Linking crenarchaeal activity to global nitrogen cycling in soil
Lead Research Organisation:
University of Aberdeen
Department Name: Plant and Soil Science
Abstract
Microbes are key players in the turnover and transformation of nutrients, including carbon and nitrogen, in the environment. However, our understanding of these microbially mediated processes is severely hampered by our inability to culture the vast majority of microbes in the laboratory. The recent application of molecular techniques has circumvented these limitations, because they bypass the need for laboratory cultivation, and they have revolutionised our view of microbial diversity by enabling us to examine the 'uncultured majority'. Many groups of microbes have been discovered which have no representative in laboratory culture, and therefore no known ecosystem function, but which are abundant in natural environments. An important example is the mesophilic crenarchaea, which constitute approximately 6% of all prokaryotes in terrestrial and marine environments. Molecular techniques recently predicted that crenarchaea may have a central role in the oxidation of ammonia in the environment, a key step in the global nitrogen cycle, and an ammonia oxidising crenarchaea has since been isolated in the laboratory. As crenarchaea are a much more abundant than previously characterised ammonia-oxidising bacteria, they may represent the most important ammonia-oxidising organisms in the biosphere. This research proposal aims to quantify their role in ammonia oxidation in soil, to compare the impact of environmental factors on their activity and that of 'traditional' ammonia-oxidising organisms and to determine whether they possess distinct ecophysiological characteristics and ecology.
Organisations
People |
ORCID iD |
| Graeme Nicol (Principal Investigator) |
Publications
Bartossek R
(2010)
Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context.
in Environmental microbiology
Coci M
(2010)
Quantitative assessment of ammonia-oxidizing bacterial communities in the epiphyton of submerged macrophytes in shallow lakes.
in Applied and environmental microbiology
Gubry-Rangin C
(2010)
Archaea rather than bacteria control nitrification in two agricultural acidic soils.
in FEMS microbiology ecology
Gubry-Rangin C
(2011)
Niche specialization of terrestrial archaeal ammonia oxidizers.
in Proceedings of the National Academy of Sciences of the United States of America
Höfferle Š
(2010)
Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile.
in FEMS microbiology ecology
Le Roux X
(2008)
Effects of aboveground grazing on coupling among nitrifier activity, abundance and community structure.
in The ISME journal
Lehtovirta LE
(2009)
Soil pH regulates the abundance and diversity of Group 1.1c Crenarchaeota.
in FEMS microbiology ecology
Lehtovirta-Morley LE
(2011)
Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil.
in Proceedings of the National Academy of Sciences of the United States of America
Levicnik-Höfferle S
(2012)
Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen.
in FEMS microbiology ecology
Merbt SN
(2012)
Differential photoinhibition of bacterial and archaeal ammonia oxidation.
in FEMS microbiology letters
Nicol GW
(2008)
The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria.
in Environmental microbiology
Nicol GW
(2007)
Afforestation of moorland leads to changes in crenarchaeal community structure.
in FEMS microbiology ecology
Nicol GW
(2011)
Strategies to determine diversity, growth, and activity of ammonia-oxidizing archaea in soil.
in Methods in enzymology
Offre P
(2011)
Community profiling and quantification of putative autotrophic thaumarchaeal communities in environmental samples.
in Environmental microbiology reports
Offre P
(2009)
Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene.
in FEMS microbiology ecology
Peterse F
(2010)
Influence of soil pH on the abundance and distribution of core and intact polar lipid-derived branched GDGTs in soil
in Organic Geochemistry
Prosser JI
(2012)
Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation.
in Trends in microbiology
Prosser JI
(2008)
Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment.
in Environmental microbiology
Schleper C
(2010)
Ammonia-oxidising archaea--physiology, ecology and evolution.
in Advances in microbial physiology
Stopnisek N
(2010)
Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment.
in Applied and environmental microbiology
Tourna M
(2008)
Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms.
in Environmental microbiology
Verhamme DT
(2011)
Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms.
in The ISME journal
Yao H
(2011)
Links between Ammonia Oxidizer Community Structure, Abundance, and Nitrification Potential in Acidic Soils
in Applied and Environmental Microbiology
Zhang LM
(2010)
Autotrophic ammonia oxidation by soil thaumarchaea.
in Proceedings of the National Academy of Sciences of the United States of America
| Description | The overall aim of this project was to understand the importance of ammonia oxidising archaea (AOA), belonging to the evolutionary lineage crenarchaea, to nitrogen cycling processes in soils. The nitrogen cycle is an essential global biogeochemical process, and the oxidation of ammonia to nitrite is a central, critical step. Not only is this a required natural process, but it is primarily responsible for the loss of nitrogen-based fertilisers. The organisms thought responsible for these processes were ammonia oxidising bacteria (AOB) and have been cultivated from soil for over 120 years. However, only 6 years ago, organisms belonging to a completely separate evolutionary lineage, the archaea, were also found to perform this process. The research programme therefore aimed to determine the importance of AOA by testing the central hypothesis that soil crenarchaea have the central role in terrestrial nitrogen cycling and had four objectives in attempting to test this hypothesis. All objectives of this research programme were met and resulted in over 20 research publications (12 first/last author) and included three papers published in PNAS. 1.1 To determine in situ growth dynamics, functional activity and nitrification kinetics of AOA and AOB in soil using differential inhibitors, quantitative RT-PCR of amo mRNA and stable isotope probing. The relative importance of AOA and AOB was determined. Using the range of experimental approaches listed, this research conclusively showed that AOA and AOB have very distinct ecological niches, and crucially, have different roles in nitrogen fertiliser transformation (e.g. Verhamme et al, 2010, ISME J; Zhang et al., 2010, PNAS). Specifically, the crucial is the source of ammonia that fuels the activity of each group. AOA are primarily dependent on ammonia derived from mineralised 'natural' organic nitrogen and to a large extent ignore applied mineral ammonia. AOB on the other hand are primarily dependent on mineral ammonia, and it is therefore they, and not AOA, who are primarily responsible for inorganic nitrogen fertiliser loss. 1.2 To compare physiological characteristics of cultivated soil AOA and AOB. Not only do AOA and AOB have distinct ecological niches in soil, but they also have contrasting physiologies. AOA are adapted to very low concentrations of ammonia with the key enzymes of AOA possessing much higher affinities for ammonia. Crucially, certain lineages of AOA, and not AOB, are acidophiles, and it is the activities of these organisms that solved the long-standing paradox of acidophilic nitrification soils (Gubry-Rangin et al., 2011, PNAS; Lehtovirta-Morley et al., 2011, PNAS). 2. To establish links between functional gene diversity and physiological diversity of AOA and AOB, and nitrification kinetics across characterised ecological gradients Of all the properties examined across ecological gradients, soil pH was demonstrated to be the primary driver for the distribution and evolution of different AOA lineages (e.g. Nicol et al., 2008, Environ Microbiol; Gubry-Rangin et al., 2010, FEMS Microbiol Ecol; Gubry-Rangin et al., 2011, PNAS). 3. To determine whether Group 1.1c and 1.3 soil crenarchaea have phylogentically and physiologically distinct monooxygenase enzymes, using novel molecular technologies. These lineages to not appear to possess AMO, and are therefore not ammonia oxidisers (e.g. Stopnisek et al., 2010, Appl Environ Microbiol). 4. To determine the functional diversity of crenarchaeal populations with respect to nitrogen and carbon biogeochemical cycling by measuring incorporation of 13C from a range of substrates. Crenarchaeal AOA populations appear to be restraicted to using ammonia as an energy source, and other compounds (e.g. methane) cannot be used (Lehtovirta et al., submitted, ISME J). |
| Exploitation Route | This research programme (finished in 2011) established that ammonia oxidising archaea play a critical role in nitrification processes in soils globally. While the principal long term legacy of the work was to direct further focused research into archaeal ammonia oxidation (not only my group but other scientists attempting to understanding the major contributors to nitrogen cycling processes), the work is of direct relevance to those concerned with inorganic nitrogen pollution (nitrate pollution from fertilizer use, eutrophication, atmospheric ammonium deposition on natural habitats, declining soil health) including regulatory and legislative organisations. |
| Sectors | Agriculture, Food and Drink,Environment |
| Description | At this moment in time, this research is largely of academic benefit. The research will add significantly to basic science understanding of how ammonia is transformed in the soil environment (by identifying the key organisms responsible), and will be of interest to governmental environmental agencies concerned with pollution associated with nitrogen fertiliser loss and atmospheric pollution associated with ammonia oxidation in soil. |
| First Year Of Impact | 2014 |
| Sector | Agriculture, Food and Drink,Environment |
| Impact Types | Policy & public services |