Metal availability and the expanding network of microbial metabolisms in the Archaean eon

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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Figure 1: Protein metallocofactors of core microbial metabolisms.
Figure 2: Preserved geochemical evidence ages of Archaean metabolisms billions of years ago (Ga) and global oxygenation.
Figure 3: Global electron-transfer network and redox potential expansion through time.
Figure 4: Phylogenetic tree of the main lineages of Bacteria and Archaea and their putative divergence times.

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References

  1. 1

    Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive Earth's biogeochemical cycles. Science 320, 1034–1039 (2008).

    Google Scholar 

  2. 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).

    Google Scholar 

  3. 3

    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).

    Google Scholar 

  4. 4

    Blankenship, R. E. Origin and early evolution of photosynthesis. Photosynth. Res. 33, 91–111 (1992).

    Google Scholar 

  5. 5

    Blankenship, R. E. & Hartman, H. The origin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 23, 94–97 (1998).

    Google Scholar 

  6. 6

    Canfield, D. E. Oxygen: A Four Billion Year History (Princeton Univ. Press, 2014).

    Google Scholar 

  7. 7

    Falkowski, P. G. Life's Engines: How Microbes Made Earth Habitable (Princeton Univ. Press, 2015).

    Google Scholar 

  8. 8

    Williams, R. The Bakerian Lecture, 1981: natural selection of the chemical elements. Proc. R. Soc. Lond. B Biol. Sci. 213, 361–397 (1981).

    Google Scholar 

  9. 9

    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).

    Google Scholar 

  10. 10

    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).

    Google Scholar 

  11. 11

    Holm, R. H., Kennepohl, P. & Solomon, E. I. Structural and functional aspects of metal sites in biology. Chem. Rev. 96, 2239–2314 (1996).

    Google Scholar 

  12. 12

    Dey, A. et al. Solvent tuning of electrochemical potentials in the active sites of HiPIP versus ferredoxin. Science 318, 1464–1468 (2007).

    Google Scholar 

  13. 13

    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).

    Google Scholar 

  14. 14

    Anbar, A. D. & Knoll, A. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137–1142 (2002).

    Google Scholar 

  15. 15

    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).

    Google Scholar 

  16. 16

    Lyons, T. W., Fike, D. A. & Zerkle, A. Emerging biogeochemical views of Earth's ancient microbial worlds. Elements 11, 415–421 (2015).

    Google Scholar 

  17. 17

    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).

    Google Scholar 

  18. 18

    Farquhar, J., Bao, H. & Thiemens, M. Atmospheric influence of Earth's earliest sulfur cycle. Science 289, 756–758 (2000).

    Google Scholar 

  19. 19

    Canfield, D. E. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36 (2005).

    Google Scholar 

  20. 20

    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).

    Google Scholar 

  21. 21

    Luo, G. et al. Rapid oxygenation of Earth's atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).

    Google Scholar 

  22. 22

    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).

    Google Scholar 

  23. 23

    David, L. A. & Alm, E. J. Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469, 93–96 (2011).

    Google Scholar 

  24. 24

    McCollom, T. M. & Shock, E. L. Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim. Cosmochim. Acta 61, 4375–4391 (1997).

    Google Scholar 

  25. 25

    Canfield, D. A new model for Proterozoic ocean chemistry. Nature 396, 450–453 (1998).

    Google Scholar 

  26. 26

    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).

    Google Scholar 

  27. 27

    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).

    Google Scholar 

  28. 28

    Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008).

    Google Scholar 

  29. 29

    Anbar, A. D. Elements and evolution. Science 322, 1481–1483 (2008).

    Google Scholar 

  30. 30

    Hardisty, D. S. et al. An iodine record of Paleoproterozoic surface ocean oxygenation. Geology 42, 619–622 (2014).

    Google Scholar 

  31. 31

    Robbins, L. J. et al. Trace elements at the intersection of marine biological and geochemical evolution. Earth Sci. Rev. 163, 323–348 (2016).

    Google Scholar 

  32. 32

    Konhauser, K. O. et al. Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458, 750–753 (2009).

    Google Scholar 

  33. 33

    Konhauser, K. O. et al. The Archean nickel famine revisited. Astrobiology 15, 804–815 (2015).

    Google Scholar 

  34. 34

    L'vov, N., Nosikov, A. & Antipov, A. Tungsten-containing enzymes. Biochemistry (Mosc.) 67, 196–200 (2002).

    Google Scholar 

  35. 35

    Cameron, V., House, C. H. & Brantley, S. L. A first analysis of metallome biosignatures of hyperthermophilic archaea. Archaea 2012, 789278 (2012).

    Google Scholar 

  36. 36

    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).

    Google Scholar 

  37. 37

    Miller, S. L. & Bada, J. L. Submarine hot springs and the origin of life. Nature 334, 609–611 (1988).

    Google Scholar 

  38. 38

    Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814 (2008).

    Google Scholar 

  39. 39

    Levitt, L. S. The role of magnesium in photosynthesis. Science 120, 33–35 (1954).

    Google Scholar 

  40. 40

    Schau, M. & Henderson, J. B. Archean chemical weathering at three localities on the Canadian Shield. Precambrian Res. 20, 189–224 (1983).

    Google Scholar 

  41. 41

    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).

    Google Scholar 

  42. 42

    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).

    Google Scholar 

  43. 43

    Orengo, C. A., Jones, D. T. & Thornton, J. M. Protein superfamilies and domain superfolds. Nature 372, 631–634 (1994).

    Google Scholar 

  44. 44

    Raymond, J., Siefert, J. L., Staples, C. R. & Blankenship, R. E. The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541–554 (2004).

    Google Scholar 

  45. 45

    Canfield, D. E., Glazer, A. N. & Falkowski, P. G. The evolution and future of Earth's nitrogen cycle. Science 330, 192–196 (2010).

    Google Scholar 

  46. 46

    Joerger, R. D., Bishop, P. E. & Evans, H. J. Bacterial alternative nitrogen fixation systems. CRC Crit. Rev. Microbiol. 16, 1–14 (1988).

    Google Scholar 

  47. 47

    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).

    Google Scholar 

  48. 48

    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).

    Google Scholar 

  49. 49

    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).

    Google Scholar 

  50. 50

    Glass, J. B., Wolfe-Simon, F. & Anbar, A. Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae. Geobiology 7, 100–123 (2009).

    Google Scholar 

  51. 51

    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).

    Google Scholar 

  52. 52

    Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).

    Google Scholar 

  53. 53

    Holland, H. D. The oxygenation of the atmosphere and oceans. Phil. Trans. R. Soc. Lond. B Biol. Sci. 361, 903–915 (2006).

    Google Scholar 

  54. 54

    Klotz, M. G. & Stein, L. Y. Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiol. Lett. 278, 146–156 (2008).

    Google Scholar 

  55. 55

    Godfrey, L. V. & Falkowski, P. G. The cycling and redox state of nitrogen in the Archaean ocean. Nat. Geosci. 2, 725–729 (2009).

    Google Scholar 

  56. 56

    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).

    Google Scholar 

  57. 57

    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).

    Google Scholar 

  58. 58

    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).

    Google Scholar 

  59. 59

    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).

    Google Scholar 

  60. 60

    Crowe, S. A. et al. Atmospheric oxygenation three billion years ago. Nature 501, 535–538 (2013).

    Google Scholar 

  61. 61

    Riding, R., Fralick, P. & Liang, L. Identification of an Archean marine oxygen oasis. Precambrian Res. 251, 232–237 (2014).

    Google Scholar 

  62. 62

    Fru, E. C. et al. Cu isotopes in marine black shales record the Great Oxidation Event. Proc. Natl Acad. Sci. USA 201523544 (2016).

  63. 63

    Underwood, E. Trace Elements in Human Health and Animal Nutrition (Academic, 1977).

    Google Scholar 

  64. 64

    Ochiai, E.-I. Copper and the biological evolution. Biosystems 16, 81–86 (1983).

    Google Scholar 

  65. 65

    Klinman, J. P. Mechanisms whereby mononuclear copper proteins functionalize organic substrates. Chem. Rev. 96, 2541–2562 (1996).

    Google Scholar 

  66. 66

    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).

    Google Scholar 

  67. 67

    Solomon, E. I. et al. Copper active sites in biology. Chem. Rev. 114, 3659–3853 (2014).

    Google Scholar 

  68. 68

    Malkin, R. & Malmström, B. G. The state and function of copper in biological systems. Adv. Enzymol. Relat. Areas Mol. Biol. 33, 177–244 (2006).

    Google Scholar 

  69. 69

    Reinhammar, B. in Copper Proteins and Copper Enzymes Vol. 3 (ed. Lontie, R.) 1–35 (CRC, 1984).

    Google Scholar 

  70. 70

    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).

    Google Scholar 

  71. 71

    Hart, P., Nersissian, A. & George, S. Encyclopedia of Inorganic Chemistry (Wiley, 2006).

    Google Scholar 

  72. 72

    Liu, J. et al. Metalloproteins containing cytochrome, iron–sulfur, or copper redox centers. Chem. Rev. 114, 4366–4469 (2014).

    Google Scholar 

  73. 73

    Castresana, J., Lübben, M., Saraste, M. & Higgins, D. G. Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J. 13, 2516 (1994).

    Google Scholar 

  74. 74

    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).

    Google Scholar 

  75. 75

    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).

    Google Scholar 

  76. 76

    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).

    Google Scholar 

  77. 77

    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).

    Google Scholar 

  78. 78

    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).

    Google Scholar 

  79. 79

    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).

    Google Scholar 

  80. 80

    Feng, X. et al. Site-directed mutations in fungal laccase: effect on redox potential, activity and pH profile. Biochem. J. 334, 63–70 (1998).

    Google Scholar 

  81. 81

    Xu, F. et al. Targeted mutations in a Trametes villosa laccase axial perturbations of the T1 copper. J. Biol. Chem. 274, 12372–12375 (1999).

    Google Scholar 

  82. 82

    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).

    Google Scholar 

  83. 83

    Diederix, R. E., Canters, G. W. & Dennison, C. The Met99Gln mutant of amicyanin from Paracoccus versutus. Biochemistry 39, 9551–9560 (2000).

    Google Scholar 

  84. 84

    Williams, R. J. P. & Da Silva, J. R. R. F. in New Trends in Bio-inorganic Chemistry, 121–171 (Academic, (1978).

    Google Scholar 

  85. 85

    Eigenbrode, J. L. & Freeman, K. H. Late Archean rise of aerobic microbial ecosystems. Proc. Natl Acad. Sci. USA 103, 15759–15764 (2006).

    Google Scholar 

  86. 86

    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).

    Google Scholar 

  87. 87

    Battistuzzi, F. & Hedges, S. in Timetree of Life (eds Hedges, S. B. & Kumar, S.) 106–115 (Oxford Univ. Press, 2009).

    Google Scholar 

  88. 88

    Ayala, F. J. Molecular clock mirages. BioEssays 21, 71–75 (1999).

    Google Scholar 

  89. 89

    Schwartz, J. H. & Maresca, B. Do molecular clocks run at all? A critique of molecular systematics. Biol. Theory 1, 357–371 (2006).

    Google Scholar 

  90. 90

    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).

    Google Scholar 

  91. 91

    Giovannelli, D. et al. Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans. eLife 6, e18990 (2017).

    Google Scholar 

  92. 92

    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).

    Google Scholar 

  93. 93

    Falkowski, P. G. From light to life. Orig. Life Evol. Biosph. 45, 347–350 (2015).

    Google Scholar 

  94. 94

    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).

    Google Scholar 

  95. 95

    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).

    Google Scholar 

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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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Correspondence to Paul G. Falkowski.

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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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