It seems that the verdict on ammonia toxicity and AOA is still not confirmed. The below study is about soils but I think it is still relevant.
There's more on pH influence on AOA and Carbon uptake in the link
Drivers of archaeal ammonia-oxidizing communities in soil
https://www.frontiersin.org/articles/10.3389/fmicb.2012.00210/full
Ammonia or Ammonium as Substrate for Ammonia Monooxygenase
Is ammonia (NH3) or the cation ammonium (NH4+) the substrate for the archaeal AMO enzyme? Ammonia is known to be the substrate of this initial step in bacterial ammonia oxidation (
Suzuki et al., 1974;
Arp et al., 2002). However, despite several studies dedicated to studying the biochemistry of AMO in bacteria, it still remains unknown whether ammonia or ammonium is the substrate for archaeal AMO (
Martens-Habbena and Stahl, 2011). Bacterial oxidation of ammonia to nitrite (NO2-) is a two-step process. AMO oxidizes ammonia to hydroxylamine (NH2OH), and hydroxylamine oxidoreductase (HAO) catalyzes oxidation of hydroxylamine to nitrite (
Arp et al., 2002). Structural differences in the archaeal AMO and bacterial AMO and the absence of genes encoding HAO and cytochrome
c proteins for recycling electrons suggest important differences between bacterial and archaeal ammonia oxidation. For example, nitroxyl (HNO) rather than hydroxylamine may be the intermediate in the AMO enzymatic reaction, or a different cytochrome system may be responsible for electron channeling in AOA (
Walker et al., 2010).
The majority of AOA discovered to date were found in oligotrophic conditions (
Hatzenpichler et al., 2008;
Walker et al., 2010). The affinity of marine archaeon
Nitrosopumilus maritimus for ammonium/ammonia was 200-fold higher than substrate affinity of AOB (
Martens-Habbena et al., 2009;
Martens-Habbena and Stahl, 2011). These microorganisms can obtain energy even under very low concentrations of substrate. It has been suggested that the differences in substrate affinities allow AOA and AOB to inhabit distinct niches separated by substrate concentration and thereby reduce competition (
Martens-Habbena et al., 2009;
Schleper, 2010;
Martens-Habbena and Stahl, 2011;
Verhamme et al., 2011). There are studies that suggest substrate inhibition of archaeal nitrification if high concentrations of ammonia are present (
Di et al., 2010;
Tourna et al., 2010).
Because AMO in AOA has a much higher affinity for substrate than the analogous process in AOB, it has been suggested that AOA dominate over AOB where ammonia concentrations are particularly low. This seems to be the case in oligotrophic environments such as sea water or hot springs (
Hatzenpichler et al., 2008;
Walker et al., 2010). For example,
Ca. Nitrososphaera gargensis, which was first found in hot springs, fixes bicarbonate at lower levels when the ammonia concentration was higher than 3.1 mM. The optimal ammonia concentration for bicarbonate fixation was much lower, between 0.14 and 0.8 mM (
Hatzenpichler et al., 2008). Some studies suggest that substrate concentration does not influence thaumarchaeal ammonia oxidation (
Stopnisek et al., 2010;
Verhamme et al., 2011). These authors showed that AOA grew similarly at low, medium, and high ammonia concentrations, whereas AOB grew best only with high ammonia concentrations. Other factors were suggested to be important in the growth of AOA.
Di et al. (2009)observed in nitrogen-rich grassland soils neither AOA abundance nor their activity increased with the application of a large dose of ammonia substrate. In this study, AOA abundance was not quantitatively related to nitrification rates. Similarly,
Ke and Lu (2012) did not see any changes in AOA in paddy field soils after urea was applied as nitrogen fertilizer.
In some studies, high ammonia appears to promote AOA growth and activity.
Treusch et al. (2005)found considerably higher amounts of archaeal
amoA transcripts in those samples that had been amended with additional ammonia (10 mM). It was demonstrated that the soil archaea
Nitrososphaera viennensis strain EN76 grows well in media containing ammonium concentrations as high as 15 mM, but its growth is inhibited at 20 mM (
Tourna et al., 2011). This is considerably higher than the inhibitory concentration of 2–3 mM reported for the aquatic AOA
Nitrosopumilus maritimus (
Walker et al., 2010) and
Ca. Nitrososphaera gargensis (
Hatzenpichler et al., 2008). Tolerance for ammonia toxicity of
Ca. Nitrosoarchaeum koreensis strain MY1, isolated from an acidic agricultural soil, was slightly lower, 5 mM, than that of
Nitrososphaera viennensis (
Jung et al., 2011).
Park et al. (2006) found archaeal
amoA in wastewater with 2 mM ammonia.
The source of substrate and its location can influence ammonia concentration in soil (
Offre et al., 2009;
Stopnisek et al., 2010;
Verhamme et al., 2011). Ammonium production via mineralization, additions of ammonical fertilizers, animal wastes, and the atmospheric deposition of ammonium increases substrate supply, while competing consumptive processes include microbial assimilation (immobilization), plant assimilation, and ammonia volatilization reduce ammonia concentration (
Norton and Stark, 2011). In addition, AOA do not respond to the addition of mineral nitrogen to soil (
Di et al., 2009;
Jia and Conrad, 2009;
Stopnisek et al., 2010;
Verhamme et al., 2011;
Ke and Lu, 2012). In contrast, AOB increase in abundance after addition of ammonium sulfate or urine (
Di et al., 2009,
2010;
Jia and Conrad, 2009;
Hofferle et al., 2010). Archaeal
amoA gene copies and nitrate concentration increased during incubation soil for 30 days (
Offre et al., 2009). All ammonia in this soil was generated by nitrogen mineralization since no ammonia was added. Also, it was shown in upland field soils archaeal 16S rRNA gene was significantly affected by the class of fertilizer (chemical or organic fertilizer). In four different soil types 16S rRNA abundance of AOA was about 0.1–0.9 × 108 gene copy number higher in the plots where organic fertilizers were added than in the plots with chemical fertilizer addition.
Nitrate concentrations likely differ greatly both spatially and temporally under these two scenarios (
Stopnisek et al., 2010). While ammonia from organic matter mineralization is slowly and constantly liberated resulting in low, but steady, levels of ammonia, an application of mineral nitrogen fertilizer promotes a burst of ammonia. Archaeal ammonia oxidizers should be expected to be in a higher abundance in the soils with high organic matter, which would provide a constant source of substrate (
Stopnisek et al., 2010).
Adaptation to different concentrations of ammonia and the ability to survive even at extremely low concentrations of ammonia, together with other ecological factors, contribute to the ecological fitness and niche adaptation of AOA and AOB. The presence of different ecophysiological adaptations such as different concentrations of substrate suggests that a wide range of ecotypes can be expected to occur among soil AOA.
Ammonia or Ammonium as Substrate for Ammonia Monooxygenase
Is ammonia (NH3) or the cation ammonium (NH4+) the substrate for the archaeal AMO enzyme? Ammonia is known to be the substrate of this initial step in bacterial ammonia oxidation (
Suzuki et al., 1974;
Arp et al., 2002). However, despite several studies dedicated to studying the biochemistry of AMO in bacteria, it still remains unknown whether ammonia or ammonium is the substrate for archaeal AMO (
Martens-Habbena and Stahl, 2011). Bacterial oxidation of ammonia to nitrite (NO2-) is a two-step process. AMO oxidizes ammonia to hydroxylamine (NH2OH), and hydroxylamine oxidoreductase (HAO) catalyzes oxidation of hydroxylamine to nitrite (
Arp et al., 2002). Structural differences in the archaeal AMO and bacterial AMO and the absence of genes encoding HAO and cytochrome
c proteins for recycling electrons suggest important differences between bacterial and archaeal ammonia oxidation. For example, nitroxyl (HNO) rather than hydroxylamine may be the intermediate in the AMO enzymatic reaction, or a different cytochrome system may be responsible for electron channeling in AOA (
Walker et al., 2010).
The majority of AOA discovered to date were found in oligotrophic conditions (
Hatzenpichler et al., 2008;
Walker et al., 2010). The affinity of marine archaeon
Nitrosopumilus maritimus for ammonium/ammonia was 200-fold higher than substrate affinity of AOB (
Martens-Habbena et al., 2009;
Martens-Habbena and Stahl, 2011). These microorganisms can obtain energy even under very low concentrations of substrate. It has been suggested that the differences in substrate affinities allow AOA and AOB to inhabit distinct niches separated by substrate concentration and thereby reduce competition (
Martens-Habbena et al., 2009;
Schleper, 2010;
Martens-Habbena and Stahl, 2011;
Verhamme et al., 2011). There are studies that suggest substrate inhibition of archaeal nitrification if high concentrations of ammonia are present (
Di et al., 2010;
Tourna et al., 2010).
Because AMO in AOA has a much higher affinity for substrate than the analogous process in AOB, it has been suggested that AOA dominate over AOB where ammonia concentrations are particularly low. This seems to be the case in oligotrophic environments such as sea water or hot springs (
Hatzenpichler et al., 2008;
Walker et al., 2010). For example,
Ca. Nitrososphaera gargensis, which was first found in hot springs, fixes bicarbonate at lower levels when the ammonia concentration was higher than 3.1 mM. The optimal ammonia concentration for bicarbonate fixation was much lower, between 0.14 and 0.8 mM (
Hatzenpichler et al., 2008). Some studies suggest that substrate concentration does not influence thaumarchaeal ammonia oxidation (
Stopnisek et al., 2010;
Verhamme et al., 2011). These authors showed that AOA grew similarly at low, medium, and high ammonia concentrations, whereas AOB grew best only with high ammonia concentrations. Other factors were suggested to be important in the growth of AOA.
Di et al. (2009)observed in nitrogen-rich grassland soils neither AOA abundance nor their activity increased with the application of a large dose of ammonia substrate. In this study, AOA abundance was not quantitatively related to nitrification rates. Similarly,
Ke and Lu (2012) did not see any changes in AOA in paddy field soils after urea was applied as nitrogen fertilizer.
In some studies, high ammonia appears to promote AOA growth and activity.
Treusch et al. (2005)found considerably higher amounts of archaeal
amoA transcripts in those samples that had been amended with additional ammonia (10 mM). It was demonstrated that the soil archaea
Nitrososphaera viennensis strain EN76 grows well in media containing ammonium concentrations as high as 15 mM, but its growth is inhibited at 20 mM (
Tourna et al., 2011). This is considerably higher than the inhibitory concentration of 2–3 mM reported for the aquatic AOA
Nitrosopumilus maritimus (
Walker et al., 2010) and
Ca. Nitrososphaera gargensis (
Hatzenpichler et al., 2008). Tolerance for ammonia toxicity of
Ca. Nitrosoarchaeum koreensis strain MY1, isolated from an acidic agricultural soil, was slightly lower, 5 mM, than that of
Nitrososphaera viennensis (
Jung et al., 2011).
Park et al. (2006) found archaeal
amoA in wastewater with 2 mM ammonia.
The source of substrate and its location can influence ammonia concentration in soil (
Offre et al., 2009;
Stopnisek et al., 2010;
Verhamme et al., 2011). Ammonium production via mineralization, additions of ammonical fertilizers, animal wastes, and the atmospheric deposition of ammonium increases substrate supply, while competing consumptive processes include microbial assimilation (immobilization), plant assimilation, and ammonia volatilization reduce ammonia concentration (
Norton and Stark, 2011). In addition, AOA do not respond to the addition of mineral nitrogen to soil (
Di et al., 2009;
Jia and Conrad, 2009;
Stopnisek et al., 2010;
Verhamme et al., 2011;
Ke and Lu, 2012). In contrast, AOB increase in abundance after addition of ammonium sulfate or urine (
Di et al., 2009,
2010;
Jia and Conrad, 2009;
Hofferle et al., 2010). Archaeal
amoA gene copies and nitrate concentration increased during incubation soil for 30 days (
Offre et al., 2009). All ammonia in this soil was generated by nitrogen mineralization since no ammonia was added. Also, it was shown in upland field soils archaeal 16S rRNA gene was significantly affected by the class of fertilizer (chemical or organic fertilizer). In four different soil types 16S rRNA abundance of AOA was about 0.1–0.9 × 108 gene copy number higher in the plots where organic fertilizers were added than in the plots with chemical fertilizer addition.
Nitrate concentrations likely differ greatly both spatially and temporally under these two scenarios (
Stopnisek et al., 2010). While ammonia from organic matter mineralization is slowly and constantly liberated resulting in low, but steady, levels of ammonia, an application of mineral nitrogen fertilizer promotes a burst of ammonia. Archaeal ammonia oxidizers should be expected to be in a higher abundance in the soils with high organic matter, which would provide a constant source of substrate (
Stopnisek et al., 2010).
Adaptation to different concentrations of ammonia and the ability to survive even at extremely low concentrations of ammonia, together with other ecological factors, contribute to the ecological fitness and niche adaptation of AOA and AOB. The presence of different ecophysiological adaptations such as different concentrations of substrate suggests that a wide range of ecotypes can be expected to occur among soil AOA.
