Abstract
Ammonia oxidation is the first and rate-limiting step in nitrification and is dominated by two distinct groups of microorganisms in soil: ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB). AOA are often more abundant than AOB and dominate activity in acid soils. The mechanism of ammonia oxidation under acidic conditions has been a long-standing paradox. While high rates of ammonia oxidation are frequently measured in acid soils, cultivated ammonia oxidizers grew only at near-neutral pH when grown in standard laboratory culture. Although a number of mechanisms have been demonstrated to enable neutrophilic AOB growth at low pH in the laboratory, these have not been demonstrated in soil, and the recent cultivation of the obligately acidophilic ammonia oxidizer “Candidatus Nitrosotalea devanaterra” provides a more parsimonious explanation for the observed high rates of activity. Analysis of the sequenced genome, transcriptional activity, and lipid content of “Ca. Nitrosotalea devanaterra” reveals that previously proposed mechanisms used by AOB for growth at low pH are not essential for archaeal ammonia oxidation in acidic environments. Instead, the genome indicates that “Ca. Nitrosotalea devanaterra” contains genes encoding both a predicted high-affinity substrate acquisition system and potential pH homeostasis mechanisms absent in neutrophilic AOA. Analysis of mRNA revealed that candidate genes encoding the proposed homeostasis mechanisms were all expressed during acidophilic growth, and lipid profiling by high-performance liquid chromatography–mass spectrometry (HPLC-MS) demonstrated that the membrane lipids of “Ca. Nitrosotalea devanaterra” were not dominated by crenarchaeol, as found in neutrophilic AOA. This study for the first time describes a genome of an obligately acidophilic ammonia oxidizer and identifies potential mechanisms enabling this unique phenotype for future biochemical characterization.
Highlights
Ammonia oxidation is integral to the global nitrogen cycle and is performed by ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA)
Kinetic studies of ammonia oxidation in cell suspensions and extracts of Nitrosomonas europaea suggest that ammonia (NH3), rather than ammonium (NH4ϩ), is the substrate for ammonia monooxygenase (AMO), which catalyzes the first step in ammonia oxidation [8]
If AOA are able to use ammonium for transport as our results suggest, AOA rather than AOB were in a better predisposition to evolve an acidophilic phenotype
Summary
Ammonia oxidation is integral to the global nitrogen cycle and is performed by ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA). Growth of all cultivated prokaryotic ammonia oxidizers in batch culture was considered possible only at a pH of Ͼ6.5 This view was challenged by the initial cultivation [6] and subsequent isolation [7] of the obligately acidophilic AOA “Candidatus Nitrosotalea devanaterra,” which grows in the pH range 4.0 to 5.5. Can this organism utilize NH4ϩ, is the active site of AMO facing the cytoplasm or the periplasm and are there other N metabolism genes that can explain the distinct physiology of “Ca. Nitrosotalea devanaterra”? The aim of this study was to examine the “Ca. Nitrosotalea devanaterra” genome for evidence of specific adaptations in N and C metabolism and to determine whether the genome contained genes involved in pH homeostasis mechanisms found in other model acidophiles There are several major unresolved questions regarding acidophilic ammonia oxidation, as follows. (i) How does “Ca. Nitrosotalea devanaterra” overcome low NH3 concentrations? can this organism utilize NH4ϩ, is the active site of AMO facing the cytoplasm or the periplasm and are there other N metabolism genes that can explain the distinct physiology of “Ca. Nitrosotalea devanaterra”? (ii) How does “Ca. Nitrosotalea devanaterra” fix carbon under acidic conditions where the HCO3Ϫ concentration is low? (iii) Is cytoplasmic pH homeostasis of “Ca. Nitrosotalea devanaterra” achieved by mechanisms similar to those in other acidophiles? The aim of this study was to examine the “Ca. Nitrosotalea devanaterra” genome for evidence of specific adaptations in N and C metabolism and to determine whether the genome contained genes involved in pH homeostasis mechanisms found in other model acidophiles
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