Abstract
Life is based on energy gained by electron-transfer processes; these processes rely on oxidoreductase enzymes, which often contain transition metals in their structures. The availability of different metals and substrates has changed over the course of Earth's history as a result of secular changes in redox conditions, particularly global oxygenation. New metabolic pathways using different transition metals co-evolved alongside changing redox conditions. Sulfur reduction, sulfate reduction, methanogenesis and anoxygenic photosynthesis appeared between about 3.8 and 3.4 billion years ago. The oxidoreductases responsible for these metabolisms incorporated metals that were readily available in Archaean oceans, chiefly iron and iron–sulfur clusters. Oxygenic photosynthesis appeared between 3.2 and 2.5 billion years ago, as did methane oxidation, nitrogen fixation, nitrification and denitrification. These metabolisms rely on an expanded range of transition metals presumably made available by the build-up of molecular oxygen in soil crusts and marine microbial mats. The appropriation of copper in enzymes before the Great Oxidation Event is particularly important, as copper is key to nitrogen and methane cycling and was later incorporated into numerous aerobic metabolisms. We find that the diversity of metals used in oxidoreductases has increased through time, suggesting that surface redox potential and metal incorporation influenced the evolution of metabolism, biological electron transfer and microbial ecology.
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References
Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive Earth's biogeochemical cycles. Science 320, 1034–1039 (2008).
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).
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. USA 107, 10567–10572 (2010).
Blankenship, R. E. Origin and early evolution of photosynthesis. Photosynth. Res. 33, 91–111 (1992).
Blankenship, R. E. & Hartman, H. The origin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 23, 94–97 (1998).
Canfield, D. E. Oxygen: A Four Billion Year History (Princeton Univ. Press, 2014).
Falkowski, P. G. Life's Engines: How Microbes Made Earth Habitable (Princeton Univ. Press, 2015).
Williams, R. The Bakerian Lecture, 1981: natural selection of the chemical elements. Proc. R. Soc. Lond. B Biol. Sci. 213, 361–397 (1981).
Kim, J. D., Senn, S., Harel, A., Jelen, B. I. & Falkowski, P. G. Discovering the electronic circuit diagram of life: structural relationships among transition metal binding sites in oxidoreductases. Phil. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120257 (2013).
Harel, A., Bromberg, Y., Falkowski, P. G. & Bhattacharya, D. Evolutionary history of redox metal-binding domains across the tree of life. Proc. Natl Acad. Sci. USA 111, 7042–7047 (2014).
Holm, R. H., Kennepohl, P. & Solomon, E. I. Structural and functional aspects of metal sites in biology. Chem. Rev. 96, 2239–2314 (1996).
Dey, A. et al. Solvent tuning of electrochemical potentials in the active sites of HiPIP versus ferredoxin. Science 318, 1464–1468 (2007).
Hosseinzadeh, P. & Lu, Y. Design and fine-tuning redox potentials of metalloproteins involved in electron transfer in bioenergetics. Biochim. Biophys. Acta Bioenerg. 1857, 557–581 (2016).
Anbar, A. D. & Knoll, A. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137–1142 (2002).
Nitschke, W. & Russell, M. J. Hydrothermal focusing of chemical and chemiosmotic energy, supported by delivery of catalytic Fe, Ni, Mo/W, Co, S and Se, forced life to emerge. J. Mol. Evol. 69, 481–496 (2009).
Lyons, T. W., Fike, D. A. & Zerkle, A. Emerging biogeochemical views of Earth's ancient microbial worlds. Elements 11, 415–421 (2015).
Dupont, C. L., Yang, S., Palenik, B. & Bourne, P. E. Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry. Proc. Natl Acad. Sci. USA 103, 17822–17827 (2006).
Farquhar, J., Bao, H. & Thiemens, M. Atmospheric influence of Earth's earliest sulfur cycle. Science 289, 756–758 (2000).
Canfield, D. E. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36 (2005).
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).
Luo, G. et al. Rapid oxygenation of Earth's atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).
Knoll, A. H., Bergmann, K. D. & Strauss, J. V. Life: the first two billion years. Phil. Trans. R. Soc. B Biol. Sci. 371, 20150493 (2016).
David, L. A. & Alm, E. J. Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469, 93–96 (2011).
McCollom, T. M. & Shock, E. L. Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim. Cosmochim. Acta 61, 4375–4391 (1997).
Canfield, D. A new model for Proterozoic ocean chemistry. Nature 396, 450–453 (1998).
Saito, M. A., Sigman, D. M. & Morel, F. M. The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean–Proterozoic boundary? Inorg. Chim. Acta 356, 308–318 (2003).
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).
Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008).
Anbar, A. D. Elements and evolution. Science 322, 1481–1483 (2008).
Hardisty, D. S. et al. An iodine record of Paleoproterozoic surface ocean oxygenation. Geology 42, 619–622 (2014).
Robbins, L. J. et al. Trace elements at the intersection of marine biological and geochemical evolution. Earth Sci. Rev. 163, 323–348 (2016).
Konhauser, K. O. et al. Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458, 750–753 (2009).
Konhauser, K. O. et al. The Archean nickel famine revisited. Astrobiology 15, 804–815 (2015).
L'vov, N., Nosikov, A. & Antipov, A. Tungsten-containing enzymes. Biochemistry (Mosc.) 67, 196–200 (2002).
Cameron, V., House, C. H. & Brantley, S. L. A first analysis of metallome biosignatures of hyperthermophilic archaea. Archaea 2012, 789278 (2012).
Baross, J. A. & Hoffman, S. E. Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Orig. Life Evol. Biosph. 15, 327–345 (1985).
Miller, S. L. & Bada, J. L. Submarine hot springs and the origin of life. Nature 334, 609–611 (1988).
Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814 (2008).
Levitt, L. S. The role of magnesium in photosynthesis. Science 120, 33–35 (1954).
Schau, M. & Henderson, J. B. Archean chemical weathering at three localities on the Canadian Shield. Precambrian Res. 20, 189–224 (1983).
Macfarlane, A. W., Danielson, A. & Holland, H. D. Geology and major and trace element chemistry of late Archean weathering profiles in the Fortescue Group, Western Australia: implications for atmospheric P O2 . Precambrian Res. 65, 297–317 (1994).
Jones, C., Nomosatryo, S., Crowe, S. A., Bjerrum, C. J. & Canfield, D. E. Iron oxides, divalent cations, silica, and the early Earth phosphorus crisis. Geology 43, 135–138 (2015).
Orengo, C. A., Jones, D. T. & Thornton, J. M. Protein superfamilies and domain superfolds. Nature 372, 631–634 (1994).
Raymond, J., Siefert, J. L., Staples, C. R. & Blankenship, R. E. The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541–554 (2004).
Canfield, D. E., Glazer, A. N. & Falkowski, P. G. The evolution and future of Earth's nitrogen cycle. Science 330, 192–196 (2010).
Joerger, R. D., Bishop, P. E. & Evans, H. J. Bacterial alternative nitrogen fixation systems. CRC Crit. Rev. Microbiol. 16, 1–14 (1988).
Zhang, X., Sigman, D. M., Morel, F. M. & Kraepiel, A. M. Nitrogen isotope fractionation by alternative nitrogenases and past ocean anoxia. Proc. Natl Acad. Sci. USA 111, 4782–4787 (2014).
Stüeken, E. E., Buick, R., Guy, B. M. & Koehler, M. C. Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr. Nature 520, 666–669 (2015).
Falkowski, P. G. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275 (1997).
Glass, J. B., Wolfe-Simon, F. & Anbar, A. Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae. Geobiology 7, 100–123 (2009).
Fennel, K., Follows, M. & Falkowski, P. G. The co-evolution of the nitrogen, carbon and oxygen cycles in the Proterozoic ocean. Am. J. Sci. 305, 526–545 (2005).
Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).
Holland, H. D. The oxygenation of the atmosphere and oceans. Phil. Trans. R. Soc. Lond. B Biol. Sci. 361, 903–915 (2006).
Klotz, M. G. & Stein, L. Y. Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiol. Lett. 278, 146–156 (2008).
Godfrey, L. V. & Falkowski, P. G. The cycling and redox state of nitrogen in the Archaean ocean. Nat. Geosci. 2, 725–729 (2009).
Godfrey, L. V. & Glass, J. B. The geochemical record of the ancient nitrogen cycle, nitrogen isotopes, and metal cofactors. Methods Enzymol. 486, 483–506 (2011).
Krissansen-Totton, J., Buick, R. & Catling, D. C. A statistical analysis of the carbon isotope record from the Archean to Phanerozoic and implications for the rise of oxygen. Am. J. Sci. 315, 275–316 (2015).
Lalonde, S. V. & Konhauser, K. O. Benthic perspective on Earth's oldest evidence for oxygenic photosynthesis. Proc. Natl Acad. Sci. USA 112, 995–1000 (2015).
Noffke, N., Beukes, N., Bower, D., Hazen, R. & Swift, D. An actualistic perspective into Archean worlds–(cyano-) bacterially induced sedimentary structures in the siliciclastic Nhlazatse Section, 2.9 Ga Pongola Supergroup, South Africa. Geobiology 6, 5–20 (2008).
Crowe, S. A. et al. Atmospheric oxygenation three billion years ago. Nature 501, 535–538 (2013).
Riding, R., Fralick, P. & Liang, L. Identification of an Archean marine oxygen oasis. Precambrian Res. 251, 232–237 (2014).
Fru, E. C. et al. Cu isotopes in marine black shales record the Great Oxidation Event. Proc. Natl Acad. Sci. USA 201523544 (2016).
Underwood, E. Trace Elements in Human Health and Animal Nutrition (Academic, 1977).
Ochiai, E.-I. Copper and the biological evolution. Biosystems 16, 81–86 (1983).
Klinman, J. P. Mechanisms whereby mononuclear copper proteins functionalize organic substrates. Chem. Rev. 96, 2541–2562 (1996).
Solomon, E. I., Chen, P., Metz, M., Lee, S. K. & Palmer, A. E. Oxygen binding, activation, and reduction to water by copper proteins. Angew. Chem. Int. Ed. 40, 4570–4590 (2001).
Solomon, E. I. et al. Copper active sites in biology. Chem. Rev. 114, 3659–3853 (2014).
Malkin, R. & Malmström, B. G. The state and function of copper in biological systems. Adv. Enzymol. Relat. Areas Mol. Biol. 33, 177–244 (2006).
Reinhammar, B. in Copper Proteins and Copper Enzymes Vol. 3 (ed. Lontie, R.) 1–35 (CRC, 1984).
Solomon, E. I., Baldwin, M. J. & Lowery, M. D. Electronic structures of active sites in copper proteins: contributions to reactivity. Chem. Rev. 92, 521–542 (1992).
Hart, P., Nersissian, A. & George, S. Encyclopedia of Inorganic Chemistry (Wiley, 2006).
Liu, J. et al. Metalloproteins containing cytochrome, iron–sulfur, or copper redox centers. Chem. Rev. 114, 4366–4469 (2014).
Castresana, J., Lübben, M., Saraste, M. & Higgins, D. G. Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J. 13, 2516 (1994).
Pascher, T., Karlsson, B. G., Nordling, M., Malmström, B. G. & Vänngård, T. Reduction potentials and their pH dependence in site-directed-mutant forms of azurin from Pseudomonas aeruginosa. Eur. J. Biochem. 212, 289–296 (1993).
Romero, A. et al. X-ray analysis and spectroscopic characterization of M121Q azurin: A copper site model for stellacyanin. J. Mol. Biol. 229, 1007–1021 (1993).
Yaver, D. S. et al. Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Appl. Environ. Microbiol. 62, 834–841 (1996).
Nersissian, A. M. et al. Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci. 7, 1915–1929 (1998).
Olesen, K. et al. Spectroscopic, kinetic, and electrochemical characterization of heterologously expressed wild-type and mutant forms of copper-containing nitrite reductase from Rhodobacter sphaeroides 2.4. 3. Biochemistry 37, 6086–6094 (1998).
Kataoka, K., Nakai, M., Yamaguchi, K. & Suzuki, S. Gene synthesis, expression, and mutagenesis of zucchini mavicyanin: the fourth ligand of blue copper center is Gln. Biochem. Biophys. Res. Commun. 250, 409–413 (1998).
Feng, X. et al. Site-directed mutations in fungal laccase: effect on redox potential, activity and pH profile. Biochem. J. 334, 63–70 (1998).
Xu, F. et al. Targeted mutations in a Trametes villosa laccase axial perturbations of the T1 copper. J. Biol. Chem. 274, 12372–12375 (1999).
Hall, J. F., Kanbi, L. D., Strange, R. W. & Hasnain, S. S. Role of the axial ligand in type 1 Cu centers studied by point mutations of Met148 in rusticyanin. Biochemistry 38, 12675–12680 (1999).
Diederix, R. E., Canters, G. W. & Dennison, C. The Met99Gln mutant of amicyanin from Paracoccus versutus. Biochemistry 39, 9551–9560 (2000).
Williams, R. J. P. & Da Silva, J. R. R. F. in New Trends in Bio-inorganic Chemistry, 121–171 (Academic, (1978).
Eigenbrode, J. L. & Freeman, K. H. Late Archean rise of aerobic microbial ecosystems. Proc. Natl Acad. Sci. USA 103, 15759–15764 (2006).
Battistuzzi, F. U., Feijao, A. & Hedges, S. B. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4, 1 (2004).
Battistuzzi, F. & Hedges, S. in Timetree of Life (eds Hedges, S. B. & Kumar, S.) 106–115 (Oxford Univ. Press, 2009).
Ayala, F. J. Molecular clock mirages. BioEssays 21, 71–75 (1999).
Schwartz, J. H. & Maresca, B. Do molecular clocks run at all? A critique of molecular systematics. Biol. Theory 1, 357–371 (2006).
Senn, S., Nanda, V., Falkowski, P. & Bromberg, Y. Function-based assessment of structural similarity measurements using metal co-factor orientation. Proteins 82, 648–656 (2014).
Giovannelli, D. et al. Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans. eLife 6, e18990 (2017).
Dos Santos, P. C., Fang, Z., Mason, S. W., Setubal, J. C. & Dixon, R. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13, 1 (2012).
Falkowski, P. G. From light to life. Orig. Life Evol. Biosph. 45, 347–350 (2015).
Bosak, T., Liang, B., Sim, M. S. & Petroff, A. P. Morphological record of oxygenic photosynthesis in conical stromatolites. Proc. Natl Acad. Sci. USA 106, 10939–10943 (2009).
Sim, M. S. et al. Oxygen-dependent morphogenesis of modern clumped photosynthetic mats and implications for the Archean stromatolite record. Geosciences 2, 235–259 (2012).
Acknowledgements
This work was funded by the Keck Foundation and the Gordon and Betty Moore Foundation. We thank R. Hazen at the Carnegie Institute for Science for his comments on the manuscript.
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E.K.M. (lead author) carried out data analysis; B.I.J., D.G. and H.R. contributed to data analysis and writing; P.G.F. (primary investigator) contributed to writing the paper.
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Moore, E., Jelen, B., Giovannelli, D. et al. Metal availability and the expanding network of microbial metabolisms in the Archaean eon. Nature Geosci 10, 629–636 (2017). https://doi.org/10.1038/ngeo3006
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DOI: https://doi.org/10.1038/ngeo3006
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