Evolutionary adaptation in Archaea

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.

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.