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Chapter 9 : Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments
Authors:
Mark Trimmer1,
Pia Engström2
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Affiliations:
1: School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom;
2: Civil and Environmental Engineering, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
Content Type: Monograph
Publication Year:
2011
Category: Environmental Microbiology
Book DOI:
10.1128/9781555817145
Chapter DOI:
10.1128/9781555817145.ch9
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Abstract:
This chapter provides a synthesis of the broadscale patterns of anammox across a spectrum of aquatic ecosystems and to put forward some hypotheses as to what regulates anammox and the total flux of N in such systems. Research into anammox falls largely into two distinct aquatic ecosystems: (i) its role in the anaerobic oxidation of ammonium in the suboxic layers of aquatic sediments, where the respective reactions and ecophysiologies are compressed into fractions of centimeters; and (ii) the same ecosystem function, but distributed over depths of tens of meters in the oxygen minimum zones (OMZs) of the global ocean. The chapter focuses on the results obtained using slurries of homogenized sediment, and then focuses on the data derived with intact sediment cores, and, finally, draw comparisons between the two at the end, without dwelling too long on the respective complexities of each method. Anammox bacteria appear active in both low-oxygen and suboxic waters, and such conditions are often considered as prerequisites for denitrification, since oxygen represses synthesis and activity of denitrifying enzymes, though the effect may be more subtle.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
Figures
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments
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Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig01
FIGURE 1
Schematic representation of the oxic and suboxic zones in sediments and OMZs to highlight the respective difference in depth scale (a, b) and representative examples for sediment in the Cascadia Basin (c) and the central Arabian Sea (d) (panels c and d are reproduced, respectively, from
Engström et al. [2009]
and
Nicholls et al. [2007]
, Copyright by the American Society of Limnology and Oceanography, Inc.). Note the high NO3
– (typical estuarine or deep sea) and low NO3
– (coastal or shelf sea) depicted in panel a.
10.1128/9781555817145/f0202-01_thmb.gif
10.1128/9781555817145/f0202-01.gif
FIGURE 1
Schematic representation of the oxic and suboxic zones in sediments and OMZs to highlight the respective difference in depth scale (a, b) and representative examples for sediment in the Cascadia Basin (c) and the central Arabian Sea (d) (panels c and d are reproduced, respectively, from Engström et al. [2009] and Nicholls et al. [2007] , Copyright by the American Society of Limnology and Oceanography, Inc.). Note the high NO3 – (typical estuarine or deep sea) and low NO3 – (coastal or shelf sea) depicted in panel a.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig02
FIGURE 2
Simplified representation of the N cycle highlighting the key characteristic of the anammox reaction. Nitrate reduction refers to the one-step reduction of NO3
– to NO2
– and complete denitrification would ultimately generate N2 gas; assimilatory reduction of NO3
– to organic N has been omitted. (Reproduced and amended from
Trimmer et al. [2003
] with permission from The American Society for Microbiology.)
10.1128/9781555817145/f0203-01_thmb.gif
10.1128/9781555817145/f0203-01.gif
FIGURE 2
Simplified representation of the N cycle highlighting the key characteristic of the anammox reaction. Nitrate reduction refers to the one-step reduction of NO3 – to NO2 – and complete denitrification would ultimately generate N2 gas; assimilatory reduction of NO3 – to organic N has been omitted. (Reproduced and amended from Trimmer et al. [2003 ] with permission from The American Society for Microbiology.)
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig03
FIGURE 3
Contribution from anammox to the production of N2 (ra %) measured in slurries of anoxic sediment. (a) Relatively simple linear relationship for water depths up to 150 m with the correlation coefficient (r). (b) Complete data set against water depth on a common log scale. The open circle is the mean for ra at this site (S9 the deep Skagerrak) (see
Table 1
).
10.1128/9781555817145/f0207-01_thmb.gif
10.1128/9781555817145/f0207-01.gif
FIGURE 3
Contribution from anammox to the production of N2 (ra %) measured in slurries of anoxic sediment. (a) Relatively simple linear relationship for water depths up to 150 m with the correlation coefficient (r). (b) Complete data set against water depth on a common log scale. The open circle is the mean for ra at this site (S9 the deep Skagerrak) (see Table 1 ).
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig04
FIGURE 4
Composite of all available anammox- and denitrification-specific activity slurry data (rate) as a function of water depth. Rate data have been log transformed (log10+1) and plotted against water depth on a common log scale. Data are from
Table 1
; note the difference in both the range and variance associated with the measures of denitrification.
10.1128/9781555817145/f0208-01_thmb.gif
10.1128/9781555817145/f0208-01.gif
FIGURE 4
Composite of all available anammox- and denitrification-specific activity slurry data (rate) as a function of water depth. Rate data have been log transformed (log10+1) and plotted against water depth on a common log scale. Data are from Table 1 ; note the difference in both the range and variance associated with the measures of denitrification.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig05
FIGURE 5
A composite of all available anammox-specific activity slurry data (rate) as a function of denitrification. The data are split between coastal and shelf waters deeper than 20 m and estuarine and coastal waters shallower than 20 m. Data have been normalized by common log transformation (log10+1) and are from
Table 1
.
10.1128/9781555817145/f0210-01_thmb.gif
10.1128/9781555817145/f0210-01.gif
FIGURE 5
A composite of all available anammox-specific activity slurry data (rate) as a function of denitrification. The data are split between coastal and shelf waters deeper than 20 m and estuarine and coastal waters shallower than 20 m. Data have been normalized by common log transformation (log10+1) and are from Table 1 .
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig06
FIGURE 6
The yield of 29N2 from the oxidation of 15NH4
+ in the presence of either just 14NO3
– or just NO2
– or a dual labeling experiment with 100 µmol of NO3
– liter–1 and increasing NO2
–. Clearly, the availability of NO2
– and NO3
– affects the significance of anammox. Data are from
Trimmer et al. (2005)
. Sediment is from Grays in the Thames estuary.
10.1128/9781555817145/f0211-01_thmb.gif
10.1128/9781555817145/f0211-01.gif
FIGURE 6
The yield of 29N2 from the oxidation of 15NH4 + in the presence of either just 14NO3 – or just NO2 – or a dual labeling experiment with 100 µmol of NO3 – liter–1 and increasing NO2 –. Clearly, the availability of NO2 – and NO3 – affects the significance of anammox. Data are from Trimmer et al. (2005) . Sediment is from Grays in the Thames estuary.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig07
FIGURE 7
Decreasing sediment metabolism as a function of water depth for both oxygen uptake and total N2 production. Note the inverted triangles for the data from Sagami Bay (
Glud et al., 2009
), which have been omitted from the nonlinear regression. The data are plotted on a double common log scale, and the coefficients were derived using a simple power function. Data are from
Table 2
.
10.1128/9781555817145/f0213-01_thmb.gif
10.1128/9781555817145/f0213-01.gif
FIGURE 7
Decreasing sediment metabolism as a function of water depth for both oxygen uptake and total N2 production. Note the inverted triangles for the data from Sagami Bay ( Glud et al., 2009 ), which have been omitted from the nonlinear regression. The data are plotted on a double common log scale, and the coefficients were derived using a simple power function. Data are from Table 2 .
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig08
FIGURE 8
Relationships between N2 metabolisms and total sediment metabolism. (a) Total N2 production scattered against oxygen uptake. (b) Anammox against denitrification. Data have been normalized by common log transformation (log10+1), and the correlation coefficient (r) is given in each panel. In a, the open triangles mark the approximate range of data reported by
Seitzinger and Giblin (1996)
. The inset gives the relationship through the original linear data, where the slope (b
1) is equivalent to the ratio (as b
0 = 0) and ratio is equivalent to the pairwise comparison given in the text.
10.1128/9781555817145/f0216-01_thmb.gif
10.1128/9781555817145/f0216-01.gif
FIGURE 8
Relationships between N2 metabolisms and total sediment metabolism. (a) Total N2 production scattered against oxygen uptake. (b) Anammox against denitrification. Data have been normalized by common log transformation (log10+1), and the correlation coefficient (r) is given in each panel. In a, the open triangles mark the approximate range of data reported by Seitzinger and Giblin (1996) . The inset gives the relationship through the original linear data, where the slope (b 1) is equivalent to the ratio (as b 0 = 0) and ratio is equivalent to the pairwise comparison given in the text.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig09
FIGURE 9
Scatter plot of anammox as a function of denitrification to illustrate the bias toward denitrification in the sediment slurries in shallower water. Units for the intact sediment core data are µmol of N m–2 h–1 (as in
Fig. 8
b) and for the slurries are nmol of N cm–3 h–1 (as in
Fig. 5
). Data have been normalized by common log transformation (log10+1), and the correlation coefficient (r) is given in each case.
10.1128/9781555817145/f0217-01_thmb.gif
10.1128/9781555817145/f0217-01.gif
FIGURE 9
Scatter plot of anammox as a function of denitrification to illustrate the bias toward denitrification in the sediment slurries in shallower water. Units for the intact sediment core data are µmol of N m–2 h–1 (as in Fig. 8 b) and for the slurries are nmol of N cm–3 h–1 (as in Fig. 5 ). Data have been normalized by common log transformation (log10+1), and the correlation coefficient (r) is given in each case.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig10
FIGURE 10
Patterns of dissolved inorganic N species and oxygen within OMZs, made up from the available anammox database (see
Table 3
). (a, b) Nitrite and ammonium each as a function of oxygen, respectively. (c) Nitrite as a function of nitrate; the label for the nitrate axis in panel c is given as the primary axis in panel d. (d) Ammonium as a function of nitrite, with nitrite on the secondary axis.
10.1128/9781555817145/f0225-01_thmb.gif
10.1128/9781555817145/f0225-01.gif
FIGURE 10
Patterns of dissolved inorganic N species and oxygen within OMZs, made up from the available anammox database (see Table 3 ). (a, b) Nitrite and ammonium each as a function of oxygen, respectively. (c) Nitrite as a function of nitrate; the label for the nitrate axis in panel c is given as the primary axis in panel d. (d) Ammonium as a function of nitrite, with nitrite on the secondary axis.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig11
FIGURE 11
Anammox activity measured by enrichment with 15NH4
+ as a function of the concentration of ambient nitrite, made up from the available anammox database (see
Table 3
.). To illustrate the overall trend, two outliers have been removed that had activity of 170 and 270 nmol of N2 liter–1 day–1.
10.1128/9781555817145/f0227-01_thmb.gif
10.1128/9781555817145/f0227-01.gif
FIGURE 11
Anammox activity measured by enrichment with 15NH4 + as a function of the concentration of ambient nitrite, made up from the available anammox database (see Table 3 .). To illustrate the overall trend, two outliers have been removed that had activity of 170 and 270 nmol of N2 liter–1 day–1.
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09fig12
FIGURE 12
Anammox activity measured by enrichment with 15NH4
+ as a function of the concentration of ambient ammonium, made up from the available anammox database (see
Table 3
.).
10.1128/9781555817145/f0228-01_thmb.gif
10.1128/9781555817145/f0228-01.gif
FIGURE 12
Anammox activity measured by enrichment with 15NH4 + as a function of the concentration of ambient ammonium, made up from the available anammox database (see Table 3 .).
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
References
/content/book/10.1128/9781555817145.ch09
1.
Aller, R. C.,, P. O. J. Hall,, P. D. Rude, and, J. Y. Aller. 1998. Bigoechemical heterogeneity and suboxic diagenesis in hemipelagic sediments of the Panama basin. Deep Sea Res. Part I 45: 133– 165.
2.
Andersson, H. J.,, J. W. M. Wijsman,, P. M. J. Herman,, J. J. Middelburg,, K. Soetaert, and, C. Heip. 2004. Respiration patterns in the deep ocean. Geophys. Res. Lett. 31: L03304.
3.
Bender, M.,, R. Jahnke,, R. Weiss,, W. Martin,, D. T. Heggie,, J. Orchardo, and, T. Sowers. 1989. Organic carbon oxidation and benthic nitrogen and silica dynamics in San Clemente Basin, a continental borderline site. Geochim. Cosmochim. Acta 53: 685– 697.
4.
Blaszczyk, M. 1993. Effect of medium composition on the denitrification of nitrate by Paracoccus denitrificans. Appl. Environ. Microbiol. 59: 3951– 3953.
5.
Brettar, I.,, and G. Rheinheimer. 1991. Denitrification in the Central Baltic: evidence for H 2S-oxidation as a motor for denitrification at the oxic-anoxic interface. Mar. Ecol. Prog. Ser. 77: 157– 169.
6.
Brunet, R. C.,, and L. J. Garcia-Gil. 1996. Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments. FEMS Microbiol. Ecol. 21: 131– 138.
7.
Chang, B. X.,, and A. H. Devol. 2009. Seasonal and spatial patterns of sedimentary denitrification rates in the Chukchi sea. Deep Sea Res. Part II 56: 1339– 1350.
8.
Christensen, P. B.,, S. Rysgaard,, N. P. Sloth,, T. Dalsgaard, and, S. Schwæter. 2000. Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aquat. Microb. Ecol. 21: 73– 84.
9.
Codispoti, L. A. 2006. An oceanic fixed nitrogen sink exceeding 400 Tg Na –1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosci. Disc. 3: 1203– 1246.
10.
Codispoti, L. A.,, J. A. Brandes,, J. P. Christensen,, A. H. Devol,, S. W. A. Naqvi,, H. W. Paerl, and, T. Yoshinari. 2001. The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene? Sci. Mar. 65: 85– 105.
11.
Codispoti, L. A.,, and J. P. Christensen. 1985. Nitrification, denitrification and nitrous oxide cycling in the eastern tropical south Pacific Ocean. Mar. Chem. 16: 277– 300.
12.
Conley, D. J.,, H. W. Paerl,, R. W. Howarth,, D. F. Boesch,, S. P. Seitzinger,, K. E. Havens,, C. Lancelot, and, G. E. Likens. 2009. Ecology. Controlling eutrophication: nitrogen and phosphorus. Science 323: 1014– 1015.
13.
Dale, O. R.,, C. R. Tobias, and, B. K. Song. 2009. Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ. Microbiol. 11: 1194– 1207.
14.
Dalsgaard, T.,, and B. Thamdrup. 2002. Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl. Environ. Microbiol. 68: 3802– 3808.
15.
Dalsgaard, T.,, D. E. Canfield,, J. Petersen,, B. Thamdrup, and, J. Acuña-González. 2003. N 2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422: 606– 608.
16.
Dalsgaard, T.,, B. Thamdrup, and, D. E. Canfield. 2005. Anaerobic ammonium oxidation (anammox) in the marine environment. Res. Microbial. 156: 457– 464.
17.
Devol, A. H. 2003. Nitrogen cycle—solution to a marine mystery. Nature 422: 575– 576.
18.
Devol, A. H.,, A. G. Uhlenhopp,, S. W. A. Naqvi,, J. A. Brandes,, D. A. Jayakumar,, H. Naik,, S. Gaurin,, L. A. Codispoti, and, T. Yoshinari. 2006. Denitrification rates and excess nitrogen gas concentrations in the Arabian Sea oxygen deficient zone. Deep Sea Res. Part II 53: 1533– 1547.
19.
Diaz, R. J.,, and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321: 926– 929.
20.
Dollar, S. J.,, S. V. Smith,, S. M. Vink,, S. Brebski, and, J. T. Hollibaugh. 1991. Annual cycle of benthic nutrient fluxes in Tomales Bay, California, and contribution of the benthos to total ecosystem metabolism. Mar. Ecol. Prog. Ser. 79: 115– 125.
21.
Dong, L. F.,, C. J. Smith,, S. Papaspyrou,, A. Stott,, M. A. Osborn, and, D. B. Nedwell. 2009. Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne Estuary, United Kingdom). Appl. Environ. Microbiol. 75: 3171– 3179.
22.
Engström, P. 2004. The importance of anaerobic ammonium oxidation (anammox) and anoxic nitrification for N removal in coastal marine sediments. Ph.D. thesis. University of Gothenburg, Gothenburg, Sweden.
23.
Engström, P.,, T. Dalsgaard,, S. Hulth, and, R. C. Aller. 2005. Anaerobic ammonium oxidation by nitrite (anammox): implications for N 2 production in coastal marine sediments. Geochim. Cosmochim. Acta 69: 2057– 2065.
24.
Engström, P.,, C. R. Penton, and, A. H. Devol. 2009. Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol. Oceanogr. 54: 1643– 1652.
25.
Falkowski, P. G. 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO 2 in the ocean. Nature 387: 272– 275.
26.
Farias, L.,, M. Castro-Gonzalez,, M. Cornejo,, J. Charpentier,, J. Faundez,, N. Boontanon, and, N. Yoshida. 2009. Denitrification and nitrous oxide cycling within the upper oxycline of the eastern tropical South Pacific oxygen minimum zone. Limnol. Oceanogr. 54: 132– 144.
27.
Fernandez-Polanco, F.,, M. Fernandez-Polanco,, N. Fernandez,, M. A. Uruena,, P. A. Garcia, and, S. Villaverde. 2001. New process for simultaneous removal of nitrogen and sulphur under anaerobic conditions. Water Res. 35: 1111– 1114.
28.
Fossing, H.,, V. A. Gallardo,, B. B. Jørgensen,, M. Huttel,, L. P. Nielsen, and, H. Schulz. 1995. Concentration and transport of nitrate by the mat-forming sulfur bacterium Thioploca. Nature 374: 713– 715.
29.
Francis, C. A.,, J. M. Beman, and, M. M. M. Kuypers. 2007. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1: 19– 27.
30.
Fuchsman, C. A.,, J. W. Murray, and, S. K. Konovalov. 2008. Concentration and natural stable isotope profiles of nitrogen species in the Black Sea. Mar. Chem. 111: 90– 105.
31.
Galan, A.,, V. Molina,, B. Thamdrup,, D. Woebken,, G. Lavik,, M. M. M. Kuypers, and, O. Ulloa. 2009. Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile. Deep Sea Res. Part II 56: 1021– 1031.
32.
Glud, R. N. 2008. Oxygen dynamics of marine sediments. Mar. Biol. Res. 4: 165– 179.
33.
Glud, R. N.,, B. Thamdrup,, H. Stahl,, F. Wenzhoefer,, A. Glud,, H. Nomaki,, K. Oguri,, N. P. Revsbech, and, H. Kitazato. 2009. Nitrogen cycling in a deep ocean margin sediment (Sagami Bay, Japan). Limnol. Oceanogr. 54: 723– 734.
34.
Gruber, N.,, and J. L. Sarmiento. 1997. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11: 235– 266.
35.
Güven, D.,, A. Dapena,, B. Kartal,, M. C. Schmind,, B. Maas,, K. van de Pas-Schoonen,, S. Sozen,, R. Mendez,, H. J. M. Op den Camp,, M. S. M. Jetten,, M. Strous, and, I. Schmidt. 2005. Propionate oxidation by and methanol inhibition of anaerobic ammonium-oxidizing bacteria. Appl. Environ. Microbiol. 71: 1066– 1071.
36.
Halm, H.,, N. Musat,, P. Lam,, R. Langlois,, F. Musat,, S. Peduzzi,, G. Lavik,, C. J. Schubert,, B. Singha,, J. LaRoche, and, M. M. M. Kuypers. 2009. Cooccurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ. Microbiol. 11: 1945– 1958.
37.
Hamersley, M. R.,, G. Lavik,, D. Woebken,, J. E. Rattray,, P. Lam,, E. C. Hopmans,, J. S. Sinninghe Damste,, S. Kruger,, M. Graco,, D. Gutierrez, and, M. M. M. Kuypers. 2007. Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol. Oceanogr. 52: 923– 933.
38.
Hannig, M.,, G. Lavik,, M. M. M. Kuypers,, D. Woebken,, W. Martens-Habbena, and, K. Juergens. 2007. Shift from denitrification to anammox after inflow events in the central Baltic Sea. Limnol. Oceanogr. 52: 1336– 1345.
39.
Hartnett, H. E.,, and A. H. Devol. 2003. Role of a strong oxygen-deficient zone in the preservation and degradation of organic matter: a carbon budget for the continental margins of northwest Mexico and Washington State. Geochim. Cosmochim. Acta 67: 247– 264.
40.
Hauck, R. D.,, S. W. Melsted, and, P. E. Yankwich. 1958. Use of N-isotope distribution in nitrogen gas in the study of denitrification. Soil Sci. 86: 287– 296.
41.
Hietanen, S. 2007. Anaerobic ammonium oxidation (anammox) in sediments of the Gulf of Finland. Aquat. Microb. Ecol. 48: 197– 205.
42.
Hietanen, S.,, and J. Kuparinen. 2008. Seasonal and short-term variation in denitrification and anammox at a coastal station on the Gulf of Finland, Baltic Sea. Hydrobiologia 596: 67– 77.
43.
Holmes, R. M.,, A. Aminot,, R. Kerouel,, B. A. Hooker, and, B. J. Peterson. 1999. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish Aquat. Sci. 56: 1801– 1808.
44.
Hulth, S.,, R. C. Aller, and, F. Gilbert. 1999. Coupled anoxic nitrification manganese reduction in marine sediments. Geochim. Cosmochim. Acta 63: 49– 66.
45.
Jaeschke, A.,, C. Rooks,, M. Trimmer,, J. C. Nicholls,, E. C. Hopmans,, S. Schouten, and, J. S. Sinninghe Damsté. 2009. Comparison of ladderane phospholipid and core lipids as indicators for anaerobic ammonium oxidation (anammox) in marine sediments. Geochim. Cosmochim. Acta 73: 2077– 2088.
46.
Jensen, M. M.,, M. M. M. Kuypers,, G. Lavik, and, B. Thamdrup. 2008. Rates and regulation of anaerobic ammonium oxidation and denitrification in the Black Sea. Limnol. Oceanogr. 53: 23– 36.
47.
Jensen, M.,, J. Petersen,, T. Dalsgaard, and, B. Thamdrup. 2009. Pathways, rates, and regulation of N 2 production in the chemocline of an anoxic basin, Mariager Fjord, Denmark. Mar. Chem. 113: 102– 113.
48.
Joye, S. B.,, and J. T. Hollibaugh. 1995. Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270: 623– 625.
49.
Kartal, B.,, M. M. M. Kuypers,, G. Lavik,, J. Schalk,, H. J. M. Op den Camp,, M. S. M. Jetten, and, M. Strous. 2007. Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ. Microbiol. 9: 635– 642.
50.
Konovalov, S. K.,, C. A. Fuchsman,, V. Belokopitov, and, J. W. Murray. 2008. Modeling the distribution of nitrogen species and isotopes in the water column of the Black Sea. Mar. Chem. 111: 106– 124.
51.
Koop-Jakobsen, K.,, and A. E. Giblin. 2009. Anammox in tidal marsh sediments: the role of salinity, nitrogen loading, and marsh vegetation. Estuar. Coasts 32: 238– 245.
52.
Körner, H.,, and W. G. Zumft. 1989. Expression of denitrification enzymes in response to the dissolved oxygen level and respiratory substrate in continuous culture of Pseudomonas stutzeri. Appl. Environ. Microbiol. 55: 1670– 1676.
53.
Kuypers, M. M. M.,, A. O. Sliekers,, G. Lavik,, M. Schmid,, B. Barker Jørgensen,, J. G. Kuenen,, J. S. Sinninghe Damsté,, M. Strous, and, M. S. M. Jetten. 2003. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422: 608– 611.
54.
Kuypers, M. M. M.,, G. Lavik,, D. Woebken,, M. Schmid,, B. M. Fuchs,, R. Amann,, B. Barker Jørgensen, and, M. S. M. Jetten. 2005. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102: 6478– 6483.
55.
Lam, P.,, M. M. Jensen,, G. Lavik,, D. F. McGinnis,, B. Muller,, C. J. Schubert,, R. Amann,, B. Thamdrup, and, M. M. M. Kuypers. 2007. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl. Acad. Sci. USA 104: 7104– 7109.
56.
Lam, P.,, G. Lavik,, M. M. Jensen,, J. van de Vossenberg,, M. Schmid,, D. Woebken,, D. Gutierrez,, R. Amann,, M. S. M. Jetten, and, M. M. M. Kuypers. 2009. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc. Natl. Acad. Sci. USA 106: 4752– 4757.
57.
Lavik, G.,, T. Stuhrmann,, V. Bruchert,, A. Van der Plas,, V. Mohrholz,, P. Lam,, M. Mußmann,, B. M. Fuchs,, R. Amann,, U. Lass, and, M. M. M. Kuypers. 2009. Detoxification of sulphidic African shelf waters by blooming chemolithotrophs. Nature 457: 581– 584.
58.
Lohse, L.,, H. F. P. Malschaert,, C. P. Slomp,, W. Helder, and, W. van Raaphorst. 1993. Nitrogen cycling in North Sea sediments: interaction of denitrification and nitrification in offshore and coastal areas. Mar. Ecol. Prog. Ser. 101: 283– 296.
59.
Meyer, R. L.,, N. Risgaard-Petersen, and, D. E. Allen. 2005. Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl. Environ. Microbiol. 71: 6142– 6149.
60.
Middelburg, J. J.,, K. Soetart,, P. M. J. Herman, and, C. H. R. Heip. 1996. Denitrification in marine sediments: a model study. Glob. Biogeochem. Cycles 10: 661– 673.
61.
Minjeaud, L.,, P. C. Bonin, and, V. D. Michotey. 2008. Nitrogen fluxes from marine sediments: quantification of the associated co-occurring bacterial processes. Biogeochemistry 90: 141– 157.
62.
Molina, V.,, and L. Farías. 2009. Aerobic ammonium oxidation in the oxycline and oxygen minimum zone of the eastern tropical South Pacific off northern Chile (~20°S). Deep Sea Res. Part II 56: 1032– 1041.
63.
Morrison, J. M.,, L. A. Codispoti,, S. L. Smith,, K. Wishner,, C. Flagg,, W. D. Gardner,, S. Gaurin,, S. W. A. Naqvi,, V. Manghnani,, L. Prosperie, and, J. S. Gunderson. 1999. The oxygen minimum zone in the Arabian Sea during 1995. Deep Sea Res. Part II 46: 1903– 1931.
64.
Mulder, A.,, A. A. van de Graaf,, L. A. Robertson, and, J. G. Kuenen. 1995. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol. Ecol. 16: 177– 184.
65.
Naqvi, S. W. A.,, R. J. Noronha,, M. S. Shailaja,, K. Somasunda, and, R. S. Gupta. 1992. Some aspects of the nitrogen cycling in the Arabian Sea, p. 285–311. In B. N. Desai (ed.), Oceanography of the Indian Ocean. Oxford and IBH Publishers, New Delhi, India.
66.
Naqvi, S. W. A.,, D. A. Jayakumar,, P. V. Narvekar,, H. Naik,, V. V. S. S. Sarma,, W. D. D’Souza, and, J. M. D. George. 2000. Increased marine production of N 2O due to intensifying anoxia on the Indian continental shelf. Nature 408: 346– 349.
67.
Nedwell, D. B.,, L. F. Dong,, A. Sage, and, G. J. C. Underwood. 2002. Variations of the nutrients loads to the mainland U.K. estuaries: correlation with catchment areas, urbanization and coastal eutrophication. Estuar. Coast. Shelf Sci. 54: 951– 970.
68.
Nicholls, J. C.,, C. A. Davies, and, M. Trimmer. 2007. High resolution profiles and nitrogen isotope tracing reveal and dominant source of nitrous oxide and multiple pathways of nitrogen gas production in the central Arabian Sea. Limnol. Oceanogr. 52: 156– 168.
69.
Nicholls, J. C.,, and M. Trimmer. 2009. Widespread relationship between the anammox reaction and organic carbon in estuarine sediments. Aquat. Microb. Ecol. 55: 105– 113.
70.
Nielsen, L. P. 1992. Denitrification in sediments determined from nitrogen isotope pairing. FEMS Microbiol. Ecol. 86: 357– 362.
71.
Nishio, T.,, I. Koike, and, A. Hattori. 1982. Denitrification, nitrate reduction, and oxygen consumption in coastal and estuarine sediments. Appl. Environ. Microbiol. 43: 648– 653.
72.
Ogilvie, B.,, D. B. Nedwell,, R. M. Harrison,, A. Robinson, and, A. Sage. 1997. High nitrate, muddy estuaries as nitrogen sinks: the nitrogen budget of the River Colne estuary (United Kingdom). Mar. Ecol. Prog. Ser. 150: 217– 228.
73.
Paulmier, A.,, and D. Ruiz-Pino. 2009. Oxygen minimum zones (OMZs) in the modern ocean. Prog. Oceanogr. 80: 113– 128.
74.
Peirels, B.,, N. Caraco,, M. Pace, and, J. Cole. 1991. Human influence on river nitrogen. Nature 350: 386– 387.
75.
Reimers, C. E.,, R. A. Jahnke, and, D. C. McCorkel. 1992. Carbon fluxes and burial rates over the continental slope of California with implications for the global carbon cycle. Glob. Biogeochem. Cycles 6: 199– 224.
76.
Revsbech, N. P.,, N. Risgaard-Petersen,, A. Schramm, and, L. P. Nielsen. 2006. Nitrogen transformations in stratified aquatic microbial ecosystems. Antonie Leeuwenhoek Int. J. G. 90: 361– 375.
77.
Rich, J. J.,, O. R. Dale.,, B. Song., and, B. B. Ward. 2008. Anaerobic ammonium oxidation in Chesapeake Bay sediments. Microbial. Ecol. 55: 311– 320.
78.
Richards, F. A.,, J. D. Cline,, W. W. Broenkow, and, L. P. Atkinson. 1965. Some consequences of the decomposition of organic matter in Lake Nitinat, an anoxic fjord. Limnol. Oceanogr. 10: R185– R201.
79.
Risgaard-Petersen, N.,, L. P. Nielsen,, S. Rysgaard,, T. Dalsgaard, and, R. L. Meyer. 2003. Application of the isotope pairing technique in sediments where anammox and denitrification coexist. Limnol. Oceanogr. Methods 1: 63– 73.
80.
Risgaard-Peterson, N.,, R. L. Meyer,, M. Schmid,, M. S. M. Jetten,, A. Enrich-Prast,, S. Rysgaard, and, N. P. Revsbech. 2004. Anaerobic ammonium oxidation in an estuarine sediment. Aquat. Microb. Ecol. 36: 293– 304.
81.
Risgaard-Peterson, N.,, R. L. Meyer, and, M. N. P. Revsbech. 2005. Denitrification and anaerobic ammonium oxidation in sediments: effects of microphytobenthos and NO 3 –. Aquat. Microbiol. Ecol. 40: 67– 76.
82.
Risgaard-Petersen, N.,, A. M. Langezaal,, S. Ingvardsen,, M. C. Schmid,, M. S. M. Jetten,, H. J. M. Op den Camp,, J. W. M. Derksen,, E. Piña-Ocho,, S. P. Eriksson,, L. P. Nielsen,, N. P. Revsbech,, T. Cedhagen, and, G. J. van der Zwaan. 2006. Evidence for complete denitrification in a benthic foraminifer. Nature 443: 93– 96.
83.
Rysgaard, S.,, R. N. Glud,, N. Risgaard-Petersen, and, T. Dalsgaard. 2004. Denitrification and anammox activity in Arctic marine sediments. Limnol. Oceanogr. 49: 1493– 1502.
84.
Sanders, I. A.,, and M. Trimmer. 2006. In-situ application of 15NO 3 – isotope pairing technique to measure denitrification in sediments at the surface water-groundwater interface. Limnol. Oceanog. Methods 4: 142– 152.
85.
Sayama, M.,, N. Risgaard-Petersen,, L. P. Nielsen,, H. Fossing, and, P. B. Christensen. 2005. Impact of bacterial NO 3 – transport on sediment biogeochemistry. Appl. Environ. Microbiol. 71: 7575– 7577.
86.
Schrum, H. N.,, A. J. Spivack,, M. Kastner, and, S. D’Holt. 2009. Sulfate-reducing ammonium oxidation: a thermodynamically feasible metabolic pathway in subseafloor sediment. Geology 37: 939– 942.
87.
Schubert, C. J.,, E. Durisch-Kaiser,, B. Wehrli,, B. Thamdrup,, P. Lam, and, M. M. M. Kuypers. 2006. Anaerobic ammonium oxidation in a tropical fresh water system (Lake Tanganyika). Environ. Microbiol. 10: 1857– 1863.
88.
Seitzinger, S. P. 1988. Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol. Oceanogr. 33: 702– 724.
89.
Seitzinger, S. P.,, and A. E. Giblin. 1996. Estimating denitrification in North Atlantic continental shelf sediments. Biogeochemistry 35: 235– 260.
90.
Smethie, W. M. 1987. Nutrient regeneration and denitrification in low oxygen fjords. Deep Sea Res. 34: 983– 1006.
91.
Steif, P.,, D. De Beer, and, D. Neumann. 2002. Small-scale distribution of interstitial nitrite in freshwater sediment microcosms: the role of nitrate and oxygen availability, and sediment permeability. Microbiol. Ecol. 43: 367– 378.
92.
Steingruber, S. M.,, J. Freidrich,, R. Gächter, and, B. Wehrli. 2001. Measurements of denitrification in sediments with the 15N isotope pairing technique. Appl. Environ. Microbiol. 67: 3771– 3778.
93.
Stramma, L.,, C. G. C. Johnson,, J. Sprintall, and, V. Mohrholz. 2008. Expanding oxygen-minimum zones in the tropical oceans. Science 320: 655– 658.
94.
Strous, M.,, J. G. Kuenen, and, M. S. M. Jetten. 1999. Key physiology of anaerobic ammonium oxidation. Appl. Environ. Microbiol. 65: 3248– 3250.
95.
Sørensen, J.,, L. K. Rasmussen, and, I. Koike. 1987. Micromolar sulfide concentrations alleviate acetylene blockage of nitrous oxide reduction by denitrifying Pseudomonas fluorescens. Can. J. Microbiol. 33: 1001– 1005.
96.
Tal, Y.,, J. E. M. Watts, and, H. J. Schreier. 2005. Anaerobic ammonia-oxidizing bacteria and related activity in Baltimore Inner Harbor Sediment. Appl. Environ. Microbiol. 71: 1816– 1821.
97.
Thamdrup, B.,, and T. Dalsgaard. 2002. Production of N 2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl. Environ. Microbiol. 68: 1312– 1318.
98.
Thamdrup, B.,, T. Dalsgaard,, M. M. Jensen,, O. Ulloa,, L. Farías, and, R. Escribano. 2006. Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnol. Oceanogr. 51: 2145– 2156.
99.
Trimmer, M.,, and J. C. Nicholls. 2009. Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnol. Oceanog. 54: 577– 589.
100.
Trimmer, M.,, J. C. Nicholls, and, B. Deflandre. 2003. Anaerobic ammonium oxidation measured in sediments along the Thames Estuary, United Kingdom. Appl. Environ. Microbiol. 69: 6447– 6454.
101.
Trimmer, M.,, J. C. Nicholls,, N. Morley,, C. A. Davies, and, J. Aldridge. 2005. Biphasic behavior of anammox regulated by nitrate and nitrite in an estuarine sediment. Appl. Environ. Microbiol. 71: 1923– 1930.
102.
Trimmer, M.,, N. Risgaard-Petersen,, J. C. Nicholls, and, P. Engström. 2006. Direct measurement of anaerobic ammonium oxidation (anammox) and denitrification in intact sediment cores. Mar. Ecol. Prog. Ser. 326: 37– 47.
103.
van de Graaf, A. A.,, A. Mulder,, P. De Bruijn,, M. S. M. Jetten,, L. A. Robertson, and, J. G. Kuenen. 1995. Anaerobic oxidation of ammonium is a biologically mediated process. Appl. Environ. Microbiol. 61: 1246– 1251.
104.
van Raaphorst, W.,, H. T. Kloosterhuis,, E. M. Berghuis,, A. J. M. Gieles,, J. F. P. Malschaert, and, G. J. van Noort. 1992. Nitrogen cycling in two types of sediments of the southern North Sea (Frisian Front, Broad Fourteens): field data and mesocosm results. Neth. J. Sea. Res. 28: 293– 316.
105.
Ward, B. B.,, C. B. Tuit,, A. Jayakumar,, J. J. Rich,, J. Moffett,, S. Wajih, and, A. Naqvi. 2008. Organic carbon, and not copper, controls denitrification in oxygen minimum zones of the ocean. Deep Sea Res., Part I 55: 1672– 1683.
106.
Ward, B. B.,, A. H. Devol,, J. J. Rich,, B. X. Chang,, S. E. Bulow,, H. Naik,, A. Pratihary, and, A. Jayakumar. 2009. Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461: 78– 82.
107.
Wenjing, J.,, N. Tovell,, S. Clegg,, M. Trimmer, and, J. A. Cole. 2008. A single channel for nitrate uptake, nitrite export and nitrite uptake by Escherichia coli NarU and a role for NirC in nitrite export and uptake. Biochem. J. 417: 295– 304.
108.
Wenzhöfer, F.,, and R. N. Glud. 2002. Benthic carbon mineralization in the Atlantic: a synthesis based on in situ data from the last decade. Deep Sea Res. Part I 49: 1255– 1279.
109.
Zhang, Y.,, X.-H. Ruan,, H. J. M. Op den Camp,, T. J. M. Smits,, M. S. M. Jetten, and, M. C. Schmid. 2007. Diversity and abundance of aerobic and anaerobic ammonium-oxidizing bacteria in freshwater sediments of the Xinyi River (China). Environ. Microbiol. 9: 2375– 2382.
110.
Zumft, W. G. 1997. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61: 533– 616.
Tables
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments
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Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09tab01
TABLE 1
Published and unpublished rates of anammox and denitrification measured in anoxic homogenized or slurrified sediment
a
TABLE 1
Published and unpublished rates of anammox and denitrification measured in anoxic homogenized or slurrified sediment a
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09tab02
TABLE 2
Published and unpublished rates of sedimentary oxygen uptake and anammox and denitrification measured in intact sediment cores
a
TABLE 2
Published and unpublished rates of sedimentary oxygen uptake and anammox and denitrification measured in intact sediment cores a
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9
/content/10.1128/9781555817145.ch09.ch09tab03
TABLE 3
Published anammox and denitrification rates measured with 15N-stable isotopes in water column OMZs
a
TABLE 3
Published anammox and denitrification rates measured with 15N-stable isotopes in water column OMZs a
Citation:
Trimmer M, Engström P.
2011.
Distribution, Activity, and Ecology of Anammox Bacteria in Aquatic Environments,
p 201-235.
In
Ward B, Arp D, Klotz M (ed),
Nitrification.
ASM Press, Washington, DC.
doi: 10.1128/9781555817145.ch9