No Nitrification in Lakes Below pH 3 - Environmental Science

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No Nitrification in Lakes Below pH 3 Christina Jeschke,*,† Carmen Falagán,‡ Kay Knöller,† Martin Schultze,§ and Matthias Koschorreck§ †

UFZ − Helmholtz Centre for Environmental Research, Department of Catchment Hydrology, Theodor-Lieser-Strasse 4, D-06120 Halle, Germany ‡ Geological Survey of Spain (IGME) C/Ríos Rosas 23, 28003 Madrid, Spain § UFZ − Helmholtz Centre for Environmental Research, Department of Lake Research, Brueckstrasse 3a, D-39114 Magdeburg, Germany ABSTRACT: Lakes affected by acid mine drainage (AMD) or acid rain often contain elevated concentrations of ammonium, which threatens water quality. It is commonly assumed that this is due to the inhibition of microbial nitrification in acidic water, but nitrification was never directly measured in mine pit lakes. For the first time, we measured nitrification by 15NH4Cl isotope tracer addition in acidic as well as neutral mine pit lakes in Spain and Germany. Nitrification activity was only detected in neutral lakes. In acidic lakes no conversion of 15 NH4+ to 15NO3− was observed. This was true both for the water column as well as for biofilms on the surface of macrophytes or dead wood and the oxic surface layer of the sediment. Stable isotope analysis of nitrate showed 18O values typical for nitrification only in neutral lakes. In a comparison of NH4+ concentrations in 297 surface waters with different pH, ammonium concentrations higher 10 mg NH4−N L−1 were only observed in lakes below pH 3. On the basis of the results from stable isotope investigations and the examination of a metadata set we conclude that the lower limit for nitrification in lakes is around pH 3.

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Acid tolerant nitrifiers have been isolated12,13 and both nitrifying prokaryotes and archaea have been detected in soils at pH 4 by molecular methods.10,14 Archaea, which are able to oxidize ammonia, seem to be less affected by low pH than bacteria.15 Growth in aggregates or biofilms seems to support the pH-resistance of nitrifiers.16−18 A Nitrosospira strain nitrified urea but not NH4+ at pH 4.5.19 Thus acid tolerant nitrifiers do exist, but the pH limit of nitrification is not known. There are several methods available to measure nitrification in aquatic systems, including nitrogen inventories using inhibitors, 14CO2 uptake in the dark, or using different 15N tracers.20 A direct proof, however, is the application of 15NH4+ tracer; thereby the formed 15NO3 will be detected. This approach is especially feasible in ammonium rich lakes, where a stimulation of the nitrification activity by added 15NH4+ does not occur. The goal of the present study was to test the hypothesis that elevated ammonium concentrations in acidic mine pit lakes are caused by the absence of microbial nitrification. We sampled different acidic mine pit lakes in Europe and, as a control, two neutral mine pit lakes, and detected nitrification activity with a 15 N tracer technique. By combining results from the isotope studies with a database of ammonium concentrations in lakes at

INTRODUCTION Lakes which have developed in former lignite mine pits are often acidic (pH < 3) and contain high concentrations of sulfate and iron.1 These acidic mine waters represent an environmental problem in mining regions worldwide. Besides high acidity and metal contents, these waters typically contain elevated concentrations of ammonium while nitrate is at the detection limit. The same is true for natural lakes which have been acidified by acid rain.2 The mean ammonium concentration of pit lakes in former coal and lignite mines with pH < 3.5 was 3.15 ± 3.68 mg NH4− N L−1 (n = 96) while the pit-lakes with pH > 3.5 contained 0.44 ± 0.76 mg NH4−N L−1 (n = 136).3 In comparison the mean ammonium concentration of 1098 European lakes was 0.08 ± 0.21 mg NH4−N L−1.4 It is commonly assumed that the high ammonium concentration is caused by an inhibition of nitrification at low pH. In laboratory incubations of acidic mine lake water, nitrate and ammonium concentrations did not change over a period of two weeks.5 The concentration of ammonium and nitrate in lakes, however, is a result of the several processes occurring simultaneously. Thus, nitrification cannot be inferred from concentration changes of nitrate and/ or ammonium alone. Definitive evidence, that nitrification does not occur in extremely acidic lakes is still missing. Nitrifying microbes are known to be inhibited at low pH.6,7 The inhibition is caused by the shift from free ammonia (NH3), which is the substrate used by nitrifying microbes,8 to ammonium (NH4+) at low pH. There are, however, reports of nitrification occurring in acidic soils9,10 and bioreactors.11 © 2013 American Chemical Society

Received: Revised: Accepted: Published: 14018

May 15, 2013 November 8, 2013 November 15, 2013 November 15, 2013 dx.doi.org/10.1021/es402179v | Environ. Sci. Technol. 2013, 47, 14018−14023

Environmental Science & Technology

Article

Table 1. Location and Physicochemical Characteristics of the Lakes Sampled for Nitrification Measurementsa lake (sampling date)

UTM coordinates [zone/E/N]

lake area [ha]

sampling depth [m]

temperature [°C]

pH

O2 [mg/L]

NH4+ [mg/L]

NO3− [mg/L]

10

1 5 10 7 20 50 3 8.5 35 1 1 1 11 15 26 29 32

18.1 12.7 6.5 24.7 15.2 nd 24.2 15.2 nd 21.5 20.1 19.2 9.8 9.7 5.5 5.5 5.5

2.7 2.7 3.1 2.7 4.1 nd 2.8 2.8 nd 2.9 3.2 7.8 6.7 6.4 7.7 7.6 7.6

8.4 12.0 0.6 13.24 0.07 nd 8.1 1.02 nd 7.8 7.4 9.1 5.3 4.4 2 1.5 0.5

2.71 2.73 nd 0.15 0.54 nd 0.13 0.1 nd 3.56 2.28 0.07 0.06 0.08 0.035 0.26 0.46

0.84 0.82 nd 1.11 98%), so that 10% of the NH4+ concentration was labeled. The labeled water was distributed across at least three replicate glass bottles. One of them was set up as a control by adding the nitrification inhibitor allylthiourea (ATU) (10 mg L−1 final concentration). Subsequently the bottles were incubated in the laboratory at room temperature in the dark for at least 20 to 24 h. In Lake Senftenberg, the bottles were incubated in situ in the lake at the original water depth. In Lake Sedlitz and Lake Partwitz we added small pieces of dead wood or reed to check for nitrification activity in epiphytic biofilms. The bottles were sampled at the beginning and the end of incubation as described below. Sedimentary nitrification was measured in slurry incubations with four replicates, including one inhibited control. In the laboratory, slurries prepared by adding 30 mL of bottom water to 30 mL of sediment were preincubated for 24 h in Erlenmeyer flasks with cotton plugs on a rotary shaker (100 rpm) at room temperature. Before the incubation in the dark started, in the slurries the nitrate/nitrite content was raised by 25% with a KNO3 solution (1.012 g/100 mL) as the samples did not contain enough nitrate/nitrite for the NOx− isotope analysis. This should have no effect on the nitrification rate, but improved the analytical measurements of 15NOx−. The incubation was continued by adding 15NH4Cl stock solution, so that 10% of the NH4+ concentration was labeled. Samples were taken after start and end of incubation with a syringe, filtered (0.2 μm) and stored at 4 °C until analysis. Samples from slurry incubations were centrifuged (10−15 min at 1544g) before filtration. Nitrification rates were calculated from the initial (15NOx−(i)) and final (15NOx−(f)) δ15N of dissolved nitrate, nitrate concentration (NOx−(f)), the quantity of added isotope tracer (α = 15N content of NH4+), and incubation time (d).30

nmol NO3L−1d−1 = [(%15NO−x(f) − %15NO−x(i))/d × NO−x(f)] × 1000/α

(2)

The isotopic analysis results were converted from per thousand to percent by multiplying of relative abundance. According to 15N analysis precision, the smallest measurable change in 15NOx− was 0.4 ‰ (i.e., all incubations with a smaller difference than 0.4 ‰ had a nitrification rate below the detection limit). Since the detection limit also depends on the nitrate concentration, the absolute detection limit in the different lakes differed between 0.2 nmol L−1 d−1 in Lake Partwitz and Sedlitz and about 100 nmol L−1 d−1 in the Spanish lakes and ML 111.

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RESULTS AND DISCUSSION In all acidic lakes the nitrification rate was below the detection limit (Table 2). This was true for the water, sediment and periphyton. Nitrification, as indicated by an appreciable enrichment of δ15N in dissolved NOx− during incubation with 15NH4+, was only detected in neutral lakes. Addition of ATU completely inhibited nitrification within the neutral lakes. The nitrification rates in Lake Senftenberg and Lake Runstedt corresponded to literature values.31−34 In Lake Runstedt, the nitrification experiment was repeated in summer with water from three depths (18 m, 25 m, 32 m) but under laboratory temperature (25 °C). Nitrification rates ranged between 545 nmol NO3 L−1d−1and 5798 nmol NO3 L−1d−1 in the deep water. As microbes living in biofilms may be protected against low pH,35 we looked for nitrification activity on the surface of dead wood and reeds. When pieces of dead wood or reed were added to incubations of water from the acidic Lakes Sedlitz and Partwitz, no formation of 15NOx− from 15NH4+ was observed. 14020

dx.doi.org/10.1021/es402179v | Environ. Sci. Technol. 2013, 47, 14018−14023


Article

8‰37,38 and −5 to 15‰,39 respectively. The oxygen-isotopes values of nitrate from the acid lakes were all higher than 15‰, only some values from Lake Sedlitz (13.4‰) were close to the range expected for nitrification. One explanation for this might be the origin of the dissolved nitrate. The oxygen-isotope values from Lake Sedlitz are typical for groundwater and/or ammonium conversion in soil.39,40 This assumption appears to be supported by the fact that the lake was in the process of flooding. In a preliminary experiment with water from the neutral Lake Runstedt the δ18O-values (4.9−7.0 ‰) were in the range indicative of nitrification (data not shown). In Figure 1 the neutral water of Lake Senftenberg showed isotopic values typical of nitrification. Additionally, δ15N in dissolved nitrate at 11 and 15 m depth was significantly enriched. The comparison of the initial and final 15NOx− content of the incubated water confirms that Lake Senftenberg was the only location where 15 NOx− was produced from the added 15NH4+. In the samples from Lake Partwitz the strong enrichment of δ18O-values indicated a clear influence of nitrate from precipitation compared to the other lakes. The shallow bay that we sampled in that lake was probably influenced by surface runoff or groundwater infiltration. Acidic mine pit lakes often contain elevated concentrations of metals. Thus, it might be possible that nitrification in these lakes is not directly inhibited by the high proton concentration but indirectly via inhibitory metal concentrations. We can exclude this for the German lignite mine lakes which contain only low concentrations of heavy metals.1 The Spanish lakes, however, contain potentially toxic concentrations of heavy metals22 and we cannot distinguish whether nitrification in these lakes was directly affected by the pH or indirectly by the high metal concentrations. Having clearly shown that nitrification does not occur in extremely acidic lakes, we may determine the lower pH limit for nitrification in lakes by plotting the ammonium concentration of various lakes against their pH (Figure 2). Data of pit lakes from metal, coal and lignite mining and from volcanically influenced waters (mainly crater lakes) were considered. Only surface waters were included to ensure well oxygenated conditions. Elevated concentrations of ammonium in deeper layers may result from anoxic conditions, e.g. in monimolimnia of meromictic acid pit lakes. We also tested the relationship

We conclude that there was no nitrification activity in the epiphyton. A further potential site for nitrifying microorganisms might be the upper oxic layer of the sediment. In sediment slurries from the acidic Lake Sedlitz, formation of 15NOx− was below the detection limit (Table 3). In two samples from Lake Table 3. Nitrification Rate and Net Production of Ammonium in Sediment Slurries [nmol L−1d−1]a

a

lake

replicate 1

replicate 2

replicate 3

sedlitz partwitz runstedt

≤DL 95 259 000

≤DL ≤DL

≤DL 84

ATU control

NH4+ mineralization rate

≤DL 202 ≤DL

73 120 178 000

DL = detection limit.

Partwitz, as well as in the ATU control, a small enrichment of 15 NOx− was detected. Since this effect was also observed in the presence of ATU, it was probably caused by a consumption of NOx− during the assay which would result in an enrichment of heavier NOx− by bacterial isotope fractionation. Compared to results from neutral Lake Runstedt, these rates were extremely low. However, we cannot completely exclude a very low activity of ammonium oxidizing archaea in the sediments of Lake Partwitz, since they are less affected by ATU.36 In the slurries of Lake Runstedt a clear nitrification rate of 259 000 nmol L−1 d−1 was measured (Table 3). ATU inhibited the nitrification activity in neutral sediments completely. Although no significant formation of 15NOx− from 15NH4+ was observed in the acidic sediments, there was a net increase of ammonium in all incubations. The reason for the increase of ammonium could be the mineralization of organic substances. Similar to the situation in neutral lakes, the sediments of the acidic pit lakes are a source of ammonium. Further proof for the lack of nitrification in acidic lakes comes from comparing the isotopic composition of dissolved nitrate (Figure 1). According to the literature the δ18O values in nitrate derived from nitrification are known to be between 0 to

Figure 2. Ammonium concentration in lakes with varying pH (• pit lakes from coal and lignite mining, ∇ pit lake from metal mining, ○ waters influenced by volcanic activity). Data sources: pit lakes from metal mining: own measurements; volcanically influenced waters,46−53 pit lakes from coal and lignite mining,54−58 and references in Schultze et al.59

Figure 1. δ15N and δ18O values of dissolved nitrate. Filled symbols show natural values while open symbols show values after incubation with 15NH4+. Circled values were affected by precipitation; the range indicative of nitrification is highlighted in gray. 14021



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(2) Rudd, J. W. M.; Kelly, C. A.; Schindler, D. W.; Turner, M. A. Disruption of the nitrogen-cycle in acidified lakes. Science 1988, 240 (4858), 1515−1517. (3) Friese, K.; Herzsprung, P.; Schultze, M., Water, sediment, and pore water. In Acidic Pit LakesThe Legacy of Coal and Metal Surface Mines; Geller, W., Schultze, M., Kleinmann, R., Wolkersdorfer, C., Eds.; Springer: Berlin, 2013. (4) Noges, T. Relationships between morphometry, geographic location and water quality parameters of European lakes. Hydrobiologia 2009, 633 (1), 33−43. (5) Ender, R.; Schmaland, G.; Nixdorf, B.; Lessmann, D., Erste Ergebnisse zur Bedeutung der Nitrifiklation in bergbaubeeinflussten Gewässern. In Entwicklungen der Gewässer im Scharmützelseegebiet und angewandte Probleme des Gewässerschutzes; Krumbeck, H.; Mischke, A., Eds.; BTU Cottbus, 2001; Vol. 6, pp 110-119. (6) Nitrification; Prosser, J. I., Ed.; IRL Press: Oxford, 1986. (7) Ward, B. B.; Arp, D. J.; Klotz, M. G. Nitrification; ASM Press: Washington DC, 2011. (8) Suzuki, I.; Dular, U.; Kwok, S. C. Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas-europaea cells and extracts. J. Bacteriol. 1974, 120 (1), 556−558. (9) de Boer, W.; Duyts, H.; Laanbroek, H. J. Autotrophic nitrification in a fertilized acid heath soil. Soil Biol. Biochem. 1988, 20 (6), 845− 850. (10) Ying, J. Y.; Zhang, L. M.; He, J. Z. Putative ammonia-oxidizing bacteria and archaea in an acidic red soil with different land utilization patterns. Environ. Microbiol. Rep. 2010, 2 (2), 304−312. (11) Tarre, S.; Green, M. High-rate nitrification at low pH in suspended- and attached-biomass reactors. Appl. Environ. Microbiol. 2004, 70 (11), 6481−6487. (12) Hayatsu, M. The lowest limit of pH for nitrification in tea soil and isolation of an acidophilic ammonia oxidizing bacterium. Soil Sci. Plant Nutr. 1993, 39 (2), 219−226. (13) Lehtovirta-Morley, L. E.; Stoecker, K.; Vilcinskas, A.; Prosser, J. I.; Nicol, G. W. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (38), 15892−15897. (14) Zhang, L. M.; Hu, H. W.; Shen, J. P.; He, J. Z. Ammoniaoxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J. 2012, 6 (5), 1032−1045. (15) Nicol, G. W.; Leininger, S.; Schleper, C.; Prosser, J. I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 2008, 10 (11), 2966−2978. (16) Allison, S. M.; Prosser, J. I. Ammonia oxidation at low pH by attached populations of nitrifying bacteria. Soil Biol. Biochem. 1993, 25 (7), 935−941. (17) de Boer, W.; Gunnewiek, P. J. A. K.; Veenhuis, M.; Bock, E.; Laanbroek, H. J. Nitrification at low pH by aggregated chemolithotrophic bacteria. Appl. Environ. Microbiol. 1991, 57 (12), 3600− 3604. (18) Gieseke, A.; Tarre, S.; Green, M.; de Beer, D. Nitrification in a biofilm at low pH values: Role of in situ microenvironments and acid tolerance. Appl. Environ. Microbiol. 2006, 72 (6), 4283−4292. (19) de Boer, W.; Laanbroek, H. J. Ureolytic Nitrification at Low pH by Nitrosospira Spec. Arch. Microbiol. 1989, 152 (2), 178−181. (20) Ward, B. B. Measurement and distribution of nitrification rates in the oceans. Methods Enzymol. 2011, 486, 307−323. (21) Sánchez-España, J. S.; López-Pamo, E.; Diez, M.; Santofimia, E. Physico-chemical gradients and meromictic stratification in Cueva de la Mora and other acidic pit lakes of the Iberian Pyrite Belt. Mine Water Environ. 2009, 28 (1), 15−29. (22) Sánchez-España, J. S.; López-Pamo, E.; Pastor, E. S.; Ercilla, M. D. The acidic mine pit lakes of the Iberian Pyrite Belt: An approach to their physical limnology and hydrogeochemistry. Appl. Geochem. 2008, 23 (5), 1260−1287.

between pH and ammonia for data from lakes acidified by atmospheric deposition. For that purpose, we used the data of the Eastern Lake Survey.41 This data set was initially described by Brake et al.42 and Ellers et al.43,44 and has been used for scientific purposes already in the past.45 However, as they did not show any significant relation between pH and ammonium concentration and the pH was generally higher than 3.5 this data is not included in Figure 2. The compilation of data from 297 lakes and other surface waters indicates that elevated ammonium concentrations above 10 mg NH4+-N L−1 occur in well oxygenated surface waters below pH 3 (Figure 2). This could be caused either by the absence of rapid ammonium consumption or a strong continuous source of ammonium. The second explanation seems improbable as high ammonium values did not occur in any neutral lakes. In rain acidified lakes, pH 5.4 was identified as the lower limit for nitrification,2 considerably higher than the limit proposed in our study. However, the authors2 of that study noted that there was evidence for nitrification in waters as acidic as pH 4.0. The lowest pH reported for Lake Orta60,61 was 3.8. Lake Orta was acidified by nitrification of ammonium originating from wastewater. Experiments simulating acidification of natural waters by nitrification revealed a pH of 3.7,62 yet did not clearly show what pH was the lower limit for nitrification. None of the studies included in Figure 2 reported direct measurements of nitrification rates. In the cited studies nitrification activity was inferred from decreasing ammonium concentrations, increasing nitrate concentrations, and changes in pH, while inhibition of nitrification was deduced from ammonium accumulation. We conclude that pH 3 is probably the lower pH boundary for the occurrence of nitrification in lakes. It remains to be proven if this boundary also applies to other habitats, for example, soils. The fact that there is no published evidence for nitrification at pH < 3 supports our conclusion that pH 3 probably represents the lower limit of nitrification in nature.

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AUTHOR INFORMATION

Corresponding Author

*(C.J.) Phone +49 345 558 5490; fax +49 341 558 5449; email: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Anja Müller, Corinna Völkner, Martin Wieprecht, and the whole team of the UFZ-Lake Research Magdeburg for technical support and helpful discussions. Also thanks goes to Martina Neuber and Sandra Zücker-Gerstner of the UFZ-Stable Isotope Laboratory Halle. Special thanks are addressed to Dr. Felix Bilek from the Groundwater Center GFI GmbH Dresden and Lausitz and Central German Mining Administration Company (LMBV) for their financial and technical support for this investigation. CF was financially supported by the European Science Foundation with the program “The Functionality of Iron Minerals in Environmental Processes” (FIMIN).

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No Nitrification in Lakes Below pH 3 - Environmental Science

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