Chemosphere 44 (2001) 1213±1221
www.elsevier.com/locate/chemosphere
Relationship between release of nitric oxide and CO2 and their
dependence on oxidation reduction potential in wastewater
treatment
M. Fuerhacker
a,*
, H. Bauer b, R. Ellinger b, U. Sree b, H. Schmid b,
F. Zibuschka a, H. Puxbaum b
a
Institute for Water Provision, Water Ecology and Waste Management, Universitat fur Bodenkultur, Muthgasse 18,
A-1190 Vienna, Austria
b
Institute for Analytical Chemistry, Vienna University of Technology, Getreidemarkt 9/151, A-1060 Vienna, Austria
Received 27 February 2000; accepted 31 July 2000
Abstract
Nitric oxide (NO) is an intermediate of denitri®cation process and can be produced by denitri®ers, nitri®ers and
other bacteria. In our experiments we measured the dynamic ¯ow of NO depending on oxidation reduction potential
(ORP). Di€erent ORP-ranges were related to various carbon loading stages in the wastewater treatment pilot plant.
Nitri®cation and denitri®cation were achieved by a sequence of aeration and non-aeration periods. Our measurements
show that di€erent carbon loading conditions (low feed, balanced and overloaded conditions) did not change the range
of the mixing ratio of NO emissions when the aeration conditions like air-¯ow and temperature were kept constant.
Minimum and maximum NO mixing ratios were 34.7 and 91.8 ppbv; 52.3 and 91.3 ppbv; 57.6 and 109 ppbv for low
feed, balanced and overloaded conditions, respectively. The curve of the NO graph relied on nitri®cation/denitri®cation
dynamics. The dependence of NO release on di€erent ORP and CO2 -release during the various conditions are shown.
Longer aeration times resulted in an increased release of gaseous NO. The net-release of NO g 1 nitrogen removed was
between 0.014% and 0.028%. The NO ¯uxes to the air were observed between 8.3 and 14.9 mg m 2 d 1 NO. The major
release occurred during high aeration periods whereas the concentration of dissolved [NOaq ] in the wastewater was less
than 0.05% of the gaseous release due to very low solubility of the NO. Ó 2001 Elsevier Science Ltd. All rights
reserved.
Keywords: NO volume-based mixing ratios; Nitric oxide; Wastewater treatment; Denitri®cation; O€-gas; ORP; Carbon dioxide
1. Introduction
In the denitri®cation process NO is an intermediate
in the sequential pathway of nitrate to nitrogen. This
reaction is coupled with the oxidation of organic sub-
*
Corresponding author. Tel.: +43-1-36006/5821; fax: +43-1368-99-49.
E-mail address: [email protected] (M. Fuerhacker).
stances or inorganic electron donors. The proposed
reaction of denitri®cation is a sequential reduction
process from nitrate to nitrogen complying di€erent
intermediates such as nitrite, nitric oxide and nitrous
oxide (Fig. 1) (Conrad, 1996).
The reduction of nitrite is catalysed by nitric oxide
reductase (Payne, 1973; Anderson and Levine, 1986;
Goretski and Hollocher, 1988; Goretski et al., 1990).
The followup reaction to N2 O is very fast and Goretski
and Hollocher (1988) found that the nitric oxide reductase is one of the fastest enzymes in the whole
0045-6535/01/$ - see front matter Ó 2001 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 4 5 - 6 5 3 5 ( 0 0 ) 0 0 3 4 2 - 8
1214
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
Fig. 1. Schemes of NO production and NO consumption in
nitri®ers and denitri®ers (Conrad, 1996).
pathway. The rapid decomposition of NO in microorganisms is necessary to avoid toxic e€ects (Zumft, 1993).
Goretski et al. (1990) showed that at least 60±70% of the
¯ux of N in certain denitrifying bacteria and 35% in
other bacteria pass through a pool of extracellular dissolved NO [NOaq ]. For many denitri®ers it seems that
once the nitric oxide reductase is synthesised, the enzyme
is relatively insensitive to oxygen, so that NO consumption by denitri®ers can take place even in wellaerated soil (Remde and Conrad, 1991a). NO release
from denitri®cation in oxic soil made up a very low
percentage comparable to the nitri®cation process, but
made up more than 10% in anoxic soil (Remde and
Conrad, 1991b; Baumg
artner and Conrad, 1992a).
Though there are possible additional ways for NO
production by aerobic denitri®cation or heterotrophic
denitri®ers, the relevance of NO production by these
pathways is still unclear. In wastewater the major
pathway for NO production seems to be denitri®cation
catalysed by nitrite reductase as this enzyme can be
produced by nitri®ers and denitri®ers.
Actually, NO production has been demonstrated in
a large number of di€erent microorganisms especially
in nitrifying and denitrifying microorganisms, but also
in other organisms (Conrad, 1990; Zumft, 1993). Different types of organisms with di€erent metabolic
pathways are involved in NO metabolism; not all are
satisfactorily understood on a biochemical basis
(Conrad, 1996).
The major source of NO production is in soil nitri®cation (Skiba et al., 1993). Of the two groups of
chemolitotrophic nitri®ers, the nitroso-bacteria, which
oxidises ammonium to nitrite, can produce signi®cant
amounts of NO. During the oxidation of ammonium to
hydroxylamine, nitrite and nitrate, NO should not be
formed. However, ammonium oxidisers denitrify some
of the produced nitrite to NO, N2 O and even N2 under
aerobic condition (Remde and Conrad, 1990). NO
emission results at least partially from di€erent kinetics
of NO production and NO consumption in nitrate-reducing and ammonium-oxidising microorganisms
(Conrad, 1996). However, it is still not known, whether
the production mechanism is due to the reduction of the
produced nitrite by a similar pathway (NO2 , NO, N2 O,
N2 ) as in denitri®ers (Poth, 1986). Usually, NO production by nitri®cation seems to account only for a low
percent of total nitrogen transformation in soil (Remde
and Conrad, 1991b; Baumg
artner and Conrad, 1992b).
Coupled oxidation/reduction pathways have often been
observed in aquatic sediments where nitrogen is limited
(Rysgaard et al., 1993).
In wastewater, nitri®cation and denitri®cation are
usual means for nitrogen removal and conventionally
biological nitrogen removal is obtained in activated
sludge processes by a sequence of aerobic and anoxic
processes. Von Schulthess et al. (1994) have shown different amounts of NO releases during denitri®cation in
wastewater from batch cultures under di€erent oxygen
concentrations, especially under anoxic and anaerobic
conditions. They found that aerobic conditions favour
the production of N2 O but not the production of NO.
Furthermore, NO is accumulated at very low concentrations and the highest emission levels occur under
complete anoxic conditions. These conditions occur not
only in sewers but also in sewage treatment plants in the
primary settler during denitri®cation and biological
phosphorous removal.
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
An increased attention needs to be paid on emission
sources as nitric oxide plays a central role in the photochemistry of the atmosphere (Logan, 1983; Singh,
1987) and is also considered to be an ozone precursor,
and hence an environmentally hazardous substance.
Nitric oxide is also a key component that leads to urban
photochemical smog. Recent evaluations indicated that
soils are major sources for NO with a source strength of
about 20 Tg NO±N yr 1 (Davidson and Kingerlee, 1997;
Skiba et al., 1993) contributing about 20% to the total
budget of atmospheric NO. Hence many studies are
dealing with NO production in soil.
The objective of this study is to investigate the dependence of NO release on dissolved oxygen (DO) and
ORP during wastewater treatment under nitrifying and
denitrifying conditions. This approach is to show an
impact of di€erent aeration times and carbon loading
rates in the wastewater on the release of NO under different ORP and oxygen conditions. It is also aimed to
assess the NO ¯ux and the release based on removed
nitrogen.Our empirical approach evaluates the NO ¯ux
in a direct way. In this case it is not necessary to differentiate between production and consumption of NO
nor between di€erent processes involved in production
or consumption since all processes are included in one
black box. In our case a characteristic feature for
wastewater treatment was chosen and the in¯uence on
NO production under the applied conditions was investigated.
2. Materials and methods
The investigations were carried out in an activated
sludge pilot plant (1.6 m3 ) (Fig. 2) with feedback of
1215
biomass (Fuerhacker et al., 2000). The plant operated in
a temperature range of 18±20°C. The wastewater used in
the tests was of municipal/industrial origin. Fresh
wastewater was pumped out of the local municipal
Viennese sewer line into a storage tank of 1 m3 .
The addition of raw sewage as a carbon source was
time controlled during aeration as well as non-aeration
periods. The NO release of the activated sludge during
wastewater treatment was studied under di€erent oxygenation conditions, yielding di€erent ranges of ORP.
The stepwise change in loading and aeration is presented
in (Table 1). Under Stage I a low feed-level was combined with a comparatively long aeration time, Stage II
was the balanced in feed and aeration times and Stage
III was the high loaded condition. Carbon removal, nitri®cation and denitri®cation were carried out in the
same reactor by a sequence of aerobic and anoxic processes.
The suspended solids concentration of the mixed liquor in the aeration tank was in the range of 4±7 g l 1 .
About 1.7 m3 d 1 of sludge was recycled constantly
throughout. The excess sludge was carried out with the
e‚uent into the local sewer system. Paddle mixers were
installed to mix the content in the aeration chamber
continuously during aeration and non-aeration periods.
Time-controlled aerators blew air into the aeration tank
at a rate of 16 m3 h 1 (based on Standard Conditions
(STP) 0°C=1013 mbar ). The aeration tank was completely sealed with a polyethylene cover to keep the expelled air in an airtight chamber, with a volume of about
2 m3 . Additional air (5.5 m3 h 1 STP) was pumped
continuously into the chamber to maintain air ¯ow
during non-aeration times and to avoid the collapse of
the cover. Additional air was also used to calculate the
carbon balance especially during non-aeration periods.
Fig. 2. Schematic diagram of the treatment plant.
1216
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
4. Results and discussion
Table 1
Operating conditions during Stages I±III
Aeration time (h)
Non-aeration time (h)
Feed: on-time (min)
Feed: o€-time (min)
In¯ow (m3 d 1 )
Hydraulic retention time (h)
Stage I
Stage II
Stage III
2
1
1.5
4
1.7
25
0.5
1
1.5
4
1.7
25
0.5
1
3
4
2.7
14
3. Analytical methods
During the experiments on-line measurements in the
wastewater of the aeration tank were carried out for
ORP and DO in the aqueous phase. NO a volatile denitri®cation intermediate was examined in the o€-gas
with a continuous automatic chemiluminescence monitor (Nitrogen Oxides Analyzer Model 8840, Monitor
Labs). Also CO2 in the o€-gas was measured continuously (UNOR 6N NDIR, Maihak). Samples were collected from the outlet of the airtight chamber through a
glass manifold kept at 25°C. Average concentrations of
ambient air were controlled frequently. System performance was monitored by analysing total organic carbon
(TOC), total nitrogen (Ntot ), phosphate (PO4 -P), total
phosphorous (Ptot ), suspended solids (SS), ammonium
nitrogen (NH4 ±N) and nitrate nitrogen (NO3 ±N) in
wastewater according to the German Standards. E‚uent samples were ®ltered prior to TOC measurements in
order to remove excess sludge.
The raw wastewater showed average concentrations
of 160 mg l 1 of TOC, 48 mg NH4 ±N, 72 mg l 1 Ntot ,
and 5 mg Ptot , respectively. The nitrogen removal rates
were in Stages I, II and III 96%, 98% and 62%, respectively. In addition carbon removal rates were based on
the ®ltered e‚uent and 94% for Stages I and II and 93%
for Stage III.
Results of kinetic measurements for NO, ORP and
CO2 during Stages I±III are given in Figs. 3±5. All
registered periods started with an aeration cycle. The
ORP at Stage I remained at very high mV-ranges between 115 and 290 mV. The corresponding oxygen levels
were also high and reached upper peaks of 5 mg l 1 O2 .
Stage II showed a di€erent picture with mV-ranges between 60 and 198 mV and oxygen levels between 0 and
1.5 mg l 1 O2 . Under low oxygenated conditions in
Stage III the ORP-graph dropped to 90 and 114 mV
and kept decreasing as the carbon loads were raised. The
O2 concentration rarely reached measurable values and
behaved corresponding to ORP. The relationship between NO and ORP (Figs. 6±8) and the relationship
between NO and CO2 mixing ratios in the o€-gas for the
three stages are given in Figs. 3±5.
The minimum and maximum mixing ratios of CO2
(vol%), NO (ppbv) and average NO emissions based
on removed nitrogen (mg NO g 1 N), and the ¯ux of
NO out of the treatment plant in the o€-gas during
Stages I±III are given in Table 2. In addition the
concentrations and releases of dissolved NO are listed
in Table 2.
Fig. 3. Actual values of ORP in mV and the volume-based mixing ratios of CO2 in vol% and NO in ppbv during Stage I
(the interrupted lines indicate the start of aeration periods).
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
1217
Fig. 4. Actual values of ORP in mV and the volume-based mixing ratios of CO2 in vol% and NO in ppbv during Stage II
(the interrupted lines indicate the start of aeration periods).
Fig. 5. Actual values of ORP in mV and the volume-based mixing ratios of CO2 in vol% and NO in ppbv during Stage III
(the interrupted lines indicate the start of aeration periods).
Our di€erent experiments show the changes in NO
during variations of oxidation time and feed rate and the
dependence on the ORP and CO2 . The ORP variations
rely mainly on the feeding rate and the concentration of
the back sludge in the settling tank and depend directly
on the concentration of biodegradable carbon. During
the aeration condition nitri®cation is possible; but as
raw sewage was added all the time in ®ve-minute periods
denitri®cation could take place simultaneously also
during aeration time. As explained before, NO is pro-
duced mainly during denitri®cation by denitri®ers or in a
denitri®cation pathway by nitri®ers (Conrad, 1996). The
NO ¯ux from water to the air is the result of simultaneously operating production and consumption processes in the activated sludge tank and di€usion e€ects
during aeration or non-aeration time. The NO production usually occurs during denitri®cation under anoxic
conditions, when the oxygen supply drops to zero.
Therefore, NO mixing ratios were decreasing due to
dilution during aeration in the o€-gas. Increase in NO
1218
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
Fig. 6. Relationship between NO mixing ratio in the o€-gas and ORP for Stage I.
Fig. 7. Relationship between NO mixing ratio in the o€-gas and ORP for Stage II.
release announces denitri®cation during aeration conditions.
In Stage I the relationship between NO and ORP
shows a decrease of NO mixing ratio with the increase in
ORP values (Figs. 3 and 6). During aeration conditions
the decrease in NO mixing ratio shows a small peak at
ORP-values between 200 and 250 mV and drops at
higher ORP values. The small peak is interpreted as simultaneous nitri®cation/denitri®cation which was possible in the highly aerated Stage I, due to the addition of
raw sewage. Under non-aeration conditions denitri®cation starts again with an increase in NO emission. In
Stage II under balanced conditions the NO emissions
show a di€erent relationship on ORP depending on aeration or non-aeration periods, as denitri®cation is enhanced during non-aeration periods (Figs. 4 and 7).
Furthermore, an expectation of an increase in NO release with a decrease in ORP indicating enhanced denitri®cation during low ORP could not be observed for
Stage II due to enhanced simultaneous nitri®cation/denitri®cation. The highest mixing ratios of NO were observed in Stage III at the lowest ORP-levels, whereas in
Stage II the maximum was reached between 200 and 100
mV during non-aeration conditions. In Stage III the
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
1219
Fig. 8. Relationship between NO mixing ratio in the o€-gas and ORP for Stage III.
Table 2
CO2 and NO in the o€-gas of the aeration tank
a
CO2 max (vol%)
CO2 min (vol%)a
NO max (ppbv)a
NO min (ppbv)a
NO background (ppbv)
NO average (lg N m 3 )
NO emissions
(mg NO g 1 Nrem )
NO emissions
(mg N g 1 Nrem )
NO-¯ux (mg m 2 d 1 )
NOaq (ng NO g 1 Nrem )
NOaq (ng N g 1 Nrem )
NOaq (ng l 1 ) (aeration)
NOaq (ng l 1 )
(non-aeration)
NOaq (ng l 1 ) (max)
NOaq (ng l 1 ) (min)
Stage I
Stage II Stage III
0.27
0.07
91.8
34.7
3
77.4
0.25
0.32
0.10
91.3
52.3
21.3
64.3
0.14
0.39
0.11
109
57.6
24.1
70.5
0.28
0.12
0.07
0.13
14.9
45
21
3.0
3.8
8.3
57
27
3.5
4.5
9.1
115
54
4.2
4.9
5.2
2.0
5.2
3.0
6.2
3.3
a
Background values included: Nrem removed nitrogen; NOaq ;
NO in solution.
pattern between aeration and non-aeration conditions
looks similar to Stage I. Both times the NO mixing ratios increased with the decrease in ORP (Figs. 5 and 8)
independent of aeration or non-aeration conditions.
The relationships between NO and CO2 and between
CO2 and ORP show a similar pattern for Stage II and
Stage III. Whereas Stage I shows a di€erence between
aerated and non-aerated conditions due to the decrease
of CO2 -mixing ratio during aeration period because of
the lack of degradable organic substances.
Our interpretation of the results of Stage II is, that
after a certain CO2 -level is reached oxygen is also
available for nitri®cation. Due to a sucient low ORP
denitri®cation starts simultaneously. For Stage III the
NO mixing ratio is increasing with the decrease in CO2 mixing ratio (Fig. 5). The high CO2 -mixing ratio
indicates that the DO is consumed by heterotrophic
organisms to degrade organic carbon compounds and
only little DO is left for nitri®cation at the end of the
aeration period. Only 62% of the NH4 ±N was eliminated. The shape of the NO mixing ratio graph shows a
decrease during aeration due to dilution and an increase
during non-aeration period (Fig. 5). Little oxygen was
left for NO3 ±N production in Stage III only at the end
of the aeration period. Denitri®cation generated NO
mainly during non-aeration period under this condition.
During all observed periods, the minimum mixing
ratio of NO did not drop to zero though the ambient air
levels were considered. The NO maximum corresponded
either to the ORP minimum (Stages I and III) or was
observed between the maximum point of the ORP curve
at the end of aeration and the nitrate breakpoint at the
endpoint of anoxic respiration (Stage II) depending on
loading conditions. Our measurements also show that
di€erent carbon loading conditions (low feed, balanced
and overloaded conditions) did not change the range of
the mixing ratio of NO emissions under constant aeration conditions (e.g., air-¯ow and temperature). The
maximum NO concentrations are given in Table 2 and
are of the same magnitude during all three stages and
varied only between 57 and 68 lg N m 3 , though the
average concentration in the o€-gas was higher under
overloaded conditions. These concentrations are relatively low compared to the batch experiments conducted
1220
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
by Von Schulthess et al. (1994), who found NO concentrations up to 6 mg N m 3 .
In addition the NO net release based on N removal
was calculated from the NO concentration in an airtight chamber and the mass ¯ow over time plus the
release of dissolved [NOaq ]. To assess the dissolved NO
in the aqueous phase the remaining concentration was
calculated using Henry's law. During aeration time
volatile substances like NO are sparged out of the
water to the atmosphere with the aeration air. During
non-aeration periods, the NO is released from water by
di€usion. The portion of NO remaining dissolved is
very low due to the low solubility (KH 25°C ˆ 1:9
10 3 M atm 1 ; Sigg and Stumm, 1994). Henry's law
states that the equilibrium value of the mole fraction
of gas dissolved in a liquid is directly proportional to
the partial pressure of that gas above the liquid surface, or
‰NOaq Š ˆ KH pNO ;
…Sigg and Stumm; 1994†
where pNO is the equilibrium partial pressure of gas in
contact with liquid (atm), ‰NOaq Š the mole fraction of
1
gas dissolved in liquid (mol lwater
), and KH is the Henry's
coecient (mol atm 1 ).
The calculations showed that the major portion of
the NO is released into the air. The NO emissions based
on 1 g of nitrogen removed depended on the operating
conditions and could be observed for Stages I, II and III
with 0.25, 0.14 and 0.28 mg NO g 1 N, respectively. The
NO release with the e‚uent was comparatively low and
for Stages I, II and III 0.02%, 0.04% and 0.04%, respectively.
The ¯ux of NO is not only in¯uenced by the NO
production rate but even more by the NO consumption
rate. Though NO consumption is enhanced under anoxic conditions (Conrad, 1996) longer aeration times
resulted in an increased net release of gaseous NO. The
investigated ¯uxes of NO into the air gave di€erent results. In this case, NO release is highest with 14.9 mg NO
m 2 d 1 during low-load/long aeration time cycles (2 h
aeration/1 h non-aeration) and about double of the release of 8.3 mg NO m 2 d 1 during balanced conditions
(1/2 h aeration/1 h non-aeration). During high aeration
periods the stripping e€ect is competing with the enzymatic turnover of the NO reductase. The NO ¯ux during
Stage III is 9.1 mg NO m 2 d 1 and comparatively low
due to lower nitrogen turnover. Von Schulthess et al.
(1995) found that increased gas stripping resulted in an
increased production of the volatile N intermediates.
Goretski and Hollocher (1988) found a dependency between net-production and high stripping eciency.
Our results also indicate that under applied conditions, which we investigated in our experiments, the total
release of NO was very small. Only between 0.014 and
0.028% of the removed nitrogen were released as NO.
Even under low oxygen conditions no major increase in
NO production or inhibition e€ects were observed. Von
Schulthess et al. (1995) showed in batch experiments,
that the addition of nitrite could cause an accumulation
of NO and N2 O and a severe inhibition of all enzymes of
the denitri®cation respiratory chain and increase the NO
production about 12 times. We conclude from our results, that no major nitrite accumulation occurred during the process.
5. Conclusions
Our experiments show that the pattern of NO release
is dependent on feed conditions. But the mixing ratios
for NO in the o€-gas and the NO emissions are of the
same magnitude at di€erent carbon loading conditions.
NO emissions from a denitrifying wastewater treatment
plant were very low during both aeration and nonaeration periods compared to the NO emissions from
soil under anoxic conditions.
Acknowledgements
The project is in part ®nanced by MA 22 of the
Viennese Municipality.
References
Anderson, I.C., Levine, J.S., 1986. Relative rates of nitric
oxide and nitrous oxide production by nitri®ers, denitri®ers, and nitrate respirers. Appl. Environ. Microbiol. 51,
938±945.
Baumgartner, M., Conrad, R., 1992a. Role of nitrate and
nitrite for production and consumption of nitric oxide
during denitri®cation in soil. FEMS Microbiol. Ecol. 101,
59±66.
Baumgartner, M., Conrad, R., 1992b. E€ects of soil variables
and season on the production and consumption of nitric
oxide in oxic soils. Biol. Fertil. Soils 14, 166±174.
Conrad, R., 1990. Flux of NOx between soil and atmosphere:
Importance and soil microbial metabolism. In: Revsbech,
N.P., Soerensen, J. (Eds.), Denitri®cation in Soil and
Sediment. Plenum Press, New York, pp. 105±128.
Conrad, R., 1996. Metabolism of nitric oxide in soil and soil
microorganisms and regulation of ¯ux to the atmosphere.
In: Murell, J.C., Kelly, D.P. (Eds.), Microbiology of
Atmospheric Trace Gases: Sources, Sinks and Global
Changes Processes. Springer, Berlin, pp. 167±203.
Davidson, E.A., Kingerlee, W., 1997. A global inventory of
nitric oxide emissions from soils. Nutrient Recycling in
Agroecosystems 48, 37±50.
Fuerhacker, M., Bauer, H., Ellinger, R., Sree, U., Schmid, H.,
Zibuschka, F., Puxbaum, H., 2000. Approach for a novel
control strategy for waste water treatment plants. Water
Res. 34, 2499±2506.
M. Fuerhacker et al. / Chemosphere 44 (2001) 1213±1221
Goretski, J., Hollocher, T.C., 1988. Trapping of nitric oxide
produced during denitri®cation by extracellular hemoglobin. J. Biol. Chem. 263, 2316±2323.
Goretski, J., Za®riou, O.C., Hollocher, T.C., 1990. Steady-state
nitric oxide concentration during denitri®cation. J. Biol.
Chem. 265, 11535±11538.
Logan, J.A., 1983. Nitrogen oxides in the troposphere: global
and regional budgets. J. Geophys. Res. 88, 10785±10807.
Payne, W.J., 1973. Reduction of nitrogenous oxide by microorganisms. Bakteriol. Rev. 37, 409±452.
Poth, M., 1986. Dinitrogen production from nitrite by a
Nitrosomonas isolate. Appl. Environ. Microbiol. 52, 957±
959.
Remde, A., Conrad, R., 1990. Production of nitric oxide in
Nitrosomonas europaea by reduction of nitrite. Arch.
Microbiol. 154, 187±191.
Remde, A., Conrad, R., 1991a. Production and consumption of
nitric oxide by denitrifying bacteria under anaerobic and
aerobic conditions. FEMS Microbiol. Lett. SO, 329±332.
Remde, A., Conrad, R., 1991b. Role of nitri®cation and
denitri®cation for NO metabolism in soil. Biogeochemistry
12, 189±205.
1221
Rysgaard, S., Risgaard-Petersen, A., Nielsen, L.P., Revsbech,
N.P., 1993. Nitri®cation and denitri®cation in lake and
estuarine sediments measured by the 15 N dilution technique
and isotope pairing. Appl. Environ. Microbiol. 59, 2093±
2098.
Singh, H.B., 1987. Reactive nitrogen in the troposphere,
chemistry and transport of NO, and PAN. Environ. Sci.
Technol. 21, 320±327.
Sigg, L., Stumm, W., 1994. Aquatische Chemie (Aquatic
Chemistry), Verlag der Vereine Z
urich, Verlag Teubner
ISBN 3-519-23651-6.
Skiba, U., Smith, K.A., Fowler, D., 1993. Nitri®cation and
denitri®cation as sources of nitric oxide and nitrous oxide in
a sandy loam soil. Soil Biol. Biochem. 25, 1527±1536.
Schulthess, R.V., Wild, D., Gujer, W., 1994. Nitric and nitrous
oxides from denitrifying activated sludge at low oxygen
concentration. Water Sci. Technol. 30 (6), 123±132.
Schulthess, R.V., Kuehni, M., Gujer, W., 1995. Release of nitric
and nitrous oxides from denitrifying activated sludge. Water
Res. 29 (1), 215±226.
Zumft, W.G., 1993. The biological role of nitric oxide in
bacteria. Arch. Microbiol. 160, 253±264.