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Nitrifying Bacteria Mediate Aerobic Ammonia Oxidation and Urea Hydrolysis Within the Grand River

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Nitrifying Bacteria Mediate Aerobic Ammonia Oxidation and Urea Hydrolysis Within the Grand River Vol. 73: 151–162, 2014 AQUATIC MICROBIAL ECOLOGY Published online October 2 doi: 10.3354/ame01712 Aquat Microb Ecol FREE ACCESS Nitrifying bacteria mediate aerobic ammonia oxidation and urea hydrolysis within the Grand River Puntipar Sonthiphand, Josh D. Neufeld* Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, Ontario N2L 3G1, Canada ABSTRACT: Ammonia oxidation is an important process for decreasing ammonia concentrations in wastewater-impacted rivers. Ammonia-oxidizing bacteria (AOB) and archaea (AOA) are re - sponsible for ammonia oxidation, which is the first step of the nitrification process. Nitrification and urea hydrolysis were monitored in sediment and water column samples in the Grand River (Ontario), and nitrification inhibitors (allylthiourea and 2-phenyl-4,4,5,5-tetramethylimidazoline- 1-oxyl 3-oxide) helped identify the relative contributions of AOA and AOB to ammonia oxidation. Despite the presence of AOA, our results implicated AOB as the dominant contributors to ammo- nia oxidation, both directly and in association with urea hydrolysis. KEY WORDS: Nitrification activity · Ammonia oxidizing bacteria · Ammonia oxidizing archaea · PTIO · ATU Resale or republication not permitted without written consent of the publisher INTRODUCTION demonstrated that AOB are more abundant and active than AOA in inorganic fertilized soils (Jia & Nitrification is composed of 2 oxidative processes. Conrad 2009, Xia et al. 2011). Systems treated with The first step is ammonia oxidation to nitrite under organic fertilizer (i.e. urea and animal urine sub- oxic conditions, which is mediated by ammonia- strate) are also dominated by AOB (Di et al. 2009, oxidizing bacteria (AOB) and archaea (AOA). This O’Callaghan et al. 2010, Di & Cameron 2011). How- process is followed by nitrite oxidation to nitrate, ever, AOA utilize ammonia from the mineralization which is mediated by aerobic nitrite-oxidizing bacte- of organic substances and outnumber AOB in soil ria (NOB). High ammonia loads in impacted rivers microcosms (Gubry-Rangin et al. 2010, Zhang et al. ad versely affect drinking water quality, aquatic life, 2010). and ecosystem health. Ammonia oxidation is an im - Ammonia monooxygenase (AMO) is a key enzyme portant process, removing ammonia from im pacted for ammonia oxidation by both AOA and AOB. How- freshwater environments (Sonthiphand et al. 2013). ever, urease is an optional enzyme, discovered in For many decades, AOB were believed to be the sole some AOB and AOA species, that is used to hydrol- microorganisms responsible for ammonia oxidation, yse urea as an alternative N energy source. Distinct until the discovery and isolation of AOA (Könneke et ammonia sources might govern the ratio of environ- al. 2005). Although both AOB and AOA have the mental AOB and AOA due to differences in urease ability to oxidize ammonia, each has unique physio- activity. Urease genes have been reported for Nitro- logical properties (i.e. enzyme structure, intermedi- somonas ureae, N. nitrosa, N. oligotropha, N. marina, ates, and substrate affinity; Zhalnina et al. 2012), evi- and N. aestuarii (Pommerening-Röser & Koops 2005). denced by differential sensitivities to nitrification Although only 2 AOA pure cultures are available, inhibitors. Distinct ammoniacal N sources might also genome analysis has revealed the presence of a ure- differentially affect the relative environmental con- ase gene within ‘Candidatus Cenarchaeum symbio- tributions of AOB and AOA. Previous studies have sum’ (Hallam et al. 2006), Nitrososphaera viennensis *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 152 Aquat Microb Ecol 73: 151–162, 2014 (Tourna et al. 2011), ‘Candidatus Nitro sos pha era gar- the hypothesis that AOB dominate ammonia oxida- gensis’ (Spang et al. 2012), and ‘Candidatus Nitro so - tion within the Grand River, which would be consis- pu milus salaria’ (Mosier et al. 2012). Consequently, tent with our initial observation that AOB became particular AOB and AOA species may generate enriched following prolonged high-ammonia incuba- am monia for aerobic respiration from urea hydrolysis tions. This is the first study to combine nitrification in situ. activities and urea hydrolysis measurements with Many studies have investigated nitrification activ- inhibitors to differentiate between AOB and AOA ity in freshwater environments (e.g. Strauss & Lam- activities within a freshwater environment. berti 2000, Kemp & Dodds 2002) and the relative ammonia oxidation activities of AOB and AOA using differential inhibitors in terrestrial environments MATERIALS AND METHODS (e.g. Di et al. 2009, Taylor et al. 2010). However, no study has reported on nitrification activities with dif- Sample collection ferential inhibitors to determine the relative contri- butions of AOB and AOA in freshwater environ- The Grand River watershed is the largest catchment ments. Allylthiourea (ATU) inhibits the first step of in Southern Ontario and much impacted by human nitrification by chelating copper from the AMO activities. In this study, a central portion of the Grand active site (Bédard & Knowles 1989). AOB and AOA River was used as an example of a watershed im- respond differently to ATU due to differences in inhi- pacted by wastewater effluent. Downstream and up- bition thresholds and amino acids in the active site of stream sampling sites of wastewater effluent repre- AMO (Lehtovirta-Morley et al. 2013, Shen et al. sented sites of high and low impact by wastewater 2013). AOB appear to be more sensitive to ATU than effluent, respectively. Sediment and water samples AOA in soil (Taylor et al. 2010) and marine (Santoro were collected approximately 180 m downstream & Casciotti 2011) environments. In a study of an from an ammonia-rich wastewater discharge pipeline AOA-enriched agricultural soil, ‘Candidatus Nitro- from a municipal wastewater treatment plant in Wa- soarchaeum koreensis’ was not inhibited by ATU, terloo, Ontario, Canada on 11 June 2013. Due to high whereas ATU at low concentrations inhibited Nitro- sample heterogeneity, sediment samples were col- somonas europaea (Jung et al. 2011). At the same lected at 5 random locations using a plastic core tube concentration, Nitrosospira multiformis was more and pooled on site. Water samples were well mixed at sensitive to ATU than N. viennensis (Shen et al. the sampling site and were collected using a 500 ml 2013). PTIO (2-phenyl-4,4,5,5-tetramethylimidazo- plastic container. All samples were kept on ice during line-1-oxyl 3-oxide) inhibits ammonia oxidation by transport to the lab. Conductivity, pH, and dissolved acting as a nitric oxide (NO) scavenger. NO is a likely oxygen were measured on site (Table 1). Follow-up intermediate of AOA ammonia oxidation, but not samples were taken on 31 July 2013. Upstream sam- AOB ammonia oxidation (Walker et al. 2010). PTIO ples, as well as downstream samples, were included can effectively inhibit N. viennensis without affect- in the follow-up study for comparison. Upstream sedi- ing N. multiformis (Shen et al. 2013). This study rep- ment and water samples were collected approxi- resents the first application of PTIO to environmental mately 390 m upstream from the pipeline effluent us- sample incubations. ing the methods described above. The objectives of this study were to assess in vitro ammonia oxidation and Table 1. Downstream and upstream water chemistry data. NA = not available; urea hydro lysis to reveal ammonia- BDL = below detection limit; pH (late-July) was analyzed in the lab oxidizer dynamics within the largest watershed in Southern Ontario, the Mid-June Late-July Grand River. This activity-based study Downstream Upstream Downstream follows on from our initial molecular water water water assessment of AOA, AOB and anaero- Conductivity (µS) 1031 480 1019 bic ammonia-oxidizing (anammox) pH 7.5 8.0 7.9 bacteria in Grand River sediment and Dissolved oxygen (mg l−1) 8.23 NA NA + water columns, and a strong enrich- N-[NH3 + NH4 ] (µM) 560.46 BDL 571.98 − − N-[NO2 + NO3 ] (µM) 147.20 151.29 166.55 ment of AOB within wastewater treat- − N-[NO2 ] (µM) BDL BDL 20.62 ment plant (WWTP) effluent plumes N-urea (µM) BDL 239.89 BDL (Sonthiphand et al. 2013). We tested Sonthiphand & Neufeld: Ammonia oxidation mediated by nitrifying bacteria 153 In vitro nitrification activity nitrate measurements were conducted by a colori- metric assay (Miranda et al. 2001). Briefly, nitrate − − For each sediment treatment replicate, 1 g of was reduced to nitrite N-[NO2 + NO3 ] by VCl3. − pooled downstream sediment was added to 10 ml of Consequently, the concentrations of N-NO2 and − − modified inorganic freshwater media (FWM; Tourna N-[NO2 + NO3 ] can be measured using the same et al. 2011). The modified FWM, without HEPES method. Urea was measured by a previously pub- buffer, was adjusted to pH 7.5. Samples were inocu- lished protocol (Zawada et al. 2009), with analysis + lated with an initial total ammonia (NH3 + NH4 ) con- at 450 nm instead of 430 nm. All ammonia, urea, centration of 600 µM. There were 3 treatments: with- and N-oxide analyses were performed on a Filter- out an inhibitor, with ATU (10 or 100 µM), and with Max F5 Multi-Mode Microplate Reader (Molecular PTIO (100 µM). In addition to sediment slurries, 10 ml Devices). of downstream water samples were added to test tubes, without FWM. Ammonia, ATU, and PTIO were added to each tube at the same concentrations as DNA extraction and quantitative real-time PCR those for the sediment set. Negative
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