TACK and Lokiarchaeota Evolution

Dissecting the Ecology and Evolution of Archaea to Elucidate the Prokaryote to Eukaryote Transition

The emergence of complex eukaryotic life forms on Earth from prokaryotic cells is one of the most fundamental questions in biology and also one of the least understood transitions in evolution. Phylogenomic studies recently indicated that the eukaryotic line of descent arose from within the TACK+L superphylum of Archaea.

This project addresses the systematic analysis of two newly discovered, but largely uncharacterized lineages of Archaea from this superphylum that mark crucial evolutionary transitions.

Thaumarchaeota harbor unique 'eukaryotic' features and represent the sole group of Archaea that has successfully radiated into virtually any moderate habitat on Earth. The Lokiarchaeota lineage found recently in deep marine sediments forms a direct sister group of Eukaryotes and exhibits an unprecedented array of genes that might have been instrumental for the ancestor of eukaryotes to develop its cellular and genomic complexity. Obviously, the molecular and biochemical investigation of both groups is timely and important, yet, it requires easy access and cultivation.

We have now discovered Lokiarchaeota in local, accessible environments and were able to successfully cultivate thermophilic Thaumarchaeota. In this project, we will characterize the metabolic and structural traits of these two archaeal lineages and reconstruct their evolutionary ancestry in the context of the TACK+L superphylum.
Beside the use of cutting edge techniques for cultivation, metagenomics and stable-isotope-based imaging, a novel method will be developed for in situ metatranscriptomic analyses of archaea.

This project will give fundamental insights into the ecological success of Archaea in commonplace environments and into the biology of the closest living prokaryotic relatives of Eukaryotes. Reconstructing the ancestral gene repertoire and biological features of lineages of the TACK+L superphylum will help resolve the enigma of the emergence of eukaryotes.

Duration: 01.08.2016-31.07.2022

Funding agency: ERC Advanced Grant

Project leader: Prof. Christa Schleper

Participants: Christa Schleper, Ricardo Alves, Thomas Angeler,  Alexandre Bagnoud, Thiago Rodrigues de Oliveira, Jasmin de Silva, Karin Hager, Angus Hilts, Logan Hodgskiss, Nathalia Jandl, Jessica Kozlowski, Lokeshwaran Manoharan, Mohammad Anas Mardini, Michael Melcher, Laureen Mertens, Marina Monserrat i Diez, Mahbod Mousavian, Thomas Pribasnig,  Ruth-Sophie Taubner, Rafael Isaac Ponce Toledo, Mary Ward, Erika Wimmer, Ülkü Yüksel, Isabelle Anna Zink.

Peer-reviewed publications related to or funded through this project

  • Zink, I. A., Wimmer, E., & Schleper, C. (2020). Heavily Armed Ancestors: CRISPR Immunity and Applications in Archaea with a Comparative Analysis of CRISPR Types in Sulfolobales. Biomolecules, 10(11), 1523. Doi: 10.3390/biom10111523
  • Abby, S. S., Kerou, M., & Schleper, C. (2020). Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments. Mbio, 11(5). Doi: 10.1128/mbio.02371-20
  • Zink, I. A., Fouqueau, T., Tarrason Risa, G., Werner, F., Baum, B., Bläsi, U., & Schleper, C. (2020). Comparative CRISPR type III-based knockdown of essential genes in hyperthermophilic Sulfolobales and the evasion of lethal gene silencing. RNA biology, 1-14. Doi: 10.1080/15476286.2020.1813411
  • Reyes, C., Hodgskiss, L. H., Kerou, M., Pribasnig, T., Abby, S. S., Bayer, B., Kraemer, S. M., Schleper, C. (2020). Genome wide transcriptomic analysis of the soil ammonia oxidizing archaeon Nitrososphaera viennensis upon exposure to copper limitation. The ISME Journal, 14(11), 2659-2674. Doi: 10.1038/s41396-020- 0715-2
  • Zink, I. A., Pfeifer, K., Wimmer, E., Sleytr, U. B., Schuster, B., & Schleper, C. (2019). CRISPR-mediated gene silencing reveals involvement of the archaeal S-layer in cell division and virus infection. Nature communications, 10(1), 1-14. Doi: 10.1038/s41467-019-12745-x
  • Manoharan, L., Kozlowski, J. A., Murdoch, R. W., Löffler, F. E., Sousa, F. L., & Schleper, C. (2019). Metagenomes from coastal marine sediments give insights into the ecological role and cellular features of Loki-and Thorarchaeota. Mbio, 10(5). Doi: 10.1128/mbio.02039-19
  • Alves, R. J. E., Kerou, M., Zappe, A., Bittner, R., Abby, S. S., Schmidt, H. A., Pfeifer, K. & Schleper, C. (2019). Ammonia oxidation by the arctic terrestrial thaumarchaeote Candidatus Nitrosocosmicus arcticus is stimulated by increasing temperatures. Frontiers in microbiology, 10, 1571. Doi: 10.3389/fmicb.2019.01571
  • Kozlowski, J. A., Johnson, M. E., Ledesma-Vázquez, J., Birgel, D., Peckmann, J., & Schleper, C. (2018). Microbial diversity of a closed salt lagoon in the Puertecitos area, Upper Gulf of California. Ciencias Marinas, 44(2), 71-90. Doi: 10.7773/cm.v 44i2.2825
  • Abby, S. S., Melcher, M., Kerou, M., Krupovic, M., Stieglmeier, M., Rossel, C., Pfeifer, K., & Schleper, C. (2018). Candidatus Nitrosocaldus cavascurensis, an ammonia oxidizing, extremely thermophilic archaeon with a highly mobile genome. Frontiers in microbiology, 9, 28. Doi: 10.3389/fmicb.2018.00028
  • Alves, R. J. E., Minh, B. Q., Urich, T., von Haeseler, A., & Schleper, C. (2018). Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nature communications, 9(1), 1-17. Doi: 10.1038/s41467-018-03861-1
  • Elling, F. J., Könneke, M., Nicol, G. W., Stieglmeier, M., Bayer, B., Spieck, E., de la Torre, J., Becker, K. W., Thomm, M., Posser, J. I., Herndl, G. J., Schleper, C., & Hinrichs, K. U. (2017). Chemotaxonomic characterisation of the thaumarchaeal lipidome. Environmental Microbiology, 19(7), 2681-2700. Doi: 10.1111/1462-2920.13759
  • Kerou, M., Offre, P., Valledor, L., Abby, S. S., Melcher, M., Nagler, M., Weckwerth, W., Schleper, C. (2016). Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers. Proceedings of the National Academy of Sciences, 113(49), E7937-E7946. Doi: 10.1073/pnas.1601212113