Soil ammonia oxidisers: an embarrassment of richness?
Lead Research Organisation:
University of Aberdeen
Department Name: Inst of Biological and Environmental Sci
Abstract
Microorganisms are essential for the creation and maintenance of soil fertility and for many other ecosystem functions, including nutrient cycling, bioremediation and plant growth. One particular group, the ammonia oxidisers, has a crucial role in the global cycling of nitrogen. These organisms perform the first, limiting step in nitrification, the sequential oxidation of ammonia to nitrite and nitrate. Nitrification can be beneficial to plants, but conversion of ammonia-based fertiliser often leads to nitrate pollution of groundwater sources of drinking water, substantial economic losses of fertiliser nitrogen and atmospheric pollution by the potent greenhouse gas nitrous oxide, a by-product of ammonia oxidation.
Microbial communities in soil, including ammonia oxidisers, are now characterised using molecular techniques, in which diagnostic genes are sequenced from DNA extracted from soil. This approach shows that microbial diversity in soil is extremely high, with tens of thousands of 'species' per gram of soil.
Studies of plant and animal communities indicate that ecosystem function (e.g. plant biomass) increases, up to a maximum, as the number of species increases. High diversity is believed to provide 'insurance' against the deleterious effects of environmental change by increasing the diversity of species able to perform the same function. Despite the crucial importance of soil ammonia oxidisers, and other microorganisms, virtually nothing is known of the relationship between their diversity and the important soil functions that they perform. This is partly due to difficulties in determining their high diversity but also to a belief, with little supporting evidence, that this high diversity 'insures' ecosystem processes against microbial species loss.
In this project we will exploit the power of modern techniques for gene sequencing to estimate the number of different ammonia oxidisers in soil, i.e. their 'total' diversity. This will involve in-depth, high-throughput sequencing of the amoA gene, a diagnostic functional gene for ammonia oxidation, crucial for the first step in ammonia oxidation. We will then determine how many and which ammonia oxidisers can function at different soil pH values and temperatures. This will be achieved by changing either pH or temperature and then performing high-throughput sequencing to determine which amoA genes are up-regulated and which of the many ammonia oxidisers are growing under the changed conditions. We will also measure changes in nitrification rate. Experiments will be carried out in laboratory systems with different degrees of simplicity and reality: soil suspensions (the simplest), soil microcosms containing sieved soil and soil monoliths (minimal disturbance). These three systems will give us information on the degree to which heterogeneity in soil characteristics influences responses to environmental change. The sequence data that we obtain are also invaluable for analysis of evolutionary relationships within soil ammonia oxidisers. We will therefore use these data to investigate the roles of temperature and soil pH in determining rates of evolution.
This approach will enable us, for the first time, to assess which of the many organisms in highly diverse soil communities are active under different conditions, whether we should be concerned about diversity loss and whether diversity is important affects levels of fertiliser loss and pollution by ammonia oxidisers. The approach is potentially applicable to other microbial groups and ecosystem functions, and will therefore benefit other researchers, while information on evolution may be valuable in predicting future changes in diversity. The findings will therefore also be invaluable for those modelling the influence of environmental change, including climate change, on ecosystem processes, environmental agencies, agriculturalists and policy makers.
Microbial communities in soil, including ammonia oxidisers, are now characterised using molecular techniques, in which diagnostic genes are sequenced from DNA extracted from soil. This approach shows that microbial diversity in soil is extremely high, with tens of thousands of 'species' per gram of soil.
Studies of plant and animal communities indicate that ecosystem function (e.g. plant biomass) increases, up to a maximum, as the number of species increases. High diversity is believed to provide 'insurance' against the deleterious effects of environmental change by increasing the diversity of species able to perform the same function. Despite the crucial importance of soil ammonia oxidisers, and other microorganisms, virtually nothing is known of the relationship between their diversity and the important soil functions that they perform. This is partly due to difficulties in determining their high diversity but also to a belief, with little supporting evidence, that this high diversity 'insures' ecosystem processes against microbial species loss.
In this project we will exploit the power of modern techniques for gene sequencing to estimate the number of different ammonia oxidisers in soil, i.e. their 'total' diversity. This will involve in-depth, high-throughput sequencing of the amoA gene, a diagnostic functional gene for ammonia oxidation, crucial for the first step in ammonia oxidation. We will then determine how many and which ammonia oxidisers can function at different soil pH values and temperatures. This will be achieved by changing either pH or temperature and then performing high-throughput sequencing to determine which amoA genes are up-regulated and which of the many ammonia oxidisers are growing under the changed conditions. We will also measure changes in nitrification rate. Experiments will be carried out in laboratory systems with different degrees of simplicity and reality: soil suspensions (the simplest), soil microcosms containing sieved soil and soil monoliths (minimal disturbance). These three systems will give us information on the degree to which heterogeneity in soil characteristics influences responses to environmental change. The sequence data that we obtain are also invaluable for analysis of evolutionary relationships within soil ammonia oxidisers. We will therefore use these data to investigate the roles of temperature and soil pH in determining rates of evolution.
This approach will enable us, for the first time, to assess which of the many organisms in highly diverse soil communities are active under different conditions, whether we should be concerned about diversity loss and whether diversity is important affects levels of fertiliser loss and pollution by ammonia oxidisers. The approach is potentially applicable to other microbial groups and ecosystem functions, and will therefore benefit other researchers, while information on evolution may be valuable in predicting future changes in diversity. The findings will therefore also be invaluable for those modelling the influence of environmental change, including climate change, on ecosystem processes, environmental agencies, agriculturalists and policy makers.
Planned Impact
Until now, we have not been able to assess properly the significance of the extremely high diversity (richness) of bacterial and archaeal communities in natural communities, such as soil. We are therefore unable to determine whether these communities, and the important ecosystems that they perform, are sensitive to loss in richness, whether particular phylotypes should be conserved and whether keystone phylotypes exist. The main aim of the proposed research is therefore to determine the significance of prokaryote richness for global biogeochemical cycling and other ecosystem functions. It aims to achieve this by development of a new approach that will overcome conceptual and technical limitations that have prevented assessment of how many and which phylotypes are active in complex communities and how they respond to environmental perturbations. This approach will be developed for one particular functional group, soil ammonia oxidisers, which play an important role in the biogeochemical cycling of nitrogen, in plant nutrition and growth, in considerable economic losses of nitrogen-based fertiliser and in pollution of groundwaters and the atmosphere by nitrate and nitrous oxide, respectively.
Who will benefit from this research?
The research will benefit a wide range of scientists with fundamental interests in biodiversity-ecosystem function relationships, the consequences of richness loss and the impact of environmental change, including climate change, for microbial communities. This research will be also be of benefit to scientists with research focussing on the soil nitrogen cycle, inorganic nitrogen pollution of natural ecosystems, (nitrogen deposition and acidification) and pollution derived from managed soils (nitrous oxide emissions, eutrophication, nitrate pollution of water courses) from a regulatory and legislative perspective. The findings of this research will therefore have direct relevance to agencies such as DEFRA, SEPA, the Environment Agency, regional and national government and the EU.
How will they benefit from this research?
This work will allow the development of a new, broadly applicable technique for assessment of diversity-function relationships and will develop the concept of Within Functional Group Richness (WFGR). A greater understanding of the sensitivity of microbial communities to environmental change and consequent impacts on soil ecosystem function will be of value to agriculture, policy makers, environment agencies and modellers.
Who will benefit from this research?
The research will benefit a wide range of scientists with fundamental interests in biodiversity-ecosystem function relationships, the consequences of richness loss and the impact of environmental change, including climate change, for microbial communities. This research will be also be of benefit to scientists with research focussing on the soil nitrogen cycle, inorganic nitrogen pollution of natural ecosystems, (nitrogen deposition and acidification) and pollution derived from managed soils (nitrous oxide emissions, eutrophication, nitrate pollution of water courses) from a regulatory and legislative perspective. The findings of this research will therefore have direct relevance to agencies such as DEFRA, SEPA, the Environment Agency, regional and national government and the EU.
How will they benefit from this research?
This work will allow the development of a new, broadly applicable technique for assessment of diversity-function relationships and will develop the concept of Within Functional Group Richness (WFGR). A greater understanding of the sensitivity of microbial communities to environmental change and consequent impacts on soil ecosystem function will be of value to agriculture, policy makers, environment agencies and modellers.
Publications

Aigle A
(2020)
Experimental testing of hypotheses for temperature- and pH-based niche specialization of ammonia oxidizing archaea and bacteria.
in Environmental microbiology

Aigle A
(2019)
The application of high-throughput sequencing technology to analysis of amoA phylogeny and environmental niche specialisation of terrestrial bacterial ammonia-oxidisers.
in Environmental microbiome

Bello M
(2019)
Differential sensitivity of ammonia oxidising archaea and bacteria to matric and osmotic potential
in Soil Biology and Biochemistry

Bello M
(2021)
Preferential temperature and ammonia concentration for in-situ growth of Candidatus N?tr??????m??u? ammonia oxidising archaea
in Soil Biology and Biochemistry

Biggs-Weber E
(2020)
Oxygen preference of deeply-rooted mesophilic thaumarchaeota in forest soil
in Soil Biology and Biochemistry

Catão ECP
(2017)
Ammonia oxidisers in a non-nitrifying Brazilian savanna soil.
in FEMS microbiology ecology

De Vries F
(2021)
Glacier forelands reveal fundamental plant and microbial controls on short-term ecosystem nitrogen retention
in Journal of Ecology

Hink L
(2018)
The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions.
in The ISME journal
Description | Lecture entitled 'Soil ammonia oxidisers: microscopic instigators of a global Catch-22' on the molecular ecology of soil nitrifies and their role in fertiliser use efficiency and greenhouse gas production. Lecture launched an interdisciplinary research centre at the University of Vienna. |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Postgraduate students |
Results and Impact | Presentation of lecture entitled 'Soil ammonia oxidisers: microscopic instigators of a global Catch-22' on the molecular ecology of soil nitrifies and their role in fertiliser use efficiency and greenhouse gas production. Lecture launched the opening of an interdisciplinary research centre at the University of Vienna. |
Year(s) Of Engagement Activity | 2019 |
Description | Lecture on 'Niche specialisation in ammonia oxidisers: mechanisms, evidence, dreams and reality' at international conference on Soil Metagenomics. |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Presentation of lecture on 'Niche specialisation in ammonia oxidisers: mechanisms, evidence, dreams and reality' at international conference on Soil Metagenomics, Braunschweig. |
Year(s) Of Engagement Activity | 2019 |
Description | Presentation of Dean's Lecture, University of Melbourne |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Presentation of lecture - Harnessing soil microbiomics for agricultural production: transforming hype and hope into reality. Dean's Lecture, University of Melbourne, September |
Year(s) Of Engagement Activity | 2018 |
Description | Presentation of lecture - University of Queensland, Brisbane, September |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Presentation of lecture - Molecular analysis of ammonia oxidisers: enlightenment or entanglement. University of Queensland, Brisbane |
Year(s) Of Engagement Activity | 2018 |
Description | Presentation of lecture at Marine Biology Station, Piran, Slovenia |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Presentation of lecture - Niche specialisation in bacterial and archaeal ammonia oxidisers. Marine Biology Station, Piran, Slovenia |
Year(s) Of Engagement Activity | 2018 |
Description | Presentation of lecture in Tsukuba, Japan |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Policymakers/politicians |
Results and Impact | Presentation of lecture - Nitrifying archaea and their role in soil nitrification - Can we control them? BNI-Technology for Genetic-Mitigation and NUE improvement in Agriculture - Constraints and Opportunities, Tsukuba, Japan |
Year(s) Of Engagement Activity | 2018 |
Description | Presentation on Niche specialisation in complex communities in complex environments to InterActive Biomes Initiative, CSIRO. |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Presentation on Niche specialisation in complex communities in complex environments to InterActive Biomes Initiative, CSIRO. |
Year(s) Of Engagement Activity | 2022 |
Description | Presentation to International Forum on Advanced Environmental Sciences and Technology (iFAST). |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Presentation on Niche specialization in microbial communities: lessons learned from ammonia oxidizers to International Forum on Advanced Environmental Sciences and Technology (iFAST). |
Year(s) Of Engagement Activity | 2021 |
Description | Presentation to JAMS (Joint Academic Microbiology Seminars), Singapore and Sydney. |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Presentation on Scientific vs. technical challenges in microbial ecology: a question of approach to JAMS (Joint Academic Microbiology Seminars), Singapore and Sydney. |
Year(s) Of Engagement Activity | 2021 |
Description | West Riding Lecture, University of Sheffield |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Postgraduate students |
Results and Impact | Presentation of lecture - Molecular analysis of ammonia oxidisers: enlightenment or entanglement. West Riding Lecture, University of Sheffield, January |
Year(s) Of Engagement Activity | 2018 |