Nitrification, the oxidation of ammonia to nitrate, is an essential process in the biogeochemical nitrogen cycle. The first step of nitrification, ammonia oxidation, is performed by three, often co-occurring guilds of chemolithoautotrophs: ammonia-oxidizing bacteria (AOB), archaea (AOA), and complete ammonia oxidizers (comammox). Substrate kinetics are considered to be a major niche-differentiating factor between these guilds, but few AOA strains have been kinetically characterized. Here, the ammonia oxidation kinetic properties of 12 AOA representing all major cultivated phylogenetic lineages were determined using microrespirometry. Members of the genus Nitrosocosmicus have the lowest affinity for both ammonia and total ammonium of any characterized AOA, and these values are similar to previously determined ammonia and total ammonium affinities of AOB. This contrasts previous assumptions that all AOA possess much higher substrate affinities than their comammox or AOB counterparts. The substrate affinity of ammonia oxidizers correlated with their cell surface area to volume ratios. In addition, kinetic measurements across a range of pH values supports the hypothesis that—like for AOB—ammonia and not ammonium is the substrate for the ammonia monooxygenase enzyme of AOA and comammox. Together, these data will facilitate predictions and interpretation of ammonia oxidizer community structures and provide a robust basis for establishing testable hypotheses on competition between AOB, AOA, and comammox.

Thaumarchaeota are responsible for a significant fraction of ammonia oxidation in the oceans and in soils that range from alkaline to acidic. However, the adaptive mechanisms underpinning their habitat expansion remain poorly understood. Here we show that expansion into acidic soils and the high pressures of the hadopelagic zone of the oceans is tightly linked to the acquisition of a variant of the energy-yielding ATPases via horizontal transfer. Whereas the ATPase genealogy of neutrophilic Thaumarchaeota is congruent with their organismal genealogy inferred from concatenated conserved proteins, a common clade of V-type ATPases unites phylogenetically distinct clades of acidophilic/acid-tolerant and piezophilic/piezotolerant species. A presumptive function of pumping cytoplasmic protons at low pH is consistent with the experimentally observed increased expression of the V-ATPase in an acid-tolerant thaumarchaeote at low pH. Consistently, heterologous expression of the thaumarchaeotal V-ATPase significantly increased the growth rate of E. coli at low pH. Its adaptive significance to growth in ocean trenches may relate to pressure-related changes in membrane structure in which this complex molecular machine must function. Together, our findings reveal that the habitat expansion of Thaumarchaeota is tightly correlated with extensive horizontal transfer of atp operons.

Consistent with the observation that ammonia-oxidizing bacteria (AOB) outnumber ammonia-oxidizing archaea (AOA) in many eutrophic ecosystems globally, AOB typically dominate activated sludge aeration basins from municipal wastewater treatment plants (WWTPs). In this study, we demonstrate that the growth of AOA strains inoculated into sterile-filtered wastewater was inhibited significantly, in contrast to uninhibited growth of a reference AOB strain. In order to identify possible mechanisms underlying AOA-specific inhibition, we show that complex mixtures of organic compounds, such as yeast extract, were highly inhibitory to all AOA strains but not to the AOB strain. By testing individual organic compounds, we reveal strong inhibitory effects of organic compounds with high metal complexation potentials implying that the inhibitory mechanism for AOA can be explained by the reduced bioavailability of an essential metal. Our results further demonstrate that the inhibitory effect on AOA can be alleviated by copper supplementation, which we observed for pure AOA cultures in a defined medium and for AOA inoculated into nitrifying sludge. Our study offers a novel mechanistic explanation for the relatively low abundance of AOA in most WWTPs and provides a basis for modulating the composition of nitrifying communities in both engineered systems and naturally occurring environments.

The third domain Archaea was known to thrive in extreme or anoxic environments based on cultivation studies. Recent metagenomics-based approaches revealed a widespread abundance of archaea, including ammonia-oxidizing archaea (AOA) of Thaumarchaeota in non-extreme and oxic environments. AOA alter nitrogen species availability by mediating the first step of chemolithoautotrophic nitrification, ammonia oxidation to nitrite, and are important primary producers in ecosystems, which affects the distribution and activity of other organisms in ecosystems. Thus, information on the interactions of AOA with other cohabiting organisms is a crucial element in understanding nitrogen and carbon cycles in ecosystems as well as the functioning of whole ecosystems. AOA are self-nourishing, and thus interactions of AOA with other organisms can often be indirect and broad. Besides, there are possibilities of specific and obligate interactions. Mechanisms of interaction are often not clearly identified but only inferred due to limited knowledge on the interaction factors analyzed by current technologies. Here, we overviewed different types of AOA interactions with other cohabiting organisms, which contribute to understanding AOA functions in ecosystems.

Nitrification is a core process in the global nitrogen (N) cycle mediated by ammonia-oxidizing microorganisms, including ammonia-oxidizing archaea (AOA) as a key player. Although much is known about AOA abundance and diversity across environments, the genetic drivers of the ecophysiological adaptations of the AOA are often less clearly defined. This is especially true for AOA within the genus Nitrosocosmicus , which have several unique physiological traits (e.g., high substrate tolerance, low substrate affinity, and large cell size). To better understand what separates the physiology of Nitrosocosmicus AOA, we performed comparative genomics with genomes from 39 cultured AOA, including five Nitrosocosmicus AOA. The absence of a canonical high-affinity type ammonium transporter and typical S-layer structural genes was found to be conserved across all Nitrosocosmicus AOA. In agreement, cryo-electron tomography confirmed the absence of a visible outermost S-layer structure, which has been observed in other AOA. In contrast to other AOA, the cryo-electron tomography highlighted the possibility that Nitrosocosmicus AOA may possess a glycoprotein or glycolipid-based glycocalyx cell covering outer layer. Together, the genomic, physiological, and metabolic properties revealed in this study provide insight into niche adaptation mechanisms and the overall ecophysiology of members of the Nitrosocosmicus clade in various terrestrial ecosystems. IMPORTANCE: Nitrification is a vital process within the global biogeochemical nitrogen cycle but plays a significant role in the eutrophication of aquatic ecosystems and the production of the greenhouse gas nitrous oxide (N ₂ O) from industrial agriculture ecosystems. While various types of ammonia-oxidizing microorganisms play a critical role in the N cycle, ammonia-oxidizing archaea (AOA) are often the most abundant nitrifiers in natural environments. Members of the genus Nitrosocosmicus are one of the prevalent AOA groups detected in undisturbed terrestrial ecosystems and have previously been reported to possess a range of physiological characteristics that set their physiology apart from other AOA species. This study provides significant progress in understanding these unique physiological traits and their genetic drivers. Our results highlight how physiological studies based on comparative genomics-driven hypotheses can contribute to understanding the unique niche of Nitrosocosmicus AOA

Interactions between metals and microbes are critical in geomicrobiology and vital in microbial ecophysiological processes. Methane-oxidizing bacteria (MOB) and ammonia-oxidizing microorganisms (AOM) are key members in aerobic environments to start the C and N cycles. Ammonia and methane are firstly oxidized by copper-binding metalloproteins, monooxygenases, and diverse iron and copper-containing enzymes that contribute to electron transportation in the energy gain pathway, which is evolutionally connected between MOB and AOM. In this review, we summarized recently updated insight into the diverse physiological pathway of aerobic ammonia and methane oxidation of different MOB and AOM groups and compared the metabolic diversity mediated by different metalloenzymes. The elevation of iron and copper concentrations in ecosystems would be critical in the activity and growth of MOB and AOM, the outcome of which can eventually influence the global C and N cycles. Therefore, we also described the impact of various concentrations of metal compounds on the physiology of MOB and AOM. This review study could give a fundamental strategy to control MOB and AOM in diverse ecosystems because they are significantly related to climate change, eutrophication, and the remediation of contaminated sites for detoxifying pollutants.