Evolutionary adaptation in Archaea
Lead Research Organisation:
University of Aberdeen
Department Name: Inst of Biological and Environmental Sci
Abstract
Biological diversity is vast in the majority of natural environments and, globally, is essential for the maintenance of ecosystem function. High diversity is believed to have arisen from adaptation to the myriad of structured environmental and biotic niches and specialisation to alternative resources. Diversity reflects the interaction between evolution and ecology, as organisms adapt to environmental change to create biological diversity, which, in turn, is selected for maintenance of ecosystem function. Therefore, adaptation is an evolutionary process of crucial importance to life on earth.
Microorganisms (comprising two of the three domains of life, namely the bacteria and the archaea) are the most abundant organisms on earth and three mechanisms are seen as important in the process of microbial adaptation: recombination, allowing lateral exchange (gain or loss) of genetic material; positive selection, favouring the increase of advantageous mutations; and differential expression of the genes. Microorganisms are useful organisms to study adaptation to the environment due to their short generation time, their small genome and their small size.
The thaumarchaea represent a significant proportion of prokaryotic abundance in mesophilic environments and play an important role in the global biogeochemical cycling of nitrogen. They are responsible for nitrate leaching and nitrous oxide production, participating in both greenhouse gas production and water/soil pollution, and thus play an important ecological role. Of all the abiotic factors investigated in terrestrial environments, pH appears to have the strongest influence on thaumarchaeal community composition at three spatial scales (world-wide, UK-wide and on a agricultural pH plot) in different ecosystems. Therefore, thaumarchaea represent a good model for studying adaptation to the environment and two main approaches will be targeted in this proposal.
First, the limited number of cultivated thaumarchaea has seriously limited knowledge on these organisms, but development of new technologies such as single-cell sequencing will enable comparison of their genomes using an approach that does not require laboratory cultivation. Genome sequencing of cells obtained from soils with different pH will be developed and used to compare their levels of recombination and selection, in order to understand why and how thaumarchaea are influenced by pH.
Second, an experimental evolution approach will be adopted to drive evolution of the thaumarchaea in the laboratory under different tightly controlled pH pressure in order to analyse their adaptation. Thaumarchaea will be compared after growth for 2.5, to assess their evolutionary adaptation over time and as a function of different pH regimes. This will provides answers to key questions on the speed of evolution, on their specialization and on the genomic basis of adaptation.
This project will be the first to analyse adaptation of terrestrial thaumarchaea by recombination and selection and will also be the first long-term evolution experiment on archaea. It will therefore impact on our understanding of the links between ecology and evolution of a microbial group important in agriculture, water and environmental pollution, and will also inform ecological and evolutionary studies of other important environmental microorganisms.
Microorganisms (comprising two of the three domains of life, namely the bacteria and the archaea) are the most abundant organisms on earth and three mechanisms are seen as important in the process of microbial adaptation: recombination, allowing lateral exchange (gain or loss) of genetic material; positive selection, favouring the increase of advantageous mutations; and differential expression of the genes. Microorganisms are useful organisms to study adaptation to the environment due to their short generation time, their small genome and their small size.
The thaumarchaea represent a significant proportion of prokaryotic abundance in mesophilic environments and play an important role in the global biogeochemical cycling of nitrogen. They are responsible for nitrate leaching and nitrous oxide production, participating in both greenhouse gas production and water/soil pollution, and thus play an important ecological role. Of all the abiotic factors investigated in terrestrial environments, pH appears to have the strongest influence on thaumarchaeal community composition at three spatial scales (world-wide, UK-wide and on a agricultural pH plot) in different ecosystems. Therefore, thaumarchaea represent a good model for studying adaptation to the environment and two main approaches will be targeted in this proposal.
First, the limited number of cultivated thaumarchaea has seriously limited knowledge on these organisms, but development of new technologies such as single-cell sequencing will enable comparison of their genomes using an approach that does not require laboratory cultivation. Genome sequencing of cells obtained from soils with different pH will be developed and used to compare their levels of recombination and selection, in order to understand why and how thaumarchaea are influenced by pH.
Second, an experimental evolution approach will be adopted to drive evolution of the thaumarchaea in the laboratory under different tightly controlled pH pressure in order to analyse their adaptation. Thaumarchaea will be compared after growth for 2.5, to assess their evolutionary adaptation over time and as a function of different pH regimes. This will provides answers to key questions on the speed of evolution, on their specialization and on the genomic basis of adaptation.
This project will be the first to analyse adaptation of terrestrial thaumarchaea by recombination and selection and will also be the first long-term evolution experiment on archaea. It will therefore impact on our understanding of the links between ecology and evolution of a microbial group important in agriculture, water and environmental pollution, and will also inform ecological and evolutionary studies of other important environmental microorganisms.
Planned Impact
Who will benefit from this research?
The aim of the proposed research is to determine relationships between genome structure, evolutionary forces and pH-driven specialisation in an ecologically important group of organisms, the thaumarchaea. In addition to the immediate archaeal research community, this research will benefit those generally interested in population genetics, ecology and evolution of other microorganisms, including those performing important ecosystem services.
A major element of the proposed programme is the development of single cell sequencing technology and whole genome application. The development of methodologies will benefit those who wish to exploit this technology for other organisms, be it for academic research, or retrieval of novel genomic content for discovery of novel gene products for industrial use.
While there is now clear evidence that terrestrial thaumarchaea are important contributors to ammonia oxidation in natural soils, we are unclear of their contributions to other environmentally important processes such as nitrous oxide production. It is likely that this research will provide novel, fundamental insights into the contribution of thaumarchaea to other aspects of carbon and nitrogen cycling and a greater understanding of the mechanisms determining ammonia oxidation, and nitrification rates, in agricultural soils with different pH. It therefore has potential consequences for increasing nitrogen fertiliser utilisation and reduction in atmospheric pollution by nitrous oxide. Beneficiaries therefore include those agencies concerned with legislation, nitrous oxide emissions and climate change (e.g. DEFRA, SEPA, Environment Agency), farmers and the fertiliser industry.
How will they benefit from this research?
This research will benefit those interested in population genetics, ecology and evolution. Mechanisms of evolution and adaptation of thaumarchaea will advance broader aspects of evolutionary theory, by comparing mechanisms in thaumarchaea with those in other archaea, bacteria and eukaryotes.
The programme of research will develop single cell sequencing technology and whole genome application. As this technology is not yet routine, the development of these methodologies will benefit other researchers who wish to utilise this technology, producing established procedures and methodologies, allowing analysis of single microbial cells in other areas of research and industry.
The work will also be of direct relevance to those concerned with inorganic nitrogen pollution of natural ecosystems (nitrogen deposition and acidification) as well as pollution derived from managed soils (nitrous oxide emissions, eutrophication, nitrate pollution of water courses). Therefore, from a regulatory and legislative perspective, these results could guide future policy decisions in land and fertilizer management.
The aim of the proposed research is to determine relationships between genome structure, evolutionary forces and pH-driven specialisation in an ecologically important group of organisms, the thaumarchaea. In addition to the immediate archaeal research community, this research will benefit those generally interested in population genetics, ecology and evolution of other microorganisms, including those performing important ecosystem services.
A major element of the proposed programme is the development of single cell sequencing technology and whole genome application. The development of methodologies will benefit those who wish to exploit this technology for other organisms, be it for academic research, or retrieval of novel genomic content for discovery of novel gene products for industrial use.
While there is now clear evidence that terrestrial thaumarchaea are important contributors to ammonia oxidation in natural soils, we are unclear of their contributions to other environmentally important processes such as nitrous oxide production. It is likely that this research will provide novel, fundamental insights into the contribution of thaumarchaea to other aspects of carbon and nitrogen cycling and a greater understanding of the mechanisms determining ammonia oxidation, and nitrification rates, in agricultural soils with different pH. It therefore has potential consequences for increasing nitrogen fertiliser utilisation and reduction in atmospheric pollution by nitrous oxide. Beneficiaries therefore include those agencies concerned with legislation, nitrous oxide emissions and climate change (e.g. DEFRA, SEPA, Environment Agency), farmers and the fertiliser industry.
How will they benefit from this research?
This research will benefit those interested in population genetics, ecology and evolution. Mechanisms of evolution and adaptation of thaumarchaea will advance broader aspects of evolutionary theory, by comparing mechanisms in thaumarchaea with those in other archaea, bacteria and eukaryotes.
The programme of research will develop single cell sequencing technology and whole genome application. As this technology is not yet routine, the development of these methodologies will benefit other researchers who wish to utilise this technology, producing established procedures and methodologies, allowing analysis of single microbial cells in other areas of research and industry.
The work will also be of direct relevance to those concerned with inorganic nitrogen pollution of natural ecosystems (nitrogen deposition and acidification) as well as pollution derived from managed soils (nitrous oxide emissions, eutrophication, nitrate pollution of water courses). Therefore, from a regulatory and legislative perspective, these results could guide future policy decisions in land and fertilizer management.
People |
ORCID iD |
Cecile Gubry-Rangin (Principal Investigator / Fellow) |
Publications

Gubry-Rangin C
(2017)
Temperature responses of soil ammonia-oxidising archaea depend on pH
in Soil Biology and Biochemistry

Gubry-Rangin C
(2015)
Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota.
in Proceedings of the National Academy of Sciences of the United States of America

Herbold CW
(2017)
Ammonia-oxidising archaea living at low pH: Insights from comparative genomics.
in Environmental microbiology

Macqueen DJ
(2016)
Molecular adaptation of ammonia monooxygenase during independent pH specialization in Thaumarchaeota.
in Molecular ecology

Oton EV
(2016)
Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota.
in The ISME journal

Sinclair L
(2016)
Seqenv: linking sequences to environments through text mining.
in PeerJ

Sinclair L
(2016)
Seqenv: linking sequences to environments through text mining

Sinclair L
(2016)
Seqenv: linking sequences to environments through text mining

Weber EB
(2015)
Ammonia oxidation is not required for growth of Group 1.1c soil Thaumarchaeota.
in FEMS microbiology ecology
Description | My key finding has been that pH has influenced their pattern of diversification over hundreds of millions of years. This research provided evidence for a paradigm shift in our understanding of the dynamics of microbial diversification, which contrast significantly with those in eukaryotes, as Thaumarchaeota maintain a high rate of diversification after the initial radiation (whereas the rate in eukaryotes usually decreases). My second greatest achievement has been to develop a technology to obtain single-cell genomes for uncultivated non-abundant microbes from soil. |
Exploitation Route | By analysing pattern of diversiifcation in other microbes and by applying the single-cell genomic methodology to other non-abundant uncultivated microbes. |
Sectors | Agriculture Food and Drink Education Environment |
Description | Interest of the public for the single-cell scientific movie |
First Year Of Impact | 2015 |
Sector | Education |
Impact Types | Societal |
Description | NERC grant |
Amount | £649,074 (GBP) |
Funding ID | NE/R001529/1 |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 11/2017 |
End | 05/2021 |
Description | Royal Society Enhancement grant |
Amount | £108,742 (GBP) |
Funding ID | RGF\EA\180253 |
Organisation | The Royal Society |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 08/2018 |
End | 01/2022 |
Description | Royal Society University Research Fellowship |
Amount | £513,586 (GBP) |
Organisation | The Royal Society |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 09/2016 |
End | 09/2021 |
Description | The Royal Society grant |
Amount | £174,408 (GBP) |
Organisation | The Royal Society |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 08/2017 |
End | 08/2021 |
Description | University of Aberdeen Postgraduate Scholarship |
Amount | £70,000 (GBP) |
Organisation | University of Aberdeen |
Sector | Academic/University |
Country | United Kingdom |
Start | 08/2013 |
End | 08/2016 |
Description | University of Aberdeen studentship |
Amount | £144,345 (GBP) |
Organisation | University of Aberdeen |
Sector | Academic/University |
Country | United Kingdom |
Start | 11/2017 |
End | 10/2021 |
Title | MDA reaction |
Description | This method allows the amplification of very little amount of DNA (for example from single-cell microbial genome) in order to sequence the genome of the organism of interest. |
Type Of Material | Improvements to research infrastructure |
Provided To Others? | No |
Impact | This method will result in several high impact papers in the next few years. The first paper has been submitted early March 2016. |
Title | Single-cell sorting |
Description | This technique allows the sorting of individual microbial cells in single-well plates. This sorting is based on the size of the cell and on the fluorescence of the probe attached. This method has been facilitated by the use of the cytometry facility platform in Aberdeen University. |
Type Of Material | Improvements to research infrastructure |
Provided To Others? | No |
Impact | This method will result in several high impact papers in the next few years. The first paper has been submitted in March 2016 for publication. |
Title | archaeal FISH |
Description | This technique has been succesfully adapted to our samples by my phD student.The archaeal-FISh is used to detect and to pseudo-quantify archaea compare to bacteria in a culture or in cells exracted from soil. |
Type Of Material | Technology assay or reagent |
Year Produced | 2014 |
Provided To Others? | Yes |
Impact | This tool has helped for the specific sorting of single-cell and will also be used for monitoring cultures (preventing DNA extraction and qPCR ) |
Title | Data from: Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota |
Description | 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. |
Type Of Material | Database/Collection of data |
Year Produced | 2016 |
Provided To Others? | Yes |
URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.0nv00 |
Description | Comparative genomics |
Organisation | University of Vienna |
Department | Division of Microbial Ecology |
Country | Austria |
Sector | Academic/University |
PI Contribution | Genomic contribution; leading the collaboration on ideas. |
Collaborator Contribution | Genomic contribution; contributing on phylogenomic and lateral gene transfer analyses |
Impact | Manuscript submitted and in revision. |
Start Year | 2015 |
Description | Public event |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Public/other audiences |
Results and Impact | Workshop on single-cell genomics using hands-on activities. Workshop rated as excellent by >90% of participants. |
Year(s) Of Engagement Activity | 2016 |
Description | Video |
Form Of Engagement Activity | A broadcast e.g. TV/radio/film/podcast (other than news/press) |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Media (as a channel to the public) |
Results and Impact | I have been involved in a video describing my research and this has been disseminated via several websites. I recived a good feedback and several people have been impressed by the science. |
Year(s) Of Engagement Activity | 2015 |
URL | https://youtu.be/U7ThQurkE1c |