Publications by authors named "James I Prosser"

107 Publications

Towards meaningful scales in ecosystem microbiome research.

Environ Microbiol 2021 01 21;23(1):1-4. Epub 2020 Oct 21.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

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http://dx.doi.org/10.1111/1462-2920.15276DOI Listing
January 2021

Differential Ecosystem Function Stability of Ammonia-Oxidizing Archaea and Bacteria following Short-Term Environmental Perturbation.

mSystems 2020 Jun 16;5(3). Epub 2020 Jun 16.

School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom

Rapidly expanding conversion of tropical forests to oil palm plantations in Southeast Asia leads to soil acidification following intensive nitrogen fertilization. Changes in soil pH are predicted to have an impact on archaeal ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), and complete (comammox) ammonia oxidizers and, consequently, on nitrification. It is therefore critical to determine whether the predicted effects of pH on ammonia oxidizers and nitrification activity apply in tropical soils subjected to various degrees of anthropogenic activity. This was investigated by experimental manipulation of pH in soil microcosms from a land-use gradient (forest, riparian, and oil palm soils). The nitrification rate was greater in forest soils with native neutral pH than in converted acidic oil palm soils. Ammonia oxidizer activity decreased following acidification of the forest soils but increased after liming of the oil palm soils, leading to a trend of a reversed net nitrification rate after pH modification. AOA and AOB nitrification activity was dependent on pH, but AOB were more sensitive to pH modification than AOA, which demonstrates a greater stability of AOA than AOB under conditions of short-term perturbation. In addition, these results predict AOB to be a good bioindicator of nitrification response following pH perturbation during land-use conversion. AOB and/or comammox species were active in all soils along the land-use gradient, even, unexpectedly, under acidic conditions, suggesting their adaptation to native acidic or acidified soils. The present study therefore provided evidence for limited stability of soil ammonia oxidizer activity following intensive anthropogenic activities, which likely aggravates the vulnerability of nitrogen cycle processes to environmental disturbance. Physiological and ecological studies have provided evidence for pH-driven niche specialization of ammonia oxidizers in terrestrial ecosystems. However, the functional stability of ammonia oxidizers following pH change has not been investigated, despite its importance in understanding the maintenance of ecosystem processes following environmental perturbation. This is particularly true after anthropogenic perturbation, such as the conversion of tropical forest to oil palm plantations. This study demonstrated a great impact of land-use conversion on nitrification, which is linked to changes in soil pH due to common agricultural practices (intensive fertilization). In addition, the different communities of ammonia oxidizers were differently affected by short-term pH perturbations, with implications for future land-use conversions but also for increased knowledge of associated global nitrous oxide emissions and current climate change concerns.
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http://dx.doi.org/10.1128/mSystems.00309-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7300361PMC
June 2020

Conceptual challenges in microbial community ecology.

Philos Trans R Soc Lond B Biol Sci 2020 05 23;375(1798):20190241. Epub 2020 Mar 23.

Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, USA.

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http://dx.doi.org/10.1098/rstb.2019.0241DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7133534PMC
May 2020

Putting science back into microbial ecology: a question of approach.

Authors:
James I Prosser

Philos Trans R Soc Lond B Biol Sci 2020 05 23;375(1798):20190240. Epub 2020 Mar 23.

School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK.

Microbial ecology, the scientific study of interactions between natural microbial communities and their environments, has been facilitated by the application of molecular and 'omics'-based techniques that overcome some of the limitations of cultivation-based studies. This has increased emphasis on community ecology and 'microbiome' studies, but the majority address technical, rather than scientific challenges. Most are descriptive, do not address scientific aims or questions and are not designed to increase understanding or test hypotheses. The term 'hypothesis' is increasingly misused and critical testing of ideas or theory is restricted to a small minority of studies. This article discusses current microbial ecology research within the context of four approaches: description, induction, inference to the best explanation and deduction. The first three of these do not follow the established scientific method and are not based on scientific ecological questions. Observations are made and sometimes compared with published data, sometimes with attempts to explain findings in the context of existing ideas or hypotheses, but all lack objectivity and are biased by the observations made. By contrast, deductive studies address ecological questions and attempt to explain currently unexplained phenomena through the construction of hypotheses, from mechanism-based assumptions, that generate predictions that are then tested experimentally. Identification of key scientific questions, research driven by meaningful hypotheses and adoption of scientific method are essential for progress in microbial ecology, rather than the current emphasis on descriptive approaches that address only technical challenges. It is, therefore, imperative that we carefully consider and define the fundamental scientific questions that drive our own research and focus on ideas, concepts and hypotheses that can increase understanding, and only then consider which techniques are required for experimental testing. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.
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http://dx.doi.org/10.1098/rstb.2019.0240DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7133526PMC
May 2020

Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies.

Glob Chang Biol 2020 01 29;26(1):103-118. Epub 2019 Nov 29.

Laboratoire Ampère, École Centrale de Lyon, Université de Lyon, Lyon, France.

Oxidation of ammonia to nitrite by bacteria and archaea is responsible for global emissions of nitrous oxide directly and indirectly through provision of nitrite and, after further oxidation, nitrate to denitrifiers. Their contributions to increasing N O emissions are greatest in terrestrial environments, due to the dramatic and continuing increases in use of ammonia-based fertilizers, which have been driven by requirement for increased food production, but which also provide a source of energy for ammonia oxidizers (AO), leading to an imbalance in the terrestrial nitrogen cycle. Direct N O production by AO results from several metabolic processes, sometimes combined with abiotic reactions. Physiological characteristics, including mechanisms for N O production, vary within and between ammonia-oxidizing archaea (AOA) and bacteria (AOB) and comammox bacteria and N O yield of AOB is higher than in the other two groups. There is also strong evidence for niche differentiation between AOA and AOB with respect to environmental conditions in natural and engineered environments. In particular, AOA are favored by low soil pH and AOA and AOB are, respectively, favored by low rates of ammonium supply, equivalent to application of slow-release fertilizer, or high rates of supply, equivalent to addition of high concentrations of inorganic ammonium or urea. These differences between AOA and AOB provide the potential for better fertilization strategies that could both increase fertilizer use efficiency and reduce N O emissions from agricultural soils. This article reviews research on the biochemistry, physiology and ecology of AO and discusses the consequences for AO communities subjected to different agricultural practices and the ways in which this knowledge, coupled with improved methods for characterizing communities, might lead to improved fertilizer use efficiency and mitigation of N O emissions.
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http://dx.doi.org/10.1111/gcb.14877DOI Listing
January 2020

Genome Sequence of " Nitrosocosmicus franklandus" C13, a Terrestrial Ammonia-Oxidizing Archaeon.

Microbiol Resour Announc 2019 Oct 3;8(40). Epub 2019 Oct 3.

School of Biological Sciences, University of East Anglia, Norwich, United Kingdom.

" Nitrosocosmicus franklandus" C13 is an ammonia-oxidizing archaeon (AOA) isolated from soil. Its complete genome is 2.84 Mb and possesses predicted AOA metabolic pathways for energy generation and carbon dioxide fixation but no typical surface layer (S-layer) proteins, only one ammonium transporter, and divergent A-type ATP synthase genes.
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http://dx.doi.org/10.1128/MRA.00435-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776761PMC
October 2019

The application of high-throughput sequencing technology to analysis of amoA phylogeny and environmental niche specialisation of terrestrial bacterial ammonia-oxidisers.

Environ Microbiome 2019 Jul 4;14(1). Epub 2019 Jul 4.

School of Biological Sciences, Cruickshank Building, University of Aberdeen, St. Machar Drive, Aberdeen, AB24 3UU, UK.

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.
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http://dx.doi.org/10.1186/s40793-019-0342-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7989807PMC
July 2019

Approaches to understanding the ecology and evolution of understudied terrestrial archaeal ammonia-oxidisers.

Emerg Top Life Sci 2018 Dec;2(4):619-628

School of Biological Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen AB24 3UU, U.K.

Ammonia-oxidising archaea (AOA) form a phylogenetic group within the phylum Thaumarchaeota and are of ecological significance due to their role in nitrification, an important biogeochemical process. Previous research has provided information on their ecosystem role and potential physiological characteristics, for example, through analyses of their environmental distribution, ecological adaptation and evolutionary history. However, most AOA diversity, assessed using several environmental marker genes, is not represented in laboratory cultures, with consequent gaps in knowledge of their physiology and evolution. The present study critically reviews existing and developing approaches for the assessment of AOA function and diversity and their potential to provide a deeper understanding of these ecologically important, but understudied microorganisms.
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http://dx.doi.org/10.1042/ETLS20180018DOI Listing
December 2018

Soil bacterial networks are less stable under drought than fungal networks.

Nat Commun 2018 08 2;9(1):3033. Epub 2018 Aug 2.

School of Earth and Environmental Sciences, The University of Manchester, Oxford Road, Manchester, M13 9PT, UK.

Soil microbial communities play a crucial role in ecosystem functioning, but it is unknown how co-occurrence networks within these communities respond to disturbances such as climate extremes. This represents an important knowledge gap because changes in microbial networks could have implications for their functioning and vulnerability to future disturbances. Here, we show in grassland mesocosms that drought promotes destabilising properties in soil bacterial, but not fungal, co-occurrence networks, and that changes in bacterial communities link more strongly to soil functioning during recovery than do changes in fungal communities. Moreover, we reveal that drought has a prolonged effect on bacterial communities and their co-occurrence networks via changes in vegetation composition and resultant reductions in soil moisture. Our results provide new insight in the mechanisms through which drought alters soil microbial communities with potential long-term consequences, including future plant community composition and the ability of aboveground and belowground communities to withstand future disturbances.
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http://dx.doi.org/10.1038/s41467-018-05516-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6072794PMC
August 2018

The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions.

ISME J 2018 04 31;12(4):1084-1093. Epub 2018 Jan 31.

School of Biological Sciences, University of Aberdeen, Cruickshank Building, Aberdeen, AB24 3UU, UK.

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 (NO) emissions from soil, NO yields (NO-N produced per NO-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 NO 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 NO production. Low ammonium supply, from mineralisation of organic matter, or of the fertiliser, led to growth, ammonia oxidation and NO production by AOA only, with low NO 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 NO 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 NO emissions through differences in niche specialisation and NO production mechanisms in AOA and AOB.
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http://dx.doi.org/10.1038/s41396-017-0025-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5864188PMC
April 2018

Ammonia-oxidising archaea living at low pH: Insights from comparative genomics.

Environ Microbiol 2017 Dec 4;19(12):4939-4952. Epub 2017 Dec 4.

School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen, AB24 3UU, UK.

Obligate acidophilic members of the thaumarchaeotal genus Candidatus Nitrosotalea play an important role in nitrification in acidic soils, but their evolutionary and physiological adaptations to acidic environments are still poorly understood, with only a single member of this genus (Ca. N. devanaterra) having its genome sequenced. In this study, we sequenced the genomes of two additional cultured Ca. Nitrosotalea strains, extracted an almost complete Ca. Nitrosotalea metagenome-assembled genome from an acidic fen, and performed comparative genomics of the four Ca. Nitrosotalea genomes with 19 other archaeal ammonia oxidiser genomes. Average nucleotide and amino acid identities revealed that the four Ca. Nitrosotalea strains represent separate species within the genus. The four Ca. Nitrosotalea genomes contained a core set of 103 orthologous gene families absent from all other ammonia-oxidizing archaea and, for most of these gene families, expression could be demonstrated in laboratory culture or the environment via proteomic or metatranscriptomic analyses respectively. Phylogenetic analyses indicated that four of these core gene families were acquired by the Ca. Nitrosotalea common ancestor via horizontal gene transfer from acidophilic representatives of Euryarchaeota. We hypothesize that gene exchange with these acidophiles contributed to the competitive success of the Ca. Nitrosotalea lineage in acidic environments.
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http://dx.doi.org/10.1111/1462-2920.13971DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5767755PMC
December 2017

Links between seawater flooding, soil ammonia oxidiser communities and their response to changes in salinity.

FEMS Microbiol Ecol 2017 11;93(11)

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, Aberdeen AB24 3UU, UK.

Coastal areas worldwide are challenged by climate change-associated increases in sea level and storm surge quantities that potentially lead to more frequent flooding of soil ecosystems. Currently, little is known of the effects of inundation events on microorganisms controlling nitrification in these ecosystems. The goal of this study was to investigate the impact of seawater flooding on the abundance, community composition and salinity tolerance of soil ammonia oxidisers. Topsoil was sampled from three islands flooded at different frequencies by the Wadden Sea. Archaeal ammonia oxidiser amoA genes were more abundant than their betaproteobacterial counterparts, and the distribution of archaeal and bacterial ammonia oxidiser amoA and 16S rRNA gene sequences significantly differed between the islands. The findings indicate selection of ammonia oxidiser phylotypes with greater tolerance to high salinity and slightly alkaline pH (e.g. Nitrosopumilus representatives) in frequently flooded soils. A cluster phylogenetically related to gammaproteobacterial ammonia oxidisers was detected in all samples analysed in this survey. Nevertheless, no gammaprotebacterial amoA genes could be amplified via PCR and only betaproteobacterial ammonia oxidisers were detected in enrichment cultures. A slurry-based experiment demonstrated the tolerance of both bacterial and archaeal ammonia oxidisers to a wide range of salinities (e.g. Wadden Sea water salinity) in soil naturally exposed to seawater at a high frequency.
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http://dx.doi.org/10.1093/femsec/fix144DOI Listing
November 2017

Abiotic Conversion of Extracellular NHOH Contributes to NO Emission during Ammonia Oxidation.

Environ Sci Technol 2017 Nov 31;51(22):13122-13132. Epub 2017 Oct 31.

Institute of Bio- and Geosciences-Agrosphere (IBG-3), Forschungszentrum Jülich GmbH , 52425 Jülich, Germany.

Abiotic processes involving the reactive ammonia-oxidation intermediates nitric oxide (NO) or hydroxylamine (NHOH) for NO production have been indicated recently. The latter process would require the availability of substantial amounts of free NHOH for chemical reactions during ammonia (NH) oxidation, but little is known about extracellular NHOH formation by the different clades of ammonia-oxidizing microbes. Here we determined extracellular NHOH concentrations in culture media of several ammonia-oxidizing bacteria (AOB) and archaea (AOA), as well as one complete ammonia oxidizer (comammox) enrichment (Ca. Nitrospira inopinata) during incubation under standard cultivation conditions. NHOH was measurable in the incubation media of Nitrosomonas europaea, Nitrosospira multiformis, Nitrososphaera gargensis, and Ca. Nitrosotenuis uzonensis, but not in media of the other tested AOB and AOA. NHOH was also formed by the comammox enrichment during NH oxidation. This enrichment exhibited the largest NHOH:final product ratio (1.92%), followed by N. multiformis (0.56%) and N. gargensis (0.46%). The maximum proportions of NH converted to NO via extracellular NHOH during incubation, estimated on the basis of NHOH abiotic conversion rates, were 0.12%, 0.08%, and 0.14% for AOB, AOA, and Ca. Nitrospira inopinata, respectively, and were consistent with published NH:NO conversion ratios for AOB and AOA.
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http://dx.doi.org/10.1021/acs.est.7b02360DOI Listing
November 2017

Ammonia oxidisers in a non-nitrifying Brazilian savanna soil.

FEMS Microbiol Ecol 2017 11;93(11)

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen AB24 3UU, UK.

Low nitrification rates in Brazilian savanna (Cerrado) soils have puzzled researchers for decades. Potential mechanisms include biological inhibitors, low pH, low microbial abundance and low soil moisture content, which hinders microbial activity, including ammonia oxidation. Two approaches were used to evaluate these potential mechanisms: (i) manipulation of soil moisture and pH in microcosms containing Cerrado soil and (ii) assessment of nitrification inhibition in slurries containing mixtures of Cerrado soil and an actively nitrifying agricultural soil. Despite high ammonium concentration in Cerrado soil microcosms, little NO3- accumulation was observed with increasing moisture or pH, but in some Cerrado soil slurries, ammonia-oxidising archaea (AOA) amoA transcripts were detected after 14 days. In mixed soil slurries, the final NO3- concentration reflected the initial proportions of agricultural and Cerrado soils in the mixture, providing no evidence of nitrification inhibitors in Cerrado soil. AOA community denaturing gradient gel electrophoresis profiles were similar in the mixed and nitrifying soils. These results suggest that nitrification in Cerrado soils is not constrained by water availability, ammonium availability, low pH or biological inhibitors, and alternative potential explanations for low nitrification levels are discussed.
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http://dx.doi.org/10.1093/femsec/fix122DOI Listing
November 2017

Spotlight on… Jim Prosser.

Authors:
James I Prosser

FEMS Microbiol Lett 2017 10;364(18)

School of Biological Sciences, University of Aberdeen, Cruickshank Building, Aberdeen AB24 3UU, United Kingdom.

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http://dx.doi.org/10.1093/femsle/fnx183DOI Listing
October 2017

Kinetics of NH -oxidation, NO-turnover, N O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers.

Environ Microbiol 2017 Dec 21;19(12):4882-4896. Epub 2017 Sep 21.

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432, Ås, Norway.

Ammonia oxidising bacteria (AOB) are thought to emit more nitrous oxide (N O) than ammonia oxidising archaea (AOA), due to their higher N O yield under oxic conditions and denitrification in response to oxygen (O ) limitation. We determined the kinetics of growth and turnover of nitric oxide (NO) and N O at low cell densities of Nitrosomonas europaea (AOB) and Nitrosopumilus maritimus (AOA) during gradual depletion of TAN (NH  + NH4+) and O . Half-saturation constants for O and TAN were similar to those determined by others, except for the half-saturation constant for ammonium in N. maritimus (0.2 mM), which is orders of magnitudes higher than previously reported. For both strains, cell-specific rates of NO turnover and N O production reached maxima near O half-saturation constant concentration (2-10 μM O ) and decreased to zero in response to complete O -depletion. Modelling of the electron flow in N. europaea demonstrated low electron flow to denitrification (≤1.2% of the total electron flow), even at sub-micromolar O concentrations. The results corroborate current understanding of the role of NO in the metabolism of AOA and suggest that denitrification is inconsequential for the energy metabolism of AOB, but possibly important as a route for dissipation of electrons at high ammonium concentration.
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http://dx.doi.org/10.1111/1462-2920.13914DOI Listing
December 2017

Chemotaxonomic characterisation of the thaumarchaeal lipidome.

Environ Microbiol 2017 07 19;19(7):2681-2700. Epub 2017 May 19.

Organic Geochemistry Group, MARUM - Center for Marine Environmental Sciences & Department of Geosciences, University of Bremen, Bremen, 28359, Germany.

Thaumarchaeota are globally distributed and abundant microorganisms occurring in diverse habitats and thus represent a major source of archaeal lipids. The scope of lipids as taxonomic markers in microbial ecological studies is limited by the scarcity of comparative data on the membrane lipid composition of cultivated representatives, including the phylum Thaumarchaeota. Here, we comprehensively describe the core and intact polar lipid (IPL) inventory of ten ammonia-oxidising thaumarchaeal cultures representing all four characterized phylogenetic clades. IPLs of these thaumarchaeal strains are generally similar and consist of membrane-spanning, glycerol dibiphytanyl glycerol tetraethers with monoglycosyl, diglycosyl, phosphohexose and hexose-phosphohexose headgroups. However, the relative abundances of these IPLs and their core lipid compositions differ systematically between the phylogenetic subgroups, indicating high potential for chemotaxonomic distinction of thaumarchaeal clades. Comparative lipidomic analyses of 19 euryarchaeal and crenarchaeal strains suggested that the lipid methoxy archaeol is synthesized exclusively by Thaumarchaeota and may thus represent a diagnostic lipid biomarker for this phylum. The unprecedented diversity of the thaumarchaeal lipidome with 118 different lipids suggests that membrane lipid composition and adaptation mechanisms in Thaumarchaeota are more complex than previously thought and include unique lipids with as yet unresolved properties.
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http://dx.doi.org/10.1111/1462-2920.13759DOI Listing
July 2017

Stream drying drives microbial ammonia oxidation and first-flush nitrate export.

Ecology 2016 Sep;97(9):2192-2198

Department of Plant Biology and Ecology, Faculty of Science and Technology, University of the Basque Country, PO Box 644, 48080, Bilbao, Spain.

Stream microbial communities and associated processes are influenced by environmental fluctuations that may ultimately dictate nutrient export. Discharge fluctuations caused by intermittent stream flow are increasing worldwide in response to global change. We examined the impact of flow cessation and drying on in-stream nitrogen cycling. We determined archaeal (AOA) and bacterial ammonia oxidizer (AOB) abundance and ammonia oxidation activity in surface and deep sediments from different sites along the Fuirosos stream (Spain) subjected to contrasting hydrological conditions (i.e., running water, isolated pools, and dry streambeds). AOA were more abundant than AOB, with no major changes across hydrological conditions or sediment layers. However, ammonia oxidation activity and sediment nitrate content increased with the degree of stream drying, especially in surface sediments. Upscaling of our results shows that ammonia oxidation in dry streambeds can contribute considerably (~50%) to the high nitrate export typically observed in intermittent streams during first-flush events following flow reconnection. Our study illustrates how the dry channels of intermittent streams can be potential hotspots of ammonia oxidation. Consequently, shifts in the duration, spatial extent and severity of intermittent flow can play a decisive role in shaping nitrogen cycling and export along fluvial networks in response to global change.
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http://dx.doi.org/10.1002/ecy.1486DOI Listing
September 2016

The Role of Microbial Community Composition in Controlling Soil Respiration Responses to Temperature.

PLoS One 2016 31;11(10):e0165448. Epub 2016 Oct 31.

University of Aberdeen, Cruickshank Building St Machar Drive, Aberdeen AB24 3UU, United Kingdom.

Rising global temperatures may increase the rates of soil organic matter decomposition by heterotrophic microorganisms, potentially accelerating climate change further by releasing additional carbon dioxide (CO2) to the atmosphere. However, the possibility that microbial community responses to prolonged warming may modify the temperature sensitivity of soil respiration creates large uncertainty in the strength of this positive feedback. Both compensatory responses (decreasing temperature sensitivity of soil respiration in the long-term) and enhancing responses (increasing temperature sensitivity) have been reported, but the mechanisms underlying these responses are poorly understood. In this study, microbial biomass, community structure and the activities of dehydrogenase and β-glucosidase enzymes were determined for 18 soils that had previously demonstrated either no response or varying magnitude of enhancing or compensatory responses of temperature sensitivity of heterotrophic microbial respiration to prolonged cooling. The soil cooling approach, in contrast to warming experiments, discriminates between microbial community responses and the consequences of substrate depletion, by minimising changes in substrate availability. The initial microbial community composition, determined by molecular analysis of soils showing contrasting respiration responses to cooling, provided evidence that the magnitude of enhancing responses was partly related to microbial community composition. There was also evidence that higher relative abundance of saprophytic Basidiomycota may explain the compensatory response observed in one soil, but neither microbial biomass nor enzymatic capacity were significantly affected by cooling. Our findings emphasise the key importance of soil microbial community responses for feedbacks to global change, but also highlight important areas where our understanding remains limited.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0165448PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5087920PMC
June 2017

A timely reminder of technical limitations.

Authors:
James I Prosser

Microb Biotechnol 2016 07;9(4):435

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen, AB24 3UU, UK.

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http://dx.doi.org/10.1111/1751-7915.12376DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4919984PMC
July 2016

Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance.

FEMS Microbiol Ecol 2016 07 28;92(7). Epub 2016 Apr 28.

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen, AB24 5UU, UK.

The influence of plants on archaeal (AOA) and bacterial (AOB) ammonia oxidisers (AO) is poorly understood. Higher microbial activity in the rhizosphere, including organic nitrogen (N) mineralisation, may stimulate both groups, while ammonia uptake by plants may favour AOA, considered to prefer lower ammonia concentration. We therefore hypothesised (i) higher AOA and AOB abundances in the rhizosphere than bulk soil and (ii) that AOA are favoured over AOB in the rhizosphere of plants with an exploitative strategy and high N demand, especially (iii) during early growth, when plant N uptake is higher. These hypotheses were tested by growing 20 grassland plants, covering a spectrum of resource-use strategies, and determining AOA and AOB amoA gene abundances, rhizosphere and bulk soil characteristics and plant functional traits. Joint Bayesian mixed models indicated no increase in AO in the rhizosphere, but revealed that AOA were more abundant in the rhizosphere of exploitative plants, mostly grasses, and less abundant under conservative plants. In contrast, AOB abundance in the rhizosphere and bulk soil depended on pH, rather than plant traits. These findings provide a mechanistic basis for plant-ammonia oxidiser interactions and for links between plant functional traits and ammonia oxidiser ecology.
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http://dx.doi.org/10.1093/femsec/fiw091DOI Listing
July 2016

Isolation of 'Candidatus Nitrosocosmicus franklandus', a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration.

FEMS Microbiol Ecol 2016 May 13;92(5):fiw057. Epub 2016 Mar 13.

Institute of Biological and Environmental Sciences, Cruickshank Building, St Machar Drive, University of Aberdeen, Aberdeen AB24 3UU, UK.

Studies of the distribution of ammonia oxidising archaea (AOA) and bacteria (AOB) suggest distinct ecological niches characterised by ammonia concentration and pH, arising through differences in substrate affinity and ammonia tolerance. AOA form five distinct phylogenetic clades, one of which, the 'Nitrososphaera sister cluster', has no cultivated isolate. A representative of this cluster, named 'Candidatus Nitrosocosmicus franklandus', was isolated from a pH 7.5 arable soil and we propose a new cluster name:'Nitrosocosmicus' While phylogenetic analysis of amoA genes indicates its association with the Nitrososphaera sister cluster, analysis of 16S rRNA genes provided no support for a relative branching that is consistent with a 'sister cluster', indicating placement within a lineage of the order Nitrososphaerales 'Ca.N. franklandus' is capable of ureolytic growth and its tolerances to nitrite and ammonia are higher than in other AOA and similar to those of typical soil AOB. Similarity of other growth characteristics of 'Ca.N. franklandus' with those of typical soil AOB isolates reduces support for niche differentiation between soil AOA and AOB and suggests that AOA have a wider physiological diversity than previously suspected. In particular, the high ammonia tolerance of 'Ca.N. franklandus' suggests potential contributions to nitrification in fertilised soils.
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http://dx.doi.org/10.1093/femsec/fiw057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4830249PMC
May 2016

Archaea produce lower yields of N O than bacteria during aerobic ammonia oxidation in soil.

Environ Microbiol 2017 Dec 28;19(12):4829-4837. Epub 2016 Apr 28.

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen, AB24 3UU, UK.

Nitrogen fertilisation of agricultural soil contributes significantly to emissions of the potent greenhouse gas nitrous oxide (N O), which is generated during denitrification and, in oxic soils, mainly by ammonia oxidisers. Although laboratory cultures of ammonia oxidising bacteria (AOB) and archaea (AOA) produce N O, their relative activities in soil are unknown. This work tested the hypothesis that AOB dominate ammonia oxidation and N O production under conditions of high inorganic ammonia (NH ) input, but result mainly from the activity of AOA when NH is derived from mineralisation. 1-octyne, a recently discovered inhibitor of AOB, was used to distinguish N O production resulting from archaeal and bacterial ammonia oxidation in soil microcosms, and specifically inhibited AOB growth, activity and N O production. In unamended soils, ammonia oxidation and N O production were lower and resulted mainly from ammonia oxidation by AOA. The AOA N O yield relative to nitrite produced was half that of AOB, likely due to additional enzymatic mechanisms in the latter, but ammonia oxidation and N O production were directly linked in all treatments. Relative contributions of AOA and AOB to N O production, therefore, reflect their respective contributions to ammonia oxidation. These results suggest potential mitigation strategies for N O emissions from fertilised agricultural soils.
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http://dx.doi.org/10.1111/1462-2920.13282DOI Listing
December 2017

Identifying Potential Mechanisms Enabling Acidophily in the Ammonia-Oxidizing Archaeon "Candidatus Nitrosotalea devanaterra".

Appl Environ Microbiol 2016 May 18;82(9):2608-2619. Epub 2016 Apr 18.

Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, United Kingdom.

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.
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http://dx.doi.org/10.1128/AEM.04031-15DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4836417PMC
May 2016

Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota.

Proc Natl Acad Sci U S A 2015 07 13;112(30):9370-5. Epub 2015 Jul 13.

Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 2TZ, United Kingdom;

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.
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http://dx.doi.org/10.1073/pnas.1419329112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4522744PMC
July 2015

Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota.

ISME J 2016 Jan 3;10(1):85-96. Epub 2015 Jul 3.

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, Aberdeen, UK.

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.
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http://dx.doi.org/10.1038/ismej.2015.101DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4604658PMC
January 2016

Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology.

Authors:
James I Prosser

Nat Rev Microbiol 2015 07 8;13(7):439-46. Epub 2015 Jun 8.

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen, AB24 3UU, UK.

Technological advances are enabling the sequencing of environmental DNA and RNA at increasing depth and with decreasing costs. Metagenomic and transcriptomic analysis of soil microbial communities and the assembly of 'population genomes' from soil DNA are therefore now feasible. Although the value of such 'omic' approaches is limited by the associated technical and bioinformatic difficulties, even if these obstacles were eliminated and 'perfect' metagenomes and metatranscriptomes were available, important conceptual challenges remain. This Opinion article considers these conceptual challenges in the context of the current use of omics in soil microbiology, but the main arguments presented are also relevant to the application of omics to marine, freshwater, gut or other environments.
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http://dx.doi.org/10.1038/nrmicro3468DOI Listing
July 2015

Ammonia oxidation is not required for growth of Group 1.1c soil Thaumarchaeota.

FEMS Microbiol Ecol 2015 Mar 13;91(3). Epub 2015 Jan 13.

Institute of Biological and Environmental Sciences, Cruickshank Building, St Machar Drive, University of Aberdeen, Aberdeen, AB24 3UU, UK.

Thaumarchaeota are among the most abundant organisms on Earth and are ubiquitous. Within this phylum, all cultivated representatives of Group 1.1a and Group 1.1b Thaumarchaeota are ammonia oxidizers, and play a key role in the nitrogen cycle. While Group 1.1c is phylogenetically closely related to the ammonia-oxidizing Thaumarchaeota and is abundant in acidic forest soils, nothing is known about its physiology or ecosystem function. The goal of this study was to perform in situ physiological characterization of Group 1.1c Thaumarchaeota by determining conditions that favour their growth in soil. Several acidic grassland, birch and pine tree forest soils were sampled and those with the highest Group 1.1c 16S rRNA gene abundance were incubated in microcosms to determine optimal growth temperature, ammonia oxidation and growth on several organic compounds. Growth of Group 1.1c Thaumarchaeota, assessed by qPCR of Group 1.1c 16S rRNA genes, occurred in soil, optimally at 30°C, but was not associated with ammonia oxidation and the functional gene amoA could not be detected. Growth was also stimulated by addition of organic nitrogen compounds (glutamate and casamino acids) but not when supplemented with organic carbon alone. This is the first evidence for non-ammonia oxidation associated growth of Thaumarchaeota in soil.
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http://dx.doi.org/10.1093/femsec/fiv001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4399444PMC
March 2015

pH as a Driver for Ammonia-Oxidizing Archaea in Forest Soils.

Microb Ecol 2015 May 12;69(4):879-83. Epub 2014 Dec 12.

Environmental Genomics, Helmholtz Zentrum München, German Research Centre for Environmental Health, Ingolstädter Landstraße 1, 85764, Neuherberg, Germany.

In this study, we investigated the impact of soil pH on the diversity and abundance of archaeal ammonia oxidizers in 27 different forest soils across Germany. DNA was extracted from topsoil samples, the amoA gene, encoding ammonia monooxygenase, was amplified; and the amplicons were sequenced using a 454-based pyrosequencing approach. As expected, the ratio of archaeal (AOA) to bacterial (AOB) ammonia oxidizers' amoA genes increased sharply with decreasing soil pH. The diversity of AOA differed significantly between sites with ultra-acidic soil pH (<3.5) and sites with higher pH values. The major OTUs from soil samples with low pH could be detected at each site with a soil pH <3.5 but not at sites with pH >4.5, regardless of geographic position and vegetation. These OTUs could be related to the Nitrosotalea group 1.1 and the Nitrososphaera subcluster 7.2, respectively, and showed significant similarities to OTUs described from other acidic environments. Conversely, none of the major OTUs typical of sites with a soil pH >4.6 could be found in the ultra- and extreme acidic soils. Based on a comparison with the amoA gene sequence data from a previous study performed on agricultural soils, we could clearly show that the development of AOA communities in soils with ultra-acidic pH (<3.5) is mainly triggered by soil pH and is not influenced significantly by the type of land use, the soil type, or the geographic position of the site, which was observed for sites with acido-neutral soil pH.
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http://dx.doi.org/10.1007/s00248-014-0548-5DOI Listing
May 2015

Temperature sensitivity of soil respiration rates enhanced by microbial community response.

Nature 2014 Sep;513(7516):81-4

Geography, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4RJ, UK.

Soils store about four times as much carbon as plant biomass, and soil microbial respiration releases about 60 petagrams of carbon per year to the atmosphere as carbon dioxide. Short-term experiments have shown that soil microbial respiration increases exponentially with temperature. This information has been incorporated into soil carbon and Earth-system models, which suggest that warming-induced increases in carbon dioxide release from soils represent an important positive feedback loop that could influence twenty-first-century climate change. The magnitude of this feedback remains uncertain, however, not least because the response of soil microbial communities to changing temperatures has the potential to either decrease or increase warming-induced carbon losses substantially. Here we collect soils from different ecosystems along a climate gradient from the Arctic to the Amazon and investigate how microbial community-level responses control the temperature sensitivity of soil respiration. We find that the microbial community-level response more often enhances than reduces the mid- to long-term (90 days) temperature sensitivity of respiration. Furthermore, the strongest enhancing responses were observed in soils with high carbon-to-nitrogen ratios and in soils from cold climatic regions. After 90 days, microbial community responses increased the temperature sensitivity of respiration in high-latitude soils by a factor of 1.4 compared to the instantaneous temperature response. This suggests that the substantial carbon stores in Arctic and boreal soils could be more vulnerable to climate warming than currently predicted.
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http://dx.doi.org/10.1038/nature13604DOI Listing
September 2014