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Martens-Habbena Et Al., 2009. “Ammonia Oxidation Kinetics Vol 461 | 15 October 2009 | doi:10.1038/nature08465 LETTERS Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria Willm Martens-Habbena1, Paul M. Berube1{, Hidetoshi Urakawa1, Jose´ R. de la Torre1{ & David A. Stahl1 The discovery of ammonia oxidation by mesophilic and thermo- oxidation stoichiometry and kinetics in the only isolated AOA strain, philic Crenarchaeota and the widespread distribution of these ‘Candidatus Nitrosopumilus maritimus’ strain SCM1. The results organisms in marine and terrestrial environments indicated an demonstrate that ammonia oxidation by AOA could indeed sustain important role for them in the global nitrogen cycle1–7. However, significant growth rates and standing stocks of these Crenarchaeota, very little is known about their physiology or their contribution to even in nutrient-depleted natural marine and terrestrial environments. nitrification8. Here we report oligotrophic ammonia oxidation In ammonium-limited batch cultures, SCM1 grew exponentially kinetics and cellular characteristics of the mesophilic crenarchaeon with high rates and depleted ammonium below the detection limit of ‘Candidatus Nitrosopumilus maritimus’ strain SCM1. Unlike 10 nM (n 5 4; Fig. 1). This ammonium concentration approaches characterized ammonia-oxidizing bacteria, SCM1 is adapted to life values measured in oligotrophic open ocean water11,16 and is more than under extreme nutrient limitation, sustaining high specific oxida- 100-fold lower than the minimum concentration required for growth tion rates at ammonium concentrations found in open oceans. Its (.1 mM near neutral pH) of cultivated AOB13,15. SCM1 attained maxi- 21 half-saturation constant (Km 5 133 nM total ammonium) and sub- mum growth rates (0.027 h ; doubling time 5 26 h) and activities strate threshold (#10 nM) closely resemble kinetics of in situ (51.9 mmol ammonium per mg protein per h) comparable to AOB nitrification in marine systems9,10 and directly link ammonia- strains (range 30–80 mmol ammonium per mg protein per h)13 (Fig. 1, oxidizing Archaea to oligotrophic nitrification. The remarkably Supplementary Note 1). Thus, SCM1 seems particularly well adapted to high specific affinity for reduced nitrogen (68,700 l per g cells per growth at ammonium levels prevailing in nutrient-limited open oceans. h) of SCM1 suggests that Nitrosopumilus-like ammonia-oxidizing We observed that growth of SCM1 was significantly impaired by Archaea could successfully compete with heterotrophic bacterio- agitation, compared to static batch cultures, which precluded con- plankton and phytoplankton. Together these findings support the tinuous culture experiments (Supplementary Note 1). To gain hypothesis that nitrification is more prevalent in the marine nitro- insight into the ammonia oxidation kinetics of SCM1, we therefore gen cycle than accounted for in current biogeochemical models11. independently determined ammonium and oxygen uptake with Aerobic ammonia oxidation is the first, rate-limiting step of nitri- ammonium-depleted (,10 nM) cells from batch cultures (Fig. 2). fication, a two-step process catalysed by ammonia-oxidizing and Ammonium-depleted, early-stationary phase cells consumed very 21 nitrite-oxidizing microorganisms. It is the only oxidative biological low amounts of oxygen (0.51 mMO2 h 5 0.67 mmol O2 per mg process linking reduced and oxidized pools of inorganic nitrogen in protein per h, s.d. 0.29, n 5 10). Oxygen uptake increased more than 12,13 21 nature . This key process in the global nitrogen cycle was thought to 50-fold to maximum rates of 27.51 mMO2 h (36.29 mmol O2 per be restricted to ammonia-oxidizing bacteria (AOB), two narrow clades mg protein per h, s.d. 3.35, n 5 10; < 24.2 mmol ammonium per mg of Beta- and Gammaproteobacteria8,13. These slow-growing, auto- trophic bacteria use ammonia oxidation as their sole source of energy. 1,000 50 The growth rates of AOB are thus directly linked to the availability of 13,14 ammonium and the kinetics of its oxidation . In situ rate measure- – NO2 ments in natural marine and terrestrial environments, however, indi- 800 40 + Cell number (10 cate that nitrification occurs almost ubiquitously, even in the most NH4 oligotrophic environments with ammonium levels significantly below the growth threshold of AOB9–11,13–15, raising the question whether 600 30 these bacteria could represent the dominant ammonia-oxidizer assemblage in oligotrophic environments9,10,13,14. Cells 6 The demonstration of autotrophic ammonia oxidation by mesophi- 400 20 ml 3–6 –1 lic and thermophilic Crenarchaeota and the widespread distribution ) Ammonium, nitrite (µM) of putative archaeal ammonia monooxygenase (amo) genes in marine 200 10 and terrestrial environments1–4,6,8 changed the perspective on nitrifica- tion. The isolation of ammonia-oxidizing Archaea (AOA) strains affiliated with Crenarchaeota clades constituting up to 39% of micro- 0 0 bial plankton in meso- and bathypelagic oceans suggested that AOA 0 50 100 150 200 250 could potentially play an important part in nitrification8,16–18. Time (h) However, AOA would need to compete with AOB, organotro- Figure 1 | Growth of SCM1 in ammonium-limited artificial sea water batch phic bacterioplankton and perhaps even phytoplankton for ammo- culture. Cultures entered stationary phase after ammonium was depleted nium11,12,19. To test this hypothesis, we determined the ammonia below the detection limit of 10 nM. 1Department of Civil & Environmental Engineering, University of Washington, Seattle, Washington 98105, USA. {Present addresses: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA (P.M.B.); Department of Biology, San Francisco State University, San Francisco, California 94132, USA (J.R.T). 976 ©2009 Macmillan Publishers Limited. All rights reserved NATURE | Vol 461 | 15 October 2009 LETTERS a 1.8 b 1.0 ) 1.6 30 (µmol per mg protein h) –1 0.8 1.4 Ammonia oxidation 25 1.2 (µM) + 0.6 4 1.0 20 0.8 15 + NH 3 0.4 0.6 NH Km = 0.134 µM 10 –1 0.4 0.2 Vmax = 0.857 µM N h Ammonium uptake (µM h 5 0.2 = 29.82 µmol N per mg protein per h 0.0 0.0 0 01234 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 Time (h) + NH3 + NH4 (µM) cdAddition of 156.4 30 10 µM NH Cl 175 4 156.2 25 25 (µmol per mg protein h) 156.0 ) –1 170 155.8 20 Ammonia oxidation 20 155.6 165 15 155.4 15 0.85 0.90 0.95 160 10 Oxygen (µM) 10 Km = 0.134 µM V = 25.72 µM N h–1 Oxygen uptake (µM h max 155 5 5 = 23.77 µmol N per mg protein per h 150 0 0 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 0246810 + Time (h) NH3 + NH4 (µM) Figure 2 | Ammonia oxidation kinetics of SCM1. a, Ammonium uptake of experiment was started by the addition of 10 mM ammonium chloride. early-stationary SCM1 cells on transfer to fresh medium containing 1.7 mM d, Michaelis–Menten plot of ammonium-dependent oxygen uptake. Uptake ammonium. b, Michaelis–Menten plot of ammonium uptake. rates were calculated from smoothed data (red line in c). For calculation of c, Ammonium-dependent oxygen uptake of early-stationary phase SCM1 kinetic parameters, a Michaelis–Menten equation was fitted to the data. See cells. Suspensions of cells were equilibrated for ,20 min before the Methods for experimental details and calculations. protein per h) within a few minutes of ammonium addition. in situ measurements strongly supports this hypothesis (Fig. 3a). Ammonium and oxygen were consumed with an AOB-like stoichi- The Km of SCM1 is by far the lowest half-saturation constant deter- ometry of 1:1.52 (s.d. 0.06, n 5 10). Notably, late-exponential and mined of any ammonia-oxidizing microorganism to date; it is very early-stationary phase SCM1 cells both exhibited maximum rates of similar to in situ nitrification measurements made in oligotrophic, ammonium and oxygen uptake at as low as 2 mM ammonium ammonium-depleted oceanic provinces9,10 and is even lower than in (Fig. 2b, d and Supplementary Fig. 1b). natural unfertilized soils21 (Fig. 3a). Assuming Michaelis–Menten- Ammonia oxidation by SCM1 followed Michaelis–Menten-type type saturation kinetics, an apparent Km of ammonia oxidation of kinetics (Fig. 2b, d and Supplementary Fig. 1b). The mean apparent ,0.15 mM ammonium was estimated in the upper oxic Cariaco 9 half-saturation constants (Km) for ammonium uptake (0.132 mM basin (Fig. 3a), and it was found that in the primary nitrite maxi- 1 NH31NH4 , range 0.005, n 5 2, equivalent to ,3nMNH3) and mum off the coast of California, ammonia oxidation was saturated at 1 10 oxygen uptake (0.133 mMNH31NH4 , s.d. 0.038, n 5 13) were 0.1 mM ammonium . Similarly, the Km values for nitrification in indistinguishable. Supplementation with as little as 0.2 mM ammo- uncultivated soil areas were significantly lower than the Km of known nium chloride triggered more than 50% of maximum oxygen uptake. AOB21. To account for these in situ nitrification measurements, In contrast, identical experiments with Nitrosomonas europaea and organisms with Nitrosopumilus-like kinetics must vastly outnumber Nitrosococcus oceani cells showed no stimulation of activity by 0.2 mM organisms typified by AOB. In contrast, a kinetic response consistent ammonium. Their Km values, determined by the same methods used with the activity of known AOB becomes prevalent only in coastal to characterize SCM1, were in a typical range previously reported environments and soils with higher nutrient levels21,22 (Fig. 3a). (Supplementary Note 2). Identical Km values and activities of SCM1 Nonetheless, even in nutrient-poor marine environments, organic- were observed in up to 5 cycles of substrate addition and depletion, matter-rich particles provide niches for nitrifiers with probably sig- up to 2 mM ammonium, and even with cells from late-exponential nificantly different kinetic properties23,24—for example, members of cultures which had not experienced ammonium concentrations the Nitrosomonas eutropha lineage24.
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