ERC Starting Grant 2020 - CoEVOLVE

Microbes significantly influence element cycling on Earth, directly controlling a large portion of biogeochemical cycles [1,2]. Most of the key biogeochemical reactions are carried out by a small set of microbially encoded proteins, all of which contain a redox-sensitive transition metal as the core catalytic center [3,4]. To be able to access different substrates, microbes precisely tune the midpoint electric potential (Eh’) of their redox proteins, a task carried out by selecting for a wide variety of metal centers and altering their position within the protein. Elements used in the catalytic centers of redox enzymes include, among others, transition metals such as Fe, Mo, W, Zn, Cu, V, Mn, Ni and Co and non-metals like S and Mg. The availability of biologically critical dissolved metals has changed over the course of Earth’s history as a result of changing redox conditions, particularly global oxygenation [5,6]. Changing metal availability has likely led to the expanded biological utilization of new transition metals [7,8], and directly influenced biological innovation and the evolution of new metabolic pathways [2–4,9]. This geochemical evolution allowed biology to access a larger number of redox couples, evolutionary tuning its machinery to use more oxidized compounds as they became available during planetary evolution [3–5,10].

How has changing metal availability influenced metabolism evolution and the emergence of biogeochemical cycles? The project will look at how the diversity and distribution of trace elements can influence the diversity and evolution of biogeochemically-relevant oxidoreductase proteins. Logo credit: Patricia Barcala Domínguez

The majority of evidence supporting a strong role of metals in controlling metabolic diversity comes from work carried out in the field of anaerobic bioreactors and biogas production, where the selective addition of Ni, Co, W and Se in different ratios controls factors such as methane/sulfide yield ratio, the total yield of the digester, as well as the diversity of the microbial consortia in the bioreactor [11,12]. Similarly, metals like Ni and Co have been shown to be key factors controlling the activity of methanogens [13–15], and Fe is a known key micronutrient controlling the diversity and productivity of phytoplankton in the oceans [16]. Despite early empirical evidence that metal availability may control microbial functional diversity in natural and artificial ecosystems, very little work has been done to understand this process. Understanding the roles of trace metal environmental distribution and availability in influencing microbial functional diversity holds the key to understanding the co-evolution of life and our planet, unlocking numerous important discoveries at the core of diverse fields like earth sciences, astrobiology, microbial ecology, bioremediation, and biotechnology.

The ERC Starting Grant project COEVOLVE will elucidate the effect of transition metal availability on microbial functional diversity through deep time, paving the way for unique discoveries in Earth system sciences and microbial ecology and evolution. The structure of COEVOLVE has been designed to balance risks/gains of such an ambitious project.

The objectives of the COEVOLVE project are: O1) To investigate the relationship between the availability of trace metals and microbial functional diversity in extant ecosystems and organisms. This objective will be addressed using a combination of fieldwork, laboratory and computational approaches, and represents the core of the project. Tackling O1 will contribute to a new understanding of the role of metals in controlling microbial diversity in diverse hydrothermal settings, with potential broader impacts in very different fields, ranging from Earth and planetary sciences to bioremediation and biotechnology. O2) To link metabolic diversity and metal availability to the different geochemical, mineralogical and geological settings under investigation. This objective will leverage the large amount of publicly available metagenomes, linking them to the available geochemical and mineralogical data. Tackling O2 will provide unprecedented details regarding the relationship between microbial functional diversity and large-scale geological processes, with far-reaching impacts. For example, it will identify potential microbial proxies to track small-scale variation in geologic processes, such as the surface expression of mantle fO2 heterogeneities, or the distribution of economically relevant ore deposits. O3) To link metabolic diversity and dependence on metal availability to the emergence and evolution of metabolic innovation. This objective will leverage the large amount of publicly available microbial genome data, linking functional profiles to their growth media composition. O3 will have far-reaching implications for how we approach the discovery and isolation of new microbial strains, and potentially change our understanding of the emergence and evolution of specific metabolisms. O4) To determine the timing of major steps in metabolic evolution and link them to geochemical proxies of planetary surface redox change. We expect that tackling O4 will potentially unveil new co-evolutionary relationship between life and our planet, leading to a deeper understanding of the role that the interplay between geology and biology has in influencing Earth’s evolution, long-term climate stability, and habitability.

Open Science Principles

We will strive to follow the European Open Science principle as outlined here. This will include do our best to make all the data, data product, code, software and publications publicly available as soon as possible, in a format that will encourage reuse and collaboration. We will also work actively to promote equality, inclusivity and intellectual and academic freedom. If you want to read more about Open Science go the the Open Science Training Handbook on GitHub.

References

  1. Falkowski, P. G., Fenchel, T. & Delong, E. F. The Microbial Engines That Drive Earth’s Biogeochemical Cycles. Science 320, 1034–1039 (2008).
  2. Jelen, B. I., Giovannelli, D. & Falkowski, P. G. The Role of Microbial Electron Transfer in the Coevolution of the Biosphere and Geosphere. Annu. Rev. Microbiol. 70, 45–62 (2016).
  3. Moore, E. K., Jelen, B. I., Giovannelli, D., Raanan, H. & Falkowski, P. G. Metal availability and the expanding network of microbial metabolisms in the Archaean eon. Nat. Geosci. 10, 629–636 (2017).
  4. Robbins, L. J. et al. Trace elements at the intersection of marine biological and geochemical evolution. Earth-Sci. Rev. 163, 323–348 (2016).
  5. Anbar, A. D. Elements and Evolution. Science 322, 1481–1483 (2008).
  6. Da Silva, J. F. & Williams, R. J. P. The biological chemistry of the elements: the inorganic chemistry of life. (Oxford University Press, 2001).
  7. Dupont, C. L., Butcher, A., Valas, R. E., Bourne, P. E. & Caetano-Anollés, G. History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc. Natl. Acad. Sci. 107, 10567–10572 (2010).
  8. Saito, M. A., Sigman, D. M. & Morel, F. M. M. The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean–Proterozoic boundary? Inorganica Chim. Acta 356, 308–318 (2003).
  9. Zerkle, A. L., House, C. H. & Brantley, S. L. Biogeochemical signatures through time as inferred from whole microbial genomes. Am. J. Sci. 305, 467–502 (2005).
  10. Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. The rise of oxygen in Earth/’s early ocean and atmosphere. Nature 506, 307–315 (2014).
  11. Feng, X. M., Karlsson, A., Svensson, B. H. & Bertilsson, S. Impact of trace element addition on biogas production from food industrial waste – linking process to microbial communities. FEMS Microbiol. Ecol. 74, 226–240 (2010).
  12. Carballa, M., Regueiro, L. & Lema, J. M. Microbial management of anaerobic digestion: exploiting the microbiome-functionality nexus. Curr. Opin. Biotechnol. 33, 103–111 (2015).
  13. Schönheit, P., Moll, J. & Thauer, R. K. Nickel, cobalt, and molybdenum requirement for growth of Methanobacterium thermoautotrophicum. Arch. Microbiol. 123, 105–107 (1979).
  14. Demirel, B. & Scherer, P. Trace element requirements of agricultural biogas digesters during biological conversion of renewable biomass to methane. Biomass Bioenergy 35, 992–998 (2011).
  15. Kida, K. et al. Influence of Ni2+ and Co2+ on methanogenic activity and the amounts of coenzymes involved in methanogenesis. J. Biosci. Bioeng. 91, 590–595 (2001).
  16. Tagliabue, A. et al. The integral role of iron in ocean biogeochemistry. Nature 543, 51–59 (2017).