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High and low rates of ammonium supply are believed to favour ammonia-oxidising bacteria (AOB) and archaea (AOA), respectively. Although their contrasting affinities for ammonium are suggested to account for these differences, the influence of ammonia concentration on AOA and AOB has not been tested under environmental conditions. In addition, while both AOB and AOA contribute to nitrous oxide (N 2 O) emissions from soil, N 2 O yields (N 2 O–N produced per NO 2 − –N generated from ammonia oxidation) of AOA are lower, suggesting lower emissions when AOA dominate ammonia oxidation. This study tested the hypothesis that ammonium supplied continuously at low rates is preferentially oxidised by AOA, with lower N 2 O yield than expected for AOB-dominated processes. Soil microcosms were supplied with water, urea or a slow release, urea-based fertiliser and 1-octyne (inhibiting only AOB) was applied to distinguish AOA and AOB activity and associated N 2 O production. Low ammonium supply, from mineralisation of organic matter, or of the fertiliser, led to growth, ammonia oxidation and N 2 O production by AOA only, with low N 2 O yield. High ammonium supply, from free urea within the fertiliser or after urea addition, led to growth of both groups, but AOB-dominated ammonia oxidation was associated with twofold greater N 2 O yield than that dominated by AOA. This study therefore demonstrates growth of both AOA and AOB at high ammonium concentration, confirms AOA dominance during low ammonium supply and suggests that slow release or organic fertilisers potentially mitigate N 2 O emissions through differences in niche specialisation and N 2 O production mechanisms in AOA and AOB.

The Terrestrial Miscellaneous Euryarchaeota Group has been identified in various environments, and the single genome investigated thus far suggests that these archaea are anaerobic sulfite reducers. We assemble 35 new genomes from this group that, based on genome analysis, appear to possess aerobic and facultative anaerobic lifestyles and may oxidise rather than reduce sulfite. We propose naming this order (representing 16 genera) “Lutacidiplasmatales” due to their occurrence in various acidic environments and placement within the phylum Thermoplasmatota. Phylum-level analysis reveals that Thermoplasmatota evolution had been punctuated by several periods of high levels of novel gene family acquisition. Several essential metabolisms, such as aerobic respiration and acid tolerance, were likely acquired independently by divergent lineages through convergent evolution rather than inherited from a common ancestor. Ultimately, this study describes the terrestrially prevalent Lutacidiciplasmatales and highlights convergent evolution as an important driving force in the evolution of archaeal lineages. Genome recovery of the order Lutacidiplasmatales reveals that key genes for environmental specialisation were acquired multiple times in the Thermoplasmatota phylum, suggesting a crucial role of convergent evolution in archaeal habitat adaptation.

Knowledge of deeply-rooted non-ammonia oxidising Thaumarchaeota lineages from terrestrial environments is scarce, despite their abundance in acidic soils. Here, 15 new deeply-rooted thaumarchaeotal genomes were assembled from acidic topsoils (0-15 cm) and subsoils (30-60 cm), corresponding to two genera of terrestrially prevalent Gagatemarchaeaceae (previously known as thaumarchaeotal Group I.1c) and to a novel genus of heterotrophic terrestrial Thaumarchaeota. Unlike previous predictions, metabolic annotations suggest Gagatemarchaeaceae perform aerobic respiration and use various organic carbon sources. Evolutionary divergence between topsoil and subsoil lineages happened early in Gagatemarchaeaceae history, with significant metabolic and genomic trait differences. Reconstruction of the evolutionary mechanisms showed that the genome expansion in topsoil Gagatemarchaeaceae resulted from extensive early lateral gene acquisition, followed by progressive gene duplication throughout evolutionary history. Ancestral trait reconstruction using the expanded genomic diversity also did not support the previous hypothesis of a thermophilic last common ancestor of the ammonia-oxidising archaea. Ultimately, this study provides a good model for studying mechanisms driving niche partitioning between spatially related ecosystems. Non-ammonia oxidising Thaumarachaeota lineages are common in acidic soils, but their evolution is unclear. Here, the authors assemble 15 genomes from deeply rooted Thaumarachaeota in topsoils and subsoils, investigating evolutionary divergence in the family Gagatemarchaeaceae.

The Thaumarchaeota is an abundant and ubiquitous phylum of archaea that plays a major role in the global nitrogen cycle. Previous analyses of the ammonia monooxygenase gene amoA suggest that pH is an important driver of niche specialization in these organisms. Although the ecological distribution and ecophysiology of extant Thaumarchaeota have been studied extensively, the evolutionary rise of these prokaryotes to ecological dominance in many habitats remains poorly understood. To characterize processes leading to their diversification, we investigated coevolutionary relationships between amoA , a conserved marker gene for Thaumarchaeota, and soil characteristics, by using deep sequencing and comprehensive environmental data in Bayesian comparative phylogenetics. These analyses reveal a large and rapid increase in diversification rates during early thaumarchaeotal evolution; this finding was verified by independent analyses of 16S rRNA. Our findings suggest that the entire Thaumarchaeota diversification regime was strikingly coupled to pH adaptation but less clearly correlated with several other tested environmental factors. Interestingly, the early radiation event coincided with a period of pH adaptation that enabled the terrestrial Thaumarchaeota ancestor to initially move from neutral to more acidic and alkaline conditions. In contrast to classic evolutionary models, whereby niches become rapidly filled after adaptive radiation, global diversification rates have remained stably high in Thaumarchaeota during the past 400–700 million years, suggesting an ongoing high rate of niche formation or switching for these microbes. Our study highlights the enduring importance of environmental adaptation during thaumarchaeotal evolution and, to our knowledge, is the first to link evolutionary diversification to environmental adaptation in a prokaryotic phylum. The link between species diversification and adaptation has long interested biologists working on multicellular eukaryotes, but remains poorly understood in prokaryotes, in which diversity is much greater. We tested the hypothesis that diversification is associated with environmental adaptation in Thaumarchaeota, an ancient and abundant microbial group and key player in the global nitrogen cycle. We provide evidence that the Thaumarchaeota underwent a major radiation event hundreds of millions of years ago that coincided with a major period of pH adaptation. Subsequently, these microbes have maintained high rates of diversification, potentially because of the high rate at which new terrestrial niches arise. This study provides a framework for comparing dynamics of evolutionary processes across the tree of life.

Thaumarchaeota form a ubiquitously distributed archaeal phylum, comprising both the ammonia-oxidising archaea (AOA) and other archaeal groups in which ammonia oxidation has not been demonstrated (including Group 1.1c and Group 1.3). The ecology of AOA in terrestrial environments has been extensively studied using either a functional gene, encoding ammonia monooxygenase subunit A ( amoA ) or 16S ribosomal RNA (rRNA) genes, which show phylogenetic coherence with respect to soil pH. To test phylogenetic congruence between these two markers and to determine ecological coherence in all Thaumarchaeota, we performed high-throughput sequencing of 16S rRNA and amoA genes in 46 UK soils presenting 29 available contextual soil characteristics. Adaptation to pH and organic matter content reflected strong ecological coherence at various levels of taxonomic resolution for Thaumarchaeota (AOA and non-AOA), whereas nitrogen, total mineralisable nitrogen and zinc concentration were also important factors associated with AOA thaumarchaeotal community distribution. Other significant associations with environmental factors were also detected for amoA and 16S rRNA genes, reflecting different diversity characteristics between these two markers. Nonetheless, there was significant statistical congruence between the markers at fine phylogenetic resolution, supporting the hypothesis of low horizontal gene transfer between Thaumarchaeota. Group 1.1c Thaumarchaeota were also widely distributed, with two clusters predominating, particularly in environments with higher moisture content and organic matter, whereas a similar ecological pattern was observed for Group 1.3 Thaumarchaeota. The ecological and phylogenetic congruence identified is fundamental to understand better the life strategies, evolutionary history and ecosystem function of the Thaumarchaeota.

Background Characterisation of microbial communities increasingly involves use of high throughput sequencing methods (e.g. MiSeq Illumina) that amplify relatively short sequences of 16S rRNA or functional genes, the latter including ammonia monooxygenase subunit A ( amoA) , a key functional gene for ammonia oxidising bacteria (AOB) and archaea (AOA). The availability of these techniques, in combination with developments in phylogenetic methodology, provides the potential for better analysis of microbial niche specialisation. This study aimed to develop an approach for sequencing of bacterial and archaeal amoA genes amplified from soil using bioinformatics pipelines developed for general analysis of functional genes and employed sequence data to reassess phylogeny and niche specialisation in terrestrial bacterial ammonia oxidisers. Results amoA richness and community composition differed with bioinformatics approaches used but analysis of MiSeq sequences was reliable for both archaeal and bacterial amoA genes and was used for subsequent assessment of potential niche specialisation of soil bacteria ammonia oxidisers. Prior to ecological analysis, phylogenetic analysis of Nitrosospira , which dominates soil AOB, was revisited using a phylogenetic analysis of 16S rRNA and amoA genes in available AOB genomes. This analysis supported congruence between phylogenies of the two genes and increased previous phylogenetic resolution, providing support for additional gene clusters of potential ecological significance. Analysis of environmental sequences using these new sequencing, bioinformatics and phylogenetic approaches demonstrated, for the first time, similar niche specialisation in AOB to that in AOA, indicating pH as a key ecological factor controlling the composition of soil ammonia oxidiser communities. Conclusions This study presents the first bioinformatics pipeline for optimal analysis of Illumina MiSeq sequencing of a functional gene and is adaptable to any amplicon size (even genes larger than 500 bp). The pipeline was used to provide an up-to-date phylogenetic analysis of terrestrial betaproteobacterial amoA genes and to demonstrate the importance of soil pH for their niche specialisation and is broadly applicable to other ecosystems and diverse microbiomes.

Biological Nitrification Inhibition (BNI) encompasses primarily NH4+‐induced release of secondary metabolites to impede the rhizospheric nitrifying microbes from performing nitrification. The intermediate wheatgrass Thinopyrum intermedium (Kernza®) is known for exuding several nitrification inhibition traits, but its BNI potential has not yet been identified. We hypothesized Kernza® to evince BNI potential through the presence and release of multiple BNI metabolites. The presence of BNI metabolites in the biomass of Kernza® and annual winter wheat (Triticum aestivum) and in the root exudates of hydroponically grown Kernza®, were fingerprinted using HPLC‐DAD and GC–MS/MS analyses. Growth bioassays involving ammonia‐oxidizing bacteria (AOB) and archaea (AOA) strains were conducted to assess the influence of the crude root metabolome of Kernza® and selected metabolites on nitrification. In most instances, significant concentrations of various metabolites with BNI potential were observed in the leaf and root biomass of Kernza® compared to annual winter wheat. Furthermore, NH4+ nutrition triggered the exudation of various phenolic BNI metabolites. Crude root exudates of Kernza® inhibited multiple AOB strains and completely inhibited N. viennensis. Vanillic acid, caffeic acid, vanillin, and phenylalanine suppressed the growth of all AOB and AOA strains tested, and reduced soil nitrification, while syringic acid and 2,6‐dihydroxybenzoic acid were ineffective. We demonstrated the considerable role of the Kernza® metabolome in suppressing nitrification through active exudation of multiple nitrification inhibitors.

Nitrification is a central component of the global nitrogen cycle. Ammonia oxidation, the first step of nitrification, is performed in terrestrial ecosystems by both ammonia‐oxidizing bacteria (AOB) and ammonia‐oxidizing archaea (AOA). Published studies indicate that soil pH may be a critical factor controlling the relative abundances of AOA and AOB communities. In order to determine the relative contributions of AOA and AOB to ammonia oxidation in two agricultural acidic Scottish soils (pH 4.5 and 6), the influence of acetylene (a nitrification inhibitor) was investigated during incubation of soil microcosms at 20 °C for 1 month. High rates of nitrification were observed in both soils in the absence of acetylene. Quantification of respective amoA genes (a key functional gene for ammonia oxidizers) demonstrated significant growth of AOA, but not AOB. A significant positive relationship was found between nitrification rate and AOA, but not AOB growth. AOA growth was inhibited in the acetylene‐containing microcosms. Moreover, AOA transcriptional activity decreased significantly in the acetylene‐containing microcosms compared with the control, whereas no difference was observed for the AOB transcriptional activity. Consequently, growth and activity of only archaeal but not bacterial ammonia oxidizer communities strongly suggest that AOA, but not AOB, control nitrification in these two acidic soils.

Nitrification is a major process within the nitrogen (N) cycle leading to global losses of N, including fertiliser N, from natural and agricultural systems and producing significant nitrous oxide emissions. One strategy for the mitigation of these losses involves nitrification inhibition by plant-derived biological nitrification inhibitors (BNIs). Cultivation-based studies of BNIs, including screening for new compounds, have predominantly investigated inhibition of a single ammonia-oxidising bacterium (AOB), Nitrosomonas europaea, even though ammonia oxidation in soil is usually dominated by ammonia-oxidising archaea (AOA), especially in acidic soils, and AOB Nitrosospira sp., rather than Nitrosomonas, in fertilised soils. This study aimed to assess the sensitivity of ammonia oxidation by a range of AOA and AOB pure cultures to BNIs produced by plant roots (methyl 3-(4-hydroxyphenyl) propionate, sakuranetin and 1,9-decanediol) and shoots (linoleic acid, linolenic acid and methyl linoleate). AOA were generally more sensitive to BNIs than AOB, and sensitivity was greater to BNIs produced by shoots than those produced by roots. Sensitivity also varied within AOA and AOB cultures and between different BNIs. In general, N. europaea was not a good indicator of BNI inhibition, and findings therefore highlight the limitations of use of a single bioassay strain and suggest the use of a broader range of strains that are more representative of natural soil communities.

Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle, but the mechanisms driving their radiation into diverse ecosystems remain underexplored. Here, existing thaumarchaeotal genomes are complemented with 12 genomes belonging to the previously under-sampled Nitrososphaerales to investigate the impact of lateral gene transfer (LGT), gene duplication and loss across thaumarchaeotal evolution. We reveal a major role for gene duplication in driving genome expansion subsequent to early LGT. In particular, two large LGT events are identified into Nitrososphaerales and the fate of these gene families is highly lineage-specific, being lost in some descendant lineages, but undergoing extensive duplication in others, suggesting niche-specific roles. Notably, some genes involved in carbohydrate transport or coenzyme metabolism were duplicated, likely facilitating niche specialisation in soils and sediments. Overall, our results suggest that LGT followed by gene duplication drives Nitrososphaerales evolution, highlighting a previously under-appreciated mechanism of genome expansion in archaea. Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle. Using 12 new genomes, this study finds evidence that Nitrososphaerales evolution was marked by lateral gene transfer followed by gene duplication.