and DAMO bacteria, detailed investigations
containing DAMO cultures (Hu et al., 2009). This suggestion seems to of the effects of pH value on the microbial culture and DAMO activity
be contradictory with the previous finding that the DAMO archaea ob- have not been carried out, and relevant studies should be conducted.
tained at 25 °C disappear when temperature is increased to 30 °C But similar to the effects of temperature mentioned above, DAMO ar-
(Ettwig et al., 2008). But it needs to be noticed that the enrichment con- chaea may also be active in some disadvantaged conditions with not
ditions between these two studies are different not only in temperature, suitable pH values, which should be investigated in future. The pH
but also in the pH value and inoculums. Therefore, this kind of contra- values used in enrichment of DAMO culture are also summarized in
diction can be acceptable, and further leading to specific studies about Table 2.
effects of temperature on DAMO archaea very needed to be conducted.
In the subsequent studies, co-culture enrichments are also carried out at 2.2.3. Medium component
35 °C (Ding et al., 2014; Hu et al., 2015). But in another study, two reac- Trace element is important for microbial growth, as well as the
tors with different temperatures are conducted, one of which is main- DAMO microbes. The trace element contents in the culture medium
tained at 30 °C and the other is adjusted from 22 to 30 °C after are modified to improve the nitrite-dependent DAMO activity (He
144 days, to explore the effects of the temperature change on the et al., 2015c). Significant stimulation on the activity and growth of
mixed DAMO culture (Li et al., 2018). Temperature is found to signifi- DAMO bacteria is observed at Fe(II) and Cu(II) concentrations of 20
cantly affect the system performance, and 30 °C is considered to be and 10 μmol·L−1, respectively, while no significant effect is observed
more suitable for the enrichment, and the number of DAMO archaea is with other trace metal elements (Zn, Mo, Co, Mn, Ni) in the tested con-
higher than that of DAMO bacteria. Moreover, the long-term centration ranges. The short- and long-term effects of the growth factors

4
J. Ding and R.J. Zeng Science of the Total Environment 757 (2021) 143928

Table 2
Temperatures and pH used for DAMO culture enrichment.

Temperature pH Enriched microbes References

25 °C 7.0–7.5a DAMO archaea and DAMO bacteria Raghoebarsing et al. (2006)

30 °C 7.3–7.6a DAMO bacteria Ettwig et al. (2008)
30 °C 6.9–7.5a DAMO bacteria Ettwig et al. (2009)
30 °C 7.3–7.6a DAMO bacteria and anammox bacteria Luesken et al. (2011a)
20–23 °C 6.8–7.3a DAMO bacteria Luesken et al. (2011b)
30 ± 1 °C 7.0–8.0a DAMO bacteria Kampman et al. (2012)
25 °C 6.0–6.2a DAMO bacteria Zhu et al. (2012)
30 ± 0.5 °C 7.0–7.2b DAMO bacteria Hu et al. (2014a)
30 ± 1 °C 7.0–7.2b DAMO bacteria He et al. (2015a)
25 °C 7.00 ± 0.01b DAMO bacteria He et al. (2015b)
30 °C 7.3–7.5b DAMO bacteria He et al. (2015c)
30 ± 0.3 °C N DAMO bacteria and methanogenic bacteria Jiang et al. (2018)
30 °C N DAMO bacteria Kampman et al. (2018)
30 °C 7.2–7.6 DAMO bacteria Wang et al. (2019b)
35 °C N DAMO archaea and DAMO bacteria Hu et al. (2009)
22 °C N DAMO bacteria Hu et al. (2009)
35 °C 7.0–8.5a DAMO archaea, DAMO bacteria, and anammox bacteria Ding et al. (2014)
35 °C 7.0–7.5a DAMO archaea, DAMO bacteria, and anammox bacteria Hu et al. (2015)
30 °C 7.0–7.5 DAMO archaea and DAMO bacteria Li et al. (2018)
a
pH of the culture.
b
pH of the influent medium; N, not mentioned in the reference.

including vitamin, heme, nucleobase, and betaine on DAMO bacteria are
investigated, and the results indicate that DAMO activity is significantly
stimulated by nucleobase and betaine instead of vitamin and heme in
the tested concentration ranges (Wang et al., 2019b). The impacts of in-
fluent COD on the reactor performance are evaluated, and the anaerobic
methane oxidation is also nitrite-dependent (Wu and Zhang, 2017). It is
observed that the reactor performance is not reduced by influent COD at
the C/N ratios less than 0.1, but it is necessary to increase the oxygen
transfer coefficient at high C/N ratios to achieve high performance.
The effects of oxygen on DAMO bacteria are also evaluated (Kampman
et al., 2018; Luesken et al., 2012). It is found that the addition of either
2% or 8% oxygen reduce the conversion rates of methane and nitrite im-
mediately (Luesken et al., 2012), while lower oxygen concentration at
0.7% and 1.1% increase the methane and nitrite consumption rates,
with the oxygen concentration of 1.1% leading to an obvious increase
in the rate (Kampman et al., 2018). The use of activated carbon and ap-
plication of high static pressure is also investigated in the nitrite-
dependent DAMO system; the methane transfer and methane adsorp-
tion capacity are increased, which facilitate the methane supply to
DAMO bacteria (Hu et al., 2019).
Similarly, much less research attention has been devoted to the
nitrate-DAMO process and DAMO archaea. The DAMO archaea is
attempted to be decoupled from DAMO bacteria with a microbial fuel
cell, in order to enable the study of the DAMO archaeal physiology
(Ding et al., 2017a). The effects of nitrogen sources on the enrichment
of DAMO co-culture and anammox bacteria are also studied (Fu et al.,
2017b). DAMO archaea are not enriched under the nitrate or nitrate/
ammonium conditions, which is unexpected and may be due to the
low content of DAMO archaea in the inocula. The addition of both nitrite
and ammonium seems to shorten the doubling time of DAMO bacteria
but prolong the doubling time of anammox bacteria. Besides, it is
found that the DAMO bacteria enriched under nitrate conditions are dif-
ferent from those enriched under nitrite conditions, and the authors
conclude that the effects of nitrogen source are more complex than ex-
pected. Iron content is confirmed to be a key factor for the competition
between the anammox and DAMO processes (Lu et al., 2018). In short-
term tests, the activity of DAMO archaea, DAMO bacteria, and anammox
bacteria could be obviously stimulated at iron concentrations of 80, 20,
and 80 μM, respectively. However, in long-term incubation, the high
iron concentration of 160 μM remarkably increases the DAMO archaeal
abundance, and DAMO bacteria are out-competed by anammox bacte-
ria under this iron concentration. Granular active carbon is also applied
in a nitrate-DAMO reactor, leading to increases in the nitrate removal
rate and the amount of DAMO microbes (both DAMO archaea and
DAMO bacteria), which may be due to the absorption of methane and
adherence of the microorganisms enabled by the porous structure of
granular active carbon that increases the amount of the microorganisms
and enhances the metabolic activity (Lu et al., 2020). Since the DAMO
microorganisms (particularly the DAMO archaea) are sensitive to envi-
ronmental conditions, appropriate environmental parameters are
highly significant for culture enrichment. The alternative carbon source
in the medium can obviously affect the methane consumption; nitrogen
sources may have selection effects on the enriched microorganisms,
thus appropriate combination of nitrogen sources may lead to optimal
methane and nitrogen removal effect; different microorganisms have
different requirements on the content of trace elements, so it is neces-
sary to further optimize the content of various trace elements in the cul-
ture medium to make both DAMO archaea and DAMO bacteria showing
high metabolic activity. However, environmental factors other than
temperature and pH have been rarely studied in DAMO reactors, and
particularly in the co-culture enrichment. Therefore, the effects of
other environmental factors such as dissolved oxygen, COD, and meth-
ane pressure on DAMO archaea and the nitrate-DAMO process should
be studied in future.
3. Environmental distribution
The distribution of DAMO bacteria in the environment has been
studied intensively, and DAMO bacteria have been observed in freshwa-
ter (Kojima et al., 2012; Shen et al., 2014b; Shen et al., 2016c; Yan et al.,
2015), paddy fields (Shen et al., 2014a; Shen et al., 2016b; Wang et al.,
2012; Zhou et al., 2014), wetland (Chen et al., 2015b; Hu et al., 2014b;
Shen et al., 2015a), saline water (Chen et al., 2015a; Chen et al., 2014;
Yang et al., 2012), estuaries (Shen et al., 2014c; Zhang et al., 2018),
and acidic forest soils (Meng et al., 2016). The wide environmental dis-
tribution indicates that DAMO bacteria contribute significantly to the
global carbon and nitrogen cycles. In addition to the existence evalua-
tion, the spatial and/or temporal distribution of DAMO bacteria in indi-
vidual ecosystems are also analyzed (Long et al., 2017a; Long et al.,
2017b; Wang et al., 2017b; Zhong et al., 2020). Compared to the numer-
ous publications on the environmental distribution of DAMO bacteria,
DAMO archaea have been much less studied. Specific 16s rRNA primers
are designed and used for DAMO archaea detection in several ecosys-
tems, namely one river sediment, two lake sediments, and one paddy

5
J. Ding and R.J. Zeng Science of the Total Environment 757 (2021) 143928

field soil (Ding et al., 2015). This represents the first primer design study Table 3
for DAMO archaea since the first discovery of DAMO. The coexistence of Natural ecosystems in which DAMO archaea and/or DAMO bacteria have been discovered.

DAMO bacteria and DAMO archaea is evaluated and confirmed in a Ecosystem Detected microbes References
paddy field (Ding et al., 2016a). This work is also the first report on River DAMO bacteria Hu et al. (2012); Long et al. (2017a);
the coexistence of DAMO bacteria and DAMO archaea in a natural eco- Shen et al. (2014b); Yan et al. (2015)
system. Following these studies, the DAMO archaea are also discovered Riverbed DAMO bacteria and Shen et al. (2019)
in an Italian paddy field together with the NC10 phylum bacteria anammox bacteria
Lake DAMO bacteria Kojima et al. (2012); Wang et al.
(Vaksmaa et al., 2016). Subsequently, Vaksmaa et al. designed another
(2017c)
two pairs of primers for DAMO archaea based on the mcrA gene, and Lake DAMO bacteria and Yang et al. (2012)
compared the quantities and phylogeny of DAMO archaea in six envi- anammox bacteria
ronmental samples (Vaksmaa et al., 2017). Besides, the community Wetland DAMO bacteria Chen et al. (2015b); Hu et al.
structure, quantity and activity of DAMO archaea and bacteria are inves- (2014b); Shen et al. (2015a); Yang
et al. (2017); Zhu et al. (2015)
tigated in an intertidal zone, by which both the nitrate-AOM and nitrite- Paddy field DAMO bacteria Shen et al. (2016b); Zhou et al. (2014)
AOM are found active with approximate methane oxidation rates Paddy field DAMO bacteria and Shen et al. (2014a); Wang et al.
(Wang et al., 2019a). The biodiversity, abundance, and activity of anammox bacteria (2012)
DAMO bacteria and DAMO archaea are also studied in intertidal marsh Peatland DAMO bacteria Zhong et al. (2020)
Forest DAMO bacteria and Meng et al. (2016)
soil cores, finding a higher biodiversity of DAMO archaea compared
anammox bacteria
with DAMO bacteria, and the nitrate-AOM activity is slightly higher Coastal area DAMO bacteria Chen et al. (2015a); Chen et al.
than the nitrite-AOM (Zheng et al., 2020). Additionally, the coexistence (2014); Shen et al. (2016a); Wang
of DAMO bacteria and DAMO archaea is also observed in intertidal et al. (2017b)
marsh sediments, and the biodiversity of DAMO archaea is shown to Estuary DAMO bacteria Shen et al. (2014c); Zhang et al.
(2018)
be higher than that of the DAMO bacteria, and DAMO archaea also
Reservoir DAMO bacteria Long et al. (2017b); Wang et al.
show slightly higher activity than DAMO bacteria, indicating the impor- (2016)
tance of DAMO process in methane and nitrate sinks in intertidal River DAMO archaea and Ding et al. (2015)
marshes (Chen et al., 2020). Therefore, in the above intertidal zones, DAMO bacteria
Lake DAMO archaea and Ding et al. (2015)
DAMO archaea seems have higher diversity and activity than DAMO
DAMO bacteria
bacteria, probably illustrating more significant contribution of DAMO Paddy soil DAMO archaea and Ding et al. (2015); Vaksmaa et al.
archaea in this type of ecosystem than DAMO bacteria. However, the DAMO bacteria (2016)
relative contribution of DAMO archaea and DAMO bacteria to methane Paddy field DAMO archaea, Ding et al. (2016a)
oxidation in other natural habitats should also be studied, to more com- DAMO bacteria,
anammox bacteria
prehensively understand their significance and contribution in the nat-
Rice field soils DAMO archaea Vaksmaa et al. (2017)
ural environment. Four microbial nitrate reduction processes Brewery WWTP
(denitrification, anammox, DAMO, DNRA) are explored in fine-scale ri- sludge
parian soil horizons, but no detectable DAMO activity is found (Wang North Sea sediment
Polluted Citarum
et al., 2020). The community diversity and abundance of DAMO archaea
River sediment
in sewage sludge from two WWTPs are also explored, and it confirms Jordan River sedi-
the presence of diverse M. nitroreducens-like archaea in the sludge, ment State Channel
which may be the basis for future application of DAMO archaea in nitro- sediment
gen removal in WWTPs (Xu et al., 2020). Overall, it can be seen that WWTP sludge DAMO archaea Xu et al. (2020)
Marsh sediments DAMO archaea and Chen et al. (2020)
much remains unknown about DAMO archaea and the catalyzed
DAMO bacteria
nitrate-DAMO process in natural environments. Therefore, further envi-
ronmental investigations of DAMO archaea should be conducted in
order to more comprehensively reveal the contribution of DAMO pro-
cess to the global carbon and nitrogen cycles. The existence of DAMO ar- comply with its slow metabolism (Wu et al., 2012b). An apparent μmax
chaea and/or DAMO bacteria in natural ecosystems is summarized in of 0.14 d−1 and corresponding doubling time of 5 days are estimated,
Table 3. which is different with the previous thought of 2–8 weeks; and the ap-
parent affinity constant of DAMO bacteria for methane is estimated to
4. Metabolism and the environmental significance 2.6 ± 0.7 μM, which is comparable to the affinity constant of aerobic
methane oxidizers (0.2 to 6 μM) (Guerrero-Cruz et al., 2019). For the
4.1. Metabolism and physiology of DAMO archaea DAMO archaea, the “reverse methanogenesis” pathway is confirmed
by metagenomic and metatranscriptomic analyses; the genes for nitrate
The DAMO bacteria are found to catalyze the nitrite-dependent an- reduction but not for the subsequent denitrification steps are identified
aerobic methane oxidation process through an intra-aerobic pathway in the genome, indicating that the DAMO archaea cannot reduce the
(Ettwig et al., 2010); oxygen is produced in NO dismutation, and then produced nitrite further to NO, N2O or N2 (Haroon et al., 2013). There-
is used to hydroxylate methane in the function of particulate methane fore, not only in the reactor enrichment culture, but also in the natural
mono-oxygenase (pMMO), producing methanol and water. In addition habitat, DAMO archaea need a partner to further reduce the produced
to the metabolism, the ultrastructure and physiological properties in- nitrite to the final nitrogen product. This is why DAMO bacteria always
cluding growth rate, doubling time, and methane/nitrite affinities coexist with DAMO archaea in the co-culture when nitrate is supplied as
have also been revealed (Guerrero-Cruz et al., 2019; Wu et al., 2012b). the electron acceptor. However, in addition to the DAMO bacteria,
DAMO bacterium is observed ultrastructurally distinct from other bac- anammox bacteria can also be the partner of DAMO archaea. Thus, the
teria by its atypical cell shape, and the intracytoplasmic membranes joint contribution of DAMO archaea, DAMO bacteria, and anammox bac-
(ICMs) which are common in classical proteobacterial methanotrophs teria to the total nitrogen removal has been often studied (Ding et al.,
are not observed in its cell (Wu et al., 2012b). One possible explanation 2014; Ding et al., 2017b; Fan et al., 2019; Fu et al., 2017a; Liu et al.,
for the lack of ICMs is that it is energetically disadvantageous for DAMO 2020a; Liu et al., 2020b; Nie et al., 2020). And even partial nitritation
bacteria to produce ICMs, because DAMO bacteria metabolize slowly, is simultaneously combined with anammox and nitrite/nitrate-
the ICMs production requires much energy investment that does not dependent anaerobic methane oxidation to obtain high-level nitrogen

6
J. Ding and R.J. Zeng
removal (Liu et al., 2019). Besides, the nitrate reductase shows an ex-
tremely unusual subunit composition that has not been observed in
other prokaryotes (Arshad et al., 2015). However, it is later found that
DAMO archaea can transform a small part of the produced nitrite to am-
monium, preventing nitrite accumulation and the caused toxicity; the
corresponding enzyme is NrfAH-like protein complex, of which 10% of
the produced nitrite can be reduced to ammonium (Ettwig et al., 2016).
The most popularly studied enzyme for DAMO archaea is the
methyl-coenzyme M reductase (MCR) that is originally identified as
an important enzyme in methanogens catalyzing the final step of meth-
ane production and in all ANME archaea acting to catalyze the first step
of methane oxidation (Shima and Thauer, 2005). The mcrA gene en-
codes the alpha subunit of the MCR enzyme and is used as a biomarker
for ANME archaea. In DAMO archaea, all of the functional genes
(mcrABCDG) are identified in the genome, indicating that the mcrA
gene may also be used as a biomarker for DAMO archaea, and can be
used to detect DAMO archaea in enriched and environmental cultures.
The methane and nitrate metabolism of DAMO archaea is shown in
Fig. 2. The ultrastructure of the enrichment co-culture containing both
DAMO archaea and DAMO bacteria is investigated, and the
Methanoperedens sp. (DAMO archaea) aggregates are found to consist
of slightly irregular coccoid cells with approximately 1.5 μm diameter
(Gambelli et al., 2018). The methane affinity of DAMO archaea is esti-
mated at 0.5 mM (Lu et al., 2019), which is much higher than that of
DAMO bacteria; this difference in methane affinity can be due to that
DAMO bacteria use canonical pMMO, while DAMO archaea use MCR
to activate methane (Guerrero-Cruz et al., 2019). Furthermore, in addi-
tion to the DAMO activity, other metabolic abilities of DAMO archaea are
also evaluated in several studies. The DAMO archaea are confirmed to be
unable to reverse its metabolic pathway to produce methane (Ding
et al., 2016b), and the nitrate-DAMO culture is also used to carry out
chromium and selenium reduction coupling with AOM (Lu et al.,
2016; Luo et al., 2018; Luo et al., 2019). Furthermore, humic substances
are also found as electron shuttles that fuel the anaerobic methane oxi-
dation in wetland sediments, and CO2 produced in AOM can be buried
into wetland sediments by the collateral promotion of humic sub-
stances (Valenzuela et al., 2019). However, overall, further studies of
the physiology and enzymes other than MCR of DAMO archaea are
still necessary.
4.2. Other potential pathways in ecosystems
As mentioned above, the nitrite-dependent DAMO process has been
discovered in many ecosystems, indicating the significant contribution
of this process to the global carbon and nitrogen cycle. By contrast,
few relevant environmental studies have been carried out for DAMO
Reverse methanogenesis
mcrABCDG
CH4 Methyl-S-CoM CO2
DAMO
archaea
narGH
NO3- NO2- h NO/N2O/N2
NrfAH
10%
NH4+
Fig. 2. Methane and nitrate metabolism in DAMO archaea.
7
Science of the Total Environment 757 (2021) 143928
archaea, even though its contributions to the global carbon and nitrogen
cycles should also be significant. In addition to the conventional contri-
bution through the DAMO process, some other pathways may also exist
in the natural ecosystems and should be evaluated such as
methanogenesis, anaerobic alkane oxidation, and selenate/chromium
reduction with DAMO culture.
Because ANME archaea are considered to oxidize methane anaerobi-
cally through “reverse methanogenesis”, they may have the potential to
reverse their metabolic pathway to produce methane, which will affect
their participation in the global carbon cycle. This metabolic reversibility
of DAMO archaea has been evaluated with a laboratory culture, while
the enriched DAMO archaea are shown to lack the methanogenic capa-
bility (Ding et al., 2016b). However, in situ studies in natural ecosystems
should be conducted in the future because the natural DAMO archaea
may have different ecological abilities with the enriched culture. Re-
cently, the anaerobic ethane oxidation coupling with sulfate reduction
is discovered in a laboratory reactor which has been operated for ten
years (Chen et al., 2019). Candidatus Argoarchaeum ethanivorans is
found as the dominant archaea in the enriched culture, and ethane ox-
idation is evidenced to be initiated by MCR to form ethyl-coenzyme M
(ethyl-CoM). This discovery triggers interest in the versatility of MCR
for the activation of the non-methane alkanes oxidation by ANME ar-
chaea. If true, this phenomenon will further expand our understanding
about ANME archaea regarding its physiology and environmental role.
Preliminary evaluation on the ability of DAMO archaea about anaerobic
ethane oxidation has been conducted in the laboratory condition, and it
is shown that the DAMO archaea could not oxidize ethane anaerobically
(Ding et al., 2020). Therefore, without evolution or adaptation in corre-
sponding environment, the original MCR in DAMO archaea may not be
used to oxidize ethane. This is the first report evaluating the DAMO ar-
chaea and even ANME archaea about their ability in oxidizing the non-
methane gaseous alkanes. However, as mentioned above, the capability
of DAMO archaea about other alkanes oxidation as well as the selenate/
chromium reduction coupling with AOM should be further evaluated in
future studies in natural ecosystems. The methane and ethane activa-
tion in corresponding microbes is shown in Fig. 3.
4.3. Speculations about various archaea conducting anaerobic metabolism
As mentioned above, there are several kinds of electron acceptors for
anaerobic methane oxidation, namely sulfate, nitrite/nitrate, Fe(III), Mn
(IV), and Se(VI) (Beal et al., 2009; Luo et al., 2018). It is well known that
DAMO bacteria can conduct nitrite-dependent DAMO process alone,
and it is mentioned above that in some cases ANME archaea can oxidize
methane solely and transfer electrons directly to metal compound (in
other cases, ANME archaea may be associated with metal-AOM together
with metal-reducing bacteria); while except these, other electron ac-
ceptors shall be reduced in the cooperation of both ANME archaea and
a bacterial partner. Sulfate-AOM was considered to be conducted by
ANME-1, 2a, 2b, 2c, 3 and SRB (Knittel and Boetius, 2009); nitrate-
AOM is conducted by ANME-2d, and M. oxyfera/anammox bacteria is
needed to further consume the produced nitrite. Moreover, DAMO ar-
chaea are also suggested to conduct Fe-AOM and Se-AOM (Fu et al.,
2016; Luo et al., 2018). The phylogenetic relationship of these ANME ar-
chaea is shown in Fig. 4. It is thus interesting about the boundary among
all of these archaea, based on their metabolic function rather than on the
basis of phylogeny. It is also interesting to determine whether certain
archaea can conduct AOM process with all of the above-mentioned elec-
tron acceptors when appropriate bacteria partners are available in the
environment (Fig. 5a).
The anaerobic ethane oxidation has also been discussed above, cou-
pling with sulfate reduction which is catalyzed by SRB. The difference
between this process and SAMO lies in the identity of the electron
donor. Even though DAMO archaea in the laboratory enrichment is con-
sidered impossible to conduct ethane oxidation, it is still interesting that
whether certain archaea can conduct both AOM and alkane oxidation
J. Ding and R.J. Zeng Science of the Total Environment 757 (2021) 143928

Fig. 3. Methane and ethane activation in corresponding microbes.

coupling with sulfate reduction (Fig. 5b). Additionally, it is even won-
dered that whether certain archaea can conduct both AOM and alkane
oxidation with various electron acceptors (Fig. 5c). All of these conjec-
tures and expectations make the studies of DAMO archaea, ANME ar-
chaea, and even anaerobically metabolizing archaea interesting and
important.
5. Conclusions
Since the discovery of DAMO process, many aspects of DAMO
bacteria have been explored while less attention has been devoted to
DAMO archaea. It has been found that appropriate inocula and enrich-
ment parameters are important for the culture enrichment and the

ANME-2a (AJ578088, AJ578107, AM745257, AY211687)

ANME-2b (AB461391, AF354128, AF354140)
ANME-2c (AF354131, AJ578096, AJ578117, AM745229)
Methanomethylovorans (AB161327, AF120163)
ANME-3 (AF354136, AJ578119, AY299515)
ANME-2d (DQ369741, FJ907179, FJ907180, KC539773, KJ573133)
Methanosaeta (AJ133791, AY835417, M59146)
ANME-1 (AF354126, AF354137, AF419624, AJ578084, AJ578136)

0.02

Fig. 4. The phylogenetic relationship of the ANME archaea and methanogens.

8
J. Ding and R.J. Zeng
Fig. 5. Conjecture regarding some types of versatile archaea. a, Archaea conducting AOM with various electron acceptors; b, Archaea conducting both AOM and anaerobic alkane oxidation
coupling with sulfate reduction; c, Archaea conducting both AOM and anaerobic alkane oxidation with various electron acceptors.
subsequent DAMO activity. By contrast, there have been relatively few
studies on the environmental evaluation and physiological metabolism
of DAMO archaea, which should be explored in future. Moreover, as
more new AOM processes are discovered, it will be interesting to
investigate the conjecture that certain archaea display versatile func-
tions by using various electron donors coupling with various electron
acceptors.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgment
The authors would like to acknowledge the financial support from
the National Natural Science Foundation of China (41807413,
51178444). Jiangsu Provincial Natural Science Foundation of China
(BK20180967), Jiangsu Provincial Natural Science Research Project
of Colleges and Universities (18KJB610018), Jiangsu Provincial Key
Laboratory of Environmental Science and Engineering (No.
Zd20170X), the Innovative and Entrepreneurial Doctor Program of
Jiangsu Province.
9
Science of the Total Environment 757 (2021) 143928
References
Arshad, A., Speth, D.R., de Graaf, R.M., Op den Camp, H.J.M., Jetten, M.S.M., Welte, C.U.,
2015. A metagenomics-based metabolic model of nitrate-dependent anaerobic oxi-
dation of methane by Methanoperedens-like archaea. Front. Microbiol. 6, 1423.
Beal, E.J., House C.H, Orphan, V.J., 2009. Manganese- and iron-dependent marine methane
oxidation. Science. 325 (5937), 184–187.
Cai, C., Leu, A.O., Xie, G.J., Guo, J.H., Feng, Y.X., Zhao, J.X., et al., 2018. A methanotrophic
archaeon couples anaerobic oxidation of methane to Fe(III) reduction. Isme J. 12,
1929–1939.
Chen, J., Zhou, Z.C., Gu, J.D., 2014. Occurrence and diversity of nitrite-dependent anaerobic
methane oxidation bacteria in the sediments of the South China Sea revealed by am-
plification of both 16S rRNA and pmoA genes. Appl. Microbiol. Biotechnol. 98 (12),
5685–5696.
Chen, J., Jiang, X.W., Gu, J.D., 2015a. Existence of novel phylotypes of nitrite-dependent
anaerobic methane-oxidizing bacteria in surface and subsurface sediments of the
South China Sea. Geomicrobiol J. 32 (1), 1–9.
Chen, J., Zhou, Z.C., Gu, J.D., 2015b. Complex community of nitrite-dependent anaerobic
methane oxidation bacteria in coastal sediments of the Mai Po wetland by PCR ampli-
fication of both 16S rRNA and pmoA genes. Appl. Microbiol. Biotechnol. 99 (3),
1463–1473.
Chen, J., Dick, R., Lin, J.G., Gu, J.D., 2016. Current advances in molecular methods for detec-
tion of nitrite-dependent anaerobic methane oxidizing bacteria in natural environ-
ments. Appl. Microbiol. Biotechnol. 100 (23), 9845–9860.
Chen, S.C., Musat, N., Lechtenfeld, O.J., Paschke, H., Schmidt, M., Said, N., et al., 2019. An-
aerobic oxidation of ethane by archaea from a marine hydrocarbon seep. Nature
568 (7750), 108–111.
Chen, F., Zheng, Y., Hou, L., Zhou, J., Yin, G., Liu, M., 2020. Denitrifying anaerobic methane
oxidation in marsh sediments of Chongming eastern intertidal flat. Mar. Pollut. Bull.
150, 110681.
J. Ding and R.J. Zeng
Ding, Z.W., Ding, J., Fu, L., Zhang, F., Zeng, R.J., 2014. Simultaneous enrichment of
denitrifying methanotrophs and anammox bacteria. Appl. Microbiol. Biotechnol. 98
(24), 10211–10221.
Ding J., Ding Z.W., Fu L., Lu Y.Z., Cheng S.H., Zeng R.J. 2015. New primers for detecting and
quantifying denitrifying anaerobic methane oxidation archaea in different ecological
niches. Appl. Microbiol. Biotechnol. 99(22). 99, 9805-9812.
Ding, J., Fu, L., Ding, Z.W., Lu, Y.Z., Cheng, S.H., Zeng, R.J., 2016a. Environmental evaluation
of coexistence of denitrifying anaerobic methane-oxidizing archaea and bacteria in a
paddy field. Appl. Microbiol. Biotechnol. 100 (1), 439–446.
Ding, J., Fu, L., Ding, Z.W., Lu, Y.Z., Cheng, S.H., Zeng, R.J., 2016b. Experimental evaluation of
the metabolic reversibility of ANME-2d between anaerobic methane oxidation and
methanogenesis. Appl. Microbiol. Biotechnol. 100 (14), 6481–6490.
Ding, J., Lu, Y.Z., Fu, L., Ding, Z.W., Mu, Y., Cheng, S.H., et al., 2017a. Decoupling of DAMO
archaea from DAMO bacteria in a methane-driven microbial fuel cell. Water Res.
110, 112–119.
Ding, Z.W., Lu, Y.Z., Fu, L., Ding, J., Zeng, R.J., 2017b. Simultaneous enrichment of
denitrifying anaerobic methane-oxidizing microorganisms and anammox bacteria
in a hollow-fiber membrane biofilm reactor. Appl. Microbiol. Biotechnol. 101 (1),
437–446.
Ding, J., Fu, L., Lu, Y.Z., Ding, Z.W., Zeng, R.J., 2020. Evaluation of anaerobic ethane oxida-
tion capability of the denitrifying anaerobic methane oxidation culture. Bioresour.
Technol. Rep. 10, 100418.
Ettwig, K.F., Shima, S., van de Pas-Schoonen, K.T., Kahnt, J., Medema, M.H., op den Camp
H.J.M., et al., 2008. Denitrifying bacteria anaerobically oxidize methane in the absence
of Archaea. Environ. Microbiol. 10 (11), 3164–3173.
Ettwig, K.F., van Alen, T., van de Pas-Schoonen, K.T., Jetten, M.S.M., Strous, M., 2009. En-
richment and molecular detection of denitrifying methanotrophic bacteria of the
NC10 phylum. Appl. Environ. Microbiol. 75 (11), 3656–3662.
Ettwig, K.F., Butler, M.K., Le Paslier, D., Pelletier, E., Mangenot, S., Kuypers, M.M.M., et al.,
2010. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464
(7288), 543–548.
Ettwig, K.F., Zhu, B., Speth, D., Keltjens, J.T., Jetten, M.S.M., Kartal, B., 2016. Archaea cata-
lyze iron-dependent anaerobic oxidation of methane. Proc. Natl. Acad. Sci. U. S. A.
113, 12792–12796.
Fan, S.Q., Xie, G.J., Lu, Y., Liu, B.F., Xing, D.F., Han, H.J., et al., 2019. Granular sludge coupling
nitrate/nitrite dependent anaerobic methane oxidation with anammox: from proof-
of-concept to high rate nitrogen removal. Environ. Sci. Technol. 54 (1), 297–305.
Fu, L., Li, S.W., Ding, Z.W., Ding, J., Lu, Y.Z., Zeng, R.J., 2016. Iron reduction in the DAMO/
Shewanella oneidensis MR-1 coculture system and the fate of Fe(II). Water Res. 88,
808–815.
Fu, L., Ding, J., Lu, Y.Z., Ding, Z.W., Zeng, R.J., 2017a. Nitrogen source effects on the
denitrifying anaerobic methane oxidation culture and anaerobic ammonium oxida-
tion bacteria enrichment process. Appl. Microbiol. Biotechnol. 101 (9), 3895–3906.
Fu, L., Ding, J., Lu, Y.Z., Ding, Z.W., Bai, Y.N., Zeng, R.J., 2017b. Hollow fiber membrane bio-
reactor affects microbial community and morphology of the DAMO and Anammox
co-culture system. Bioresour. Technol. 232, 247–253.
Gambelli L., Guerrero-Cruz S., Mesman R.J., Cremers G., Jetten M.S.M., Op den Camp H.J.M.,
et al. 2018. Community composition and ultrastructure of a nitrate-dependent anaero-
bic methane-oxidizing enrichment culture. Appl. Environ. Microbiol. 84(3), e02186-17.
Guerrero-Cruz S., Stultiens K., van Kessel M., Versantvoort W., Jetten M.S.M., Op den Camp
H.J.M., et al. 2019. Key physiology of a nitrite-dependent methane-oxidizing enrich-
ment culture. Appl. Environ. Microbiol. 85(8), e00124-19.
Han, P., Gu, J.D., 2013. A newly designed degenerate PCR primer based on pmoA gene for
detection of nitrite-dependent anaerobic methane-oxidizing bacteria from different
ecological niches. Appl. Microbiol. Biotechnol. 97 (23), 10155–10162.
Haroon, M.F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., et al., 2013. Anaerobic
oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature
500 (7464), 567–570.
He, Z.F., Cai, C., Geng, S., Lou, L.P., Xu, X.Y., Zheng, P., et al., 2013. Mdodeling a nitrite-
dependent anaerobic methane oxidation process: parameters identification and
model evaluation. Bioresour. Technol. 147, 315–320.
He, Z.F., Cai, C., Shen, L.D., Lou, L.P., Zheng, P., Xu, X.H., et al., 2015a. Effect of inoculum
sources on the enrichment of nitrite-dependent anaerobic methane-oxidizing bacte-
ria. Appl. Microbiol. Biotechnol. 99 (2), 939–946.
He, Z.F., Geng, S., Cai, C.Y., Liu, S., Liu, Y., Pan, Y.W., et al., 2015b. Anaerobic Oxidation of
Methane Coupled to Nitrite Reduction by Halophilic Marine NC10 Bacteria. Appl. En-
viron. Microbiol. 81 (16), 5538–5545.
He, Z.F., Geng, S., Pan, Y.W., Cai, C.Y., Wang, J.Q., Wang, L.Q., et al., 2015c. Improvement of
the trace metal composition of medium for nitrite-dependent anaerobic methane ox-
idation bacteria: Iron (II) and copper (II) make a difference. Water Res. 85, 235–243.
He, Z.F., Geng, S., Shen, L.D., Lou, L.P., Zheng, P., Xu, X.H., et al., 2015d. The short- and long-
term effects of environmental conditions on anaerobic methane oxidation coupled to
nitrite reduction. Water Res. 68, 554–562.
He, Z., Wang, J., Hu, J., Zhang, H., Cai, C., Shen, J., et al., 2016. Improved PCR primers to am-
plify 16S rRNA genes from NC10 bacteria. Appl. Microbiol. Biotechnol. 100 (11),
5099–5108.
He, Z.F., Feng, Y.D., Zhang, S.J., Wang, X.N., Wu, S.Y., Pan, X.L., 2018a. Oxygenic denitrifica-
tion for nitrogen removal with less greenhouse gas emissions: microbiology and po-
tential applications. Sci. Total Environ. 621, 453–464.
He, Z.F., Zhang, Q.Y., Feng, Y.D., Luo, H.W., Pan, X.L., Gadd, G.M., 2018b. Microbiological
and environmental significance of metal-dependent anaerobic oxidation of methane.
Sci. Total Environ. 610, 759–768.
Hu, S.H., Zeng, R.J., Burow, L.C., Lant, P., Keller, J., Yuan, Z.G., 2009. Enrichment of
denitrifying anaerobic methane oxidizing microorganisms. Environ. Microbiol. Rep.
1 (5), 377–384.
10
Science of the Total Environment 757 (2021) 143928
Hu, S.H., Zeng, R.J., Keller, J., Lant, P.A., Yuan, Z.G., 2011. Effect of nitrate and nitrite on the
selection of microorganisms in the denitrifying anaerobic methane oxidation process.
Environ. Microbiol. Rep. 3 (3), 315–319.
Hu, B.L., Shen, L.D., Zheng, P., Hu, A.H., Chen, T.T., Cai, C., et al., 2012. Distribution and di-
versity of anaerobic ammonium-oxidizing bacteria in the sediments of the Qiantang
River. Environ. Microbiol. Rep. 4 (5), 540–547.
Hu, B.L., He, Z.F., Geng, S., Cai, C., Lou, L.P., Zheng, P., et al., 2014a. Cultivation of nitrite-
dependent anaerobic methane-oxidizing bacteria: impact of reactor configuration.
Appl. Microbiol. Biotechnol. 98 (18), 7983–7991.
Hu, B.L., Shen, L.D., Lian, X., Zhu, Q., Liu, S., Huang, Q., et al., 2014b. Evidence for nitrite-
dependent anaerobic methane oxidation as a previously overlooked microbial meth-
ane sink in wetlands. Proc. Natl. Acad. Sci. U. S. A. 111 (12), 4495–4500.
Hu, S.H., Zeng, R.J., Haroon, M.F., Keller, J., Lant, P.A., Tyson, G.W., et al., 2015. A laboratory
investigation of interactions between denitrifying anaerobic methane oxidation
(DAMO) and anammox processes in anoxic environments. Sci. Rep. 5, 8706.
Hu, Z., Ru, D., Wang, Y., Zhang, J., Jiang, L., Xu, X., et al., 2019. Optimization of a nitrite-
dependent anaerobic methane oxidation (n-damo) process by enhancing methane
availability. Bioresour. Technol. 275, 101–108.
Jiang, L., Hu, Z., Wang, Y., Ru, D., Li, J., Fan, J., 2018. Effect of trace elements on the devel-
opment of co-cultured nitrite-dependent anaerobic methane oxidation and methan-
ogenic bacteria consortium. Bioresour. Technol. 268, 190–196.
Kampman, C., Hendrickx, T.L.G., Luesken, F.A., van Alen, T.A., Op den Camp, H.J.M., Jetten,
M.S.M., et al., 2012. Enrichment of denitrifying methanotrophic bacteria for applica-
tion after direct low-temperature anaerobic sewage treatment. J. Hazard. Mater.
227, 164–171.
Kampman, C., Piai, L., Temmink, H., Hendrickx, T.L.G., Zeeman, G., Buisman, C.J.N., 2018.
Effect of low concentrations of dissolved oxygen on the activity of denitrifying
methanotrophic bacteria. Water Sci. Technol. 77, 2589–2597.
van Kessel, M.A.H.J., Stultiens, K., Slegers, M.F.W., Cruz, S.G., Jetten, M.S.M., Kartal, B., et al.,
2018. Current perspectives on the application of N-damo and anammox in wastewa-
ter treatment. Curr. Opin. Biotech. 50, 222–227.
Knittel, K., Boetius, A., 2009. Anaerobic oxidation of methane: progress with an unknown
process. Annu. Rev. Microbiol. 63, 311–334.
Kojima, H., Tsutsumi, M., Ishikawa, K., Iwata, T., Mussmann, M., Fukui, M., 2012. Distribu-
tion of putative denitrifying methane oxidizing bacteria in sediment of a freshwater
lake. Lake Biwa. Syst. Appl. Microbiol. 35 (4), 233–238.
Leu, A.O., Cai, C., McIlroy, S.J., Southam, G., Orphan, V.J., Yuan, Z.G., et al., 2020. Anaerobic
methane oxidation coupled to manganese reduction by members of the
Methanoperedenaceae. Isme J. 14, 1030–1041.
Li, W., Lu, P., Chai, F., Zhang, L., Han, X., Zhang, D., 2018. Long-term nitrate removal
through methane-dependent denitrification microorganisms in sequencing batch re-
actors fed with only nitrate and methane. AMB Express 8 (18), 108.
Li, W., Lu, P., Zhang, L., Ding, A., Wang, X., Yang, H., et al., 2020. Long-term performance of
denitrifying anaerobic methane oxidation under stepwise cooling and ambient tem-
perature conditions. Sci. Total Environ. 713, 136739.
Liu, T., Hu, S., Yuan, Z., Guo, J., 2019. High-level nitrogen removal by simultaneous partial
nitritation, anammox and nitrite/nitrate-dependent anaerobic methane oxidation.
Water Res. 166, 115057.
Liu, T., Guo, J., Hu, S., Yuan, Z., 2020a. Model-based investigation of membrane biofilm re-
actors coupling anammox with nitrite/nitrate-dependent anaerobic methane oxida-
tion. Environ. Int. 137, 105501.
Liu, T., Khai, Lim Z., Chen, H., Hu, S., Yuan, Z., Guo, J., 2020b. Temperature-tolerated main-
stream nitrogen removal by Anammox and nitrite/nitrate-dependent anaerobic
methane oxidation in a membrane biofilm reactor. Environ. Sci. Technol. 54 (5),
3012–3021.
Long, Y., Jiang, X., Guo, Q., Li, B., Xie, S., 2017a. Sediment nitrite-dependent methane-
oxidizing microorganisms temporally and spatially shift in the Dongjiang River.
Appl. Microbiol. Biotechnol. 101, 401–410.
Long, Y., Liu, C., Lin, H., Li, N., Guo, Q., Xie, S., 2017b. Vertical and horizontal distribution of
sediment nitrite-dependent methane-oxidizing organisms in a mesotrophic freshwa-
ter reservoir. Can. J. Microbiol. 63 (6), 525–534.
Lou, J., Wang, X., Li, J., Han, J., 2019. The short- and long-term effects of nitrite on
denitrifying anaerobic methane oxidation (DAMO) organisms. Environ. Sci. Pollut.
Res. Int. 26 (5), 4777–4790.
Lu, Y.Z., Fu, L., Ding, J., Ding, Z.W., Li, N., Zeng, R.J., 2016. Cr(VI) reduction coupled with an-
aerobic oxidation of methane in a laboratory reactor. Water Res. 102, 445–452.
Lu, Y.Z., Fu, L., Li, N., Ding, J., Bai, Y.N., Samaras, P., et al., 2018. The content of trace element
iron is a key factor for competition between anaerobic ammonium oxidation and
methane-dependent denitrification processes. Chemosphere. 198, 370–376.
Lu, P., Liu, T., Ni, B.J., Guo, J., Yuan, Z., Hu, S., 2019. Growth kinetics of Candidatus
‘Methanoperedens nitroreducens’ enriched in a laboratory reactor. Sci. Total Environ.
659, 442–450.
Lu, P., Wang, X., Tang, Y., Ding, A., Yang, H., Guo, J., et al., 2020. Granular activated carbon
assisted nitrate-dependent anaerobic methane oxidation-membrane bioreactor:
strengthening effect and mechanisms. Environ. Int. 138, 105675.
Luesken, F.A., Sanchez, J., van Alen, T.A., Sanabria, J., Op den Camp, H.J.M., Jetten, M.S.M., et
al., 2011a. Simultaneous nitrite-dependent anaerobic methane and ammonium oxi-
dation process. Appl. Environ. Microbiol. 77 (19), 6802–6807.
Luesken, F.A., van Alen, T.A., van der Biezen, E., Frijters, C., Toonen, G., Kampman, C., et al.,
2011b. Diversity and enrichment of nitrite-dependent anaerobic methane oxidizing
bacteria from wastewater sludge. Appl. Microbiol. Biotechnol. 92 (4), 845–854.
Luesken, F.A., Zhu, B.L., van Alen, T.A., Butler, M.K., Diaz, M.R., Song, B., et al., 2011c. pmoA
primers for detection of anaerobic methanotrophs. Appl. Environ. Microbiol. 77 (11),
3877–3880.
Luesken, F.A., Wu, M.L., Op den Camp, H.J., Keltjens, J.T., Stunnenberg, H., Francoijs, K.J., et
al., 2012. Effect of oxygen on the anaerobic methanotroph ‘Candidatus
J. Ding and R.J. Zeng
Methylomirabilis oxyfera’: kinetic and transcriptional analysis. Environ. Microbiol. 14
(4), 1024–1034.
Luo, J.H., Chen, H., Hu, S., Cai, C., Yuan, Z., Guo, J., 2018. Microbial selenate reduction driven
by a denitrifying anaerobic methane oxidation biofilm. Environ. Sci. Technol. 52 (7),
4006–4012.
Luo, J.H., Wu, M., Liu, J., Qian, G., Yuan, Z., Guo, J., 2019. Microbial chromate reduction
coupled with anaerobic oxidation of methane in a membrane biofilm reactor. Envi-
ron. Int. 130, 104926.
Ma, R., Hu, Z., Zhang, J., Ma, H., Jiang, L., Ru, D., 2017. Reduction of greenhouse gases emis-
sions during anoxic wastewater treatment by strengthening nitrite-dependent an-
aerobic methane oxidation process. Bioresour. Technol. 235, 211–218.
Meng, H., Wang, Y.F., Chan, H.W., Wu, R.N., Gu, J.D., 2016. Co-occurrence of nitrite-
dependent anaerobic ammonium and methane oxidation processes in subtropical
acidic forest soils. Appl. Microbiol. Biotechnol. 100 (17), 7727–7739.
Nie, W.B., Xie, G.J., Ding, J., Peng, L., Lu, Y., Tan, X., et al., 2020. Operation strategies of n-
DAMO and Anammox process based on microbial interactions for high rate nitrogen
removal from landfill leachate. Environ. Int. 139, 105596.
Raghoebarsing, A.A., Pol, A., van de Pas-Schoonen, K.T., Smolders, A.J.P., Ettwig, K.F.,
Rijpstra, W.I.C., et al., 2006. A microbial consortium couples anaerobic methane oxi-
dation to denitrification. Nature. 440 (7086), 918–921.
Shen, L.D., He, Z.F., Zhu, Q., Chen, D.Q., Lou, L.P., Xu, X.Y., et al., 2012. Microbiology, ecology,
and application of the nitrite-dependent anaerobic methane oxidation process. Front.
Microbiol. 3, 269.
Shen, L.D., Liu, S., Huang, Q., Lian, X., He, Z.F., Geng, S., et al., 2014a. Evidence for the
cooccurrence of nitrite-dependent anaerobic ammonium and methane oxidation
processes in a flooded paddy field. Appl. Environ. Microbiol. 80 (24), 7611–7619.
Shen, L.D., Liu, S., Zhu, Q., Li, X.Y., Cai, C., Cheng, D.Q., et al., 2014b. Distribution and diver-
sity of nitrite-dependent anaerobic methane-oxidising bacteria in the sediments of
the Qiantang river. Microb. Ecol. 67 (2), 341–349.
Shen, L.D., Zhu, Q., Liu, S., Du, P., Zeng, J.N., Cheng, D.Q., et al., 2014c. Molecular evidence
for nitrite-dependent anaerobic methane-oxidising bacteria in the Jiaojiang Estuary
of the East Sea (China). Appl. Microbiol. Biotechnol. 98 (11), 5029–5038.
Shen, L.D., Huang, Q., He, Z.F., Lian, X., Liu, S., He, Y.F., et al., 2015a. Vertical distribution of
nitrite-dependent anaerobic methane-oxidising bacteria in natural freshwater wet-
land soils. Appl. Microbiol. Biotechnol. 99 (1), 349–357.
Shen, L.D., Wu, H.S., Gao, Z.Q., 2015b. Distribution and environmental significance of
nitrite-dependent anaerobic methane-oxidising bacteria in natural ecosystems.
Appl. Microbiol. Biotechnol. 99 (1), 133–142.
Shen, L.D., Hu, B.L., Liu, S., Chai, X.P., He, Z.F., Ren, H.X., et al., 2016a. Anaerobic methane
oxidation coupled to nitrite reduction can be a potential methane sink in coastal en-
vironments. Appl. Microbiol. Biotechnol. 100 (6), 7171–7180.
Shen, L.D., Wu, H.S., Gao, Z.Q., Li, J., Liu, X., 2016b. Presence of diverse Candidatus
Methylomirabilis oxyfera-like bacteria of NC10 phylum in agricultural soils. J. Appl.
Microbiol. 120 (6), 1552–1560.
Shen, L.D., Wu, H.S., Gao, Z.Q., Liu, X., Li, J., 2016c. Comparison of community structures of
Candidatus Methylomirabilis oxyfera-like bacteria of NC10 phylum in different fresh-
water habitats. Sci. Rep. 6, 25647.
Shen, L., Ouyang, L., Zhu, Y., Trimmer, M., 2019. Spatial separation of anaerobic ammo-
nium oxidation and nitrite-dependent anaerobic methane oxidation in permeable
riverbeds. Environ. Microbiol. 21 (4), 1185–1195.
Shima, S., Thauer, R.K., 2005. Methyl-coenzyme M reductase and the anaerobic oxidation
of methane in methanotrophic Archaea. Curr. Opin. Microbiol. 8 (6), 643–648.
Vaksmaa, A., Luke, C., van Alen, T., Vale, G., Lupotto, E., Jetten, M.S., et al., 2016. Distribu-
tion and activity of the anaerobic methanotrophic community in a nitrogen-
fertilized Italian paddy soil. FEMS Microbiol. Ecol. 92 (12), 1–11.
Vaksmaa, A., Jetten, M.S., Ettwig, K.F., Luke, C., 2017. McrA primers for the detection and
quantification of the anaerobic archaeal methanotroph ‘Candidatus Methanoperedens
nitroreducens’. Appl. Microbiol. Biotechnol. 101 (4), 1631–1641.
Valenzuela, E.I., Avendano, K.A., Balagurusamy, N., Arriaga, S., Nieto-Delgado, C., Thalasso,
F., et al., 2019. Electron shuttling mediated by humic substances fuels anaerobic
methane oxidation and carbon burial in wetland sediments. Sci. Total Environ. 650,
2674–2684.
Wang, Y., Zhu, G., Harhangi, H.R., Zhu, B., Jetten, M.S.M., Yin, C., et al., 2012. Co-occurrence
and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing
bacteria in a paddy soil. FEMS Microbiol. Lett. 336 (2), 79–88.
Wang, J., Hua, M., Li, Y., Ma, F., Zheng, P., Hu, B., 2019b. Achieving high nitrogen removal
efficiency by optimizing nitrite-dependent anaerobic methane oxidation process
with growth factors. Water Res. 161, 35–42.
Wang, Y., Huang, P., Ye, F., Jiang, Y., Song, L., Op den Camp, H.J.M., et al., 2016. Nitrite-
dependent anaerobic methane oxidizing bacteria along the water level fluctuation
zone of the Three Gorges Reservoir. Appl. Microbiol. Biotechnol. 100 (4), 1977–1986.
11
Science of the Total Environment 757 (2021) 143928
Wang, D., Wang, Y., Liu, Y., Ngo, H.H., Lian, Y., Zhao, J., et al., 2017a. Is denitrifying anaer-
obic methane oxidation-centered technologies a solution for the sustainable opera-
tion of wastewater treatment plants? Bioresour. Technol. 234, 456–465.
Wang, J.Q., Shen, L.D., He, Z.F., Hu, J.J., Cai, Z.Y., Zheng, P., et al., 2017b. Spatial and temporal
distribution of nitrite-dependent anaerobic methane-oxidizing bacteria in an inter-
tidal zone of the East China Sea. Appl. Microbiol. Biotechnol. 101 (21), 8007–8014.
Wang, S., Liu, Y., Liu, G., Huang, Y., Zhou, Y., 2017c. A new primer to amplify pmoA gene
from NC10 bacteria in the sediments of Dongchang Lake and Dongping Lake. Curr.
Microbiol. 74 (8), 908–914.
Wang, J., Cai, C., Li, Y., Hua, M., Wang, J., Yang, H., et al., 2019a. Denitrifying anaerobic
methane oxidation: a previously overlooked methane sink in intertidal zone. Environ.
Sci. Technol. 53, 203–212.
Wang, S., Pi, Y., Jiang, Y., Pan, H., Wang, X., Wang, X., et al., 2020. Nitrate reduction in the
reed rhizosphere of a riparian zone: from functional genes to activity and contribu-
tion. Environ. Res. 180, 108867.
Welte, C.U., Rasigraf, O., Vaksmaa, A., Versantvoort, W., Arshad, A., Op den Camp, H.J.M., et
al., 2016. Nitrate- and nitrite-dependent anaerobic oxidation of methane. Environ.
Microbiol. Rep. 8, 941–955.
Wu, J., Zhang, Y., 2017. Evaluation of the impact of organic material on the anaerobic
methane and ammonium removal in a membrane aerated biofilm reactor (MABR)
based on the multispecies biofilm modeling. Environ. Sci. Pollut. Res. Int. 24 (2),
1677–1685.
Wu, M.L., de Vries, S., van Alen, T.A., Butler, M.K., den Camp, H.J.M.O., Keltjens, J.T., et al.,
2011. Physiological role of the respiratory quinol oxidase in the anaerobic nitrite-
reducing methanotroph ‘Candidatus Methylomirabilis oxyfera’. Microbiol-Sgm. 157,
890–898.
Wu, M.L., van Alen, T.A., van Donselaar, E.G., Strous, M., Jetten, M.S., van Niftrik, L., 2012a.
Co-localization of particulate methane monooxygenase and cd1 nitrite reductase in
the denitrifying methanotroph ‘Candidatus Methylomirabilis oxyfera’. FEMS
Microbiol. Lett. 334 (1), 49–56.
Wu, M.L., van Teeseling, M.C.F., Willems, M.J.R., van Donselaar, E.G., Klingl, A., Rachel, R., et
al., 2012b. Ultrastructure of the denitrifying methanotroph “Candidatus
Methylomirabilis oxyfera”, a novel polygon-shaped bacterium. J. Bacteriol. 194 (2),
284–291.
Wu, M.L., Wessels, J.C., Pol, A., Op den Camp, H.J., Jetten, M.S., van Niftrik, L., 2015. XoxF-
type methanol dehydrogenase from the anaerobic methanotroph “Candidatus
Methylomirabilis oxyfera”. Appl. Environ. Microbiol. 81 (4), 1442–1451.
Xu, S., Lu, W., Mustafa, M.F., Liu, Y., Wang, H., 2020. Presence of diverse nitrate-dependent
anaerobic methane oxidizing archaea in sewage sludge. J. Appl. Microbiol. 128,
775–783.
Yan, P.Z., Li, M.C., Wei, G.S., Li, H., Gao, Z., 2015. Molecular fingerprint and dominant envi-
ronmental factors of nitrite-dependent anaerobic methane- oxidizing bacteria in sed-
iments from the Yellow River estuary, China. PLoS One 10 (9), e0137996.
Yan, Z., Joshi, P., Gorski, C.A., Ferry, J.G., 2018. A biochemical framework for anaerobic ox-
idation of methane driven by Fe(III)-dependent respiration. Nat. Commun. 9, 1642.
Yang, J., Jiang, H.C., Wu, G., Hou, W.G., Sun, Y.J., Lai, Z.P., et al., 2012. Co-occurrence of
nitrite-dependent anaerobic methane oxidizing and anaerobic ammonia oxidizing
bacteria in two Qinghai-Tibetan saline lakes. Front Earth Sci-Prc. 6 (4), 383–391.
Yang, M., Guo, Q., Tong, T., Li, N., Xie, S., Long, Y., 2017. Vegetation type and layer depth
influence nitrite-dependent methane-oxidizing bacteria in constructed wetland.
Arch. Microbiol. 199 (3), 505–511.
Zhang, M., Luo, Y., Lin, L., Lin, X., Hetharua, B., Zhao, W., et al., 2018. Molecular and stable
isotopic evidence for the occurrence of nitrite-dependent anaerobic methane-
oxidizing bacteria in the mangrove sediment of Zhangjiang Estuary. China. Appl.
Microbiol. Biotechnol. 102 (5), 2441–2454.
Zheng, Y.L., Hou, L.J., Chen, F.Y., Zhou, J., Liu, M., Yin, G.Y., et al., 2020. Denitrifying anaer-
obic methane oxidation in intertidal marsh soils: occurrence and environmental sig-
nificance. Geoderma. 357, 113943.
Zhong Q., Xue D., Chen H., Liu L., He Y., Zhu D., et al. 2020. Structure and distribution of
nitrite-dependent anaerobic methane oxidation bacteria vary with water tables in
Zoige peatlands. FEMS Microbiol. Ecol. 96(5), fiaa039.
Zhou, L.L., Wang, Y., Long, X.E., Guo, J.H., Zhu, G.B., 2014. High abundance and diversity of
nitrite-dependent anaerobic methane-oxidizing bacteria in a paddy field profile.
FEMS Microbiol. Lett. 360 (1), 33–41.
Zhu, B.L., van Dijk, G., Fritz, C., Smolders, A.J.P., Pol, A., Jetten, M.S.M., et al., 2012. Anaerobic
oxidization of methane in a minerotrophic peatland: enrichment of nitrite-
dependent methane-oxidizing bacteria. Appl. Environ. Microbiol. 78 (24),
8657–8665.
Zhu, G.B., Zhou, L.L., Wang, Y., Wang, S.Y., Guo, J.H., Long, X.E., et al., 2015. Biogeographical
distribution of denitrifying anaerobic methane oxidizing bacteria in Chinese wetland
ecosystems. Environ. Microbiol. Rep. 7 (1), 128–138.