nature.com

The evolution of oxygen-utilizing enzymes suggests early biosphere oxygenation - Nature Ecology & Evolution

  • ️Tawfik, Dan S.
  • ️Thu Feb 25 2021
  • Raymond, J. & Segrè, D. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311, 1764–1767 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Holland, H. D. The oxygenation of the atmosphere and oceans. Philos. Trans. R. Soc. Lond. B https://doi.org/10.1098/rstb.2006.1838 (2006).

  • Holland, H. D. Volcanic gases, black smokers, and the great oxidation event. Geochim. Cosmochim. Acta 66, 3811–3826 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kasting, J. F. & Howard, M. T. Atmospheric composition and climate on the early Earth. Philos. Trans. R. Lond. Soc. B 361, 1733–1741 (2006).

  • Olson, S. L., Kump, L. R. & Kasting, J. F. Quantifying the areal extent and dissolved oxygen concentrations of Archean oxygen oases. Chem. Geol. 362, 35–43 (2013).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan, Y. et al. A whiff of oxygen before the great oxidation event? Science 317, 1903–1906 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Jabłońska, J. & Tawfik, D. S. The number and type of oxygen-utilizing enzymes indicates aerobic vs. anaerobic phenotype. Free Radic. Biol. Med. 140, 84–92 (2019).

    Article  PubMed  CAS  Google Scholar 

  • Sousa, F. L., Nelson-Sathi, S. & Martin, W. F. One step beyond a ribosome: the ancient anaerobic core. Biochim. Biophys. Acta Bioenerg. 1857, 1027–1038 (2016).

    Article  CAS  Google Scholar 

  • Das, A., Silaghi-Dumitrescu, R., Ljungdahl, L. G. & Kurtz, D. M. Cytochrome bd oxidase, oxidative stress, and dioxygen tolerance of the strictly anaerobic bacterium Moorella thermoacetica. J. Bacteriol. 187, 2020–2029 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ettwig, K. F. et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464, 543–548 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Slesak, I., Slesak, H. & Kruk, J. Oxygen and hydrogen peroxide in the early evolution of life on earth: in silico comparative analysis of biochemical pathways. Astrobiology 12, 775–784 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouzounis, C. A., Kunin, V., Darzentas, N. & Goldovsky, L. A minimal estimate for the gene content of the last universal common ancestor – exobiology from a terrestrial perspective. Res. Microbiol. 157, 57–68 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Hofbauer, S., Schaffner, I., Furtmüller, P. G. & Obinger, C. Chlorite dismutases – a heme enzyme family for use in bioremediation and generation of molecular oxygen. Biotechnol. J. 9, 461–473 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanehisa, M. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gribaldo, S., Talla, E. & Brochier-Armanet, C. Evolution of the haem copper oxidases superfamily: a rooting tale. Trends Biochem. Sci. 34, 375–381 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Fischer, W. W., Hemp, J. & Johnson, J. E. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44, 647–683 (2016).

    Article  CAS  Google Scholar 

  • Battistuzzi, F. U. & Hedges, S. B. A major clade of prokaryotes with ancient adaptations to life on land. Mol. Biol. Evol. 26, 335–343 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Bansal, M. S., Wu, Y.-C., Alm, E. J. & Kellis, M. Improved gene tree error correction in the presence of horizontal gene transfer. Bioinformatics 31, 1211–1218 (2015).

    Article  PubMed  Google Scholar 

  • Gribaldo, S. & Brochier, C. Phylogeny of prokaryotes: does it exist and why should we care? Res. Microbiol. 160, 513–521 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Nelson-Sathi, S. et al. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517, 77–80 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Fuchsman, C. A., Collins, R. E., Rocap, G. & Brazelton, W. J. Effect of the environment on horizontal gene transfer between bacteria and archaea. PeerJ. 2017, e3865 (2017).

    Article  CAS  Google Scholar 

  • Garushyants, S. K., Kazanov, M. D. & Gelfand, M. S. Horizontal gene transfer and genome evolution in Methanosarcina. BMC Evol. Biol. 15, 102 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  • Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).

    Article  CAS  PubMed  Google Scholar 

  • Maxwell Burroughs, A., Glasner, M. E., Barry, K. P., Taylor, E. A. & Aravind, L. Oxidative opening of the aromatic ring: tracing the natural history of a large superfamily of dioxygenase domains and their relatives. J. Biol. Chem. 294, 10211–10235 (2019).

    Article  CAS  PubMed  Google Scholar 

  • Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Cardona, T., Sánchez-Baracaldo, P., Rutherford, A. W. & Larkum, A. W. Early Archean origin of Photosystem II. Geobiology 17, 127–150 (2019).

    Article  CAS  PubMed  Google Scholar 

  • Granold, M., Hajieva, P., Toşa, M. I., Irimie, F. D. & Moosmann, B. Modern diversification of the amino acid repertoire driven by oxygen. Proc. Natl Acad. Sci. USA 115, 41–46 (2018).

    Article  CAS  PubMed  Google Scholar 

  • Gray, H. B. & Winkler, J. R. Living with oxygen. Acc. Chem. Res. 51, 1850–1857 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fournier, G. P. & Alm, E. J. Ancestral reconstruction of a pre-LUCA aminoacyl-tRNA synthetase ancestor supports the late addition of Trp to the genetic code. J. Mol. Evol. 80, 171–185 (2015).

    Article  CAS  PubMed  Google Scholar 

  • De Pouplana, L. R., Frugier, M., Quinn, C. L. & Schimmel, P. Evidence that two present-day components needed for the genetic code appeared after nucleated cells separated from eubacteria. Proc. Natl Acad. Sci. USA 93, 166–170 (1996).

    Article  Google Scholar 

  • Waldbauer, J. R., Newman, D. K. & Summons, R. E. Microaerobic steroid biosynthesis and the molecular fossil record of Archean life. Proc. Natl Acad. Sci. USA 108, 13409–13414 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss, M. C., Preiner, M., Xavier, J. C., Zimorski, V. & Martin, W. F. The last universal common ancestor between ancient Earth chemistry and the onset of genetics. PLoS Genet. 14, e1007518 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Berkemer, S. J. & McGlynn, S. E. A new analysis of archaea–bacteria domain separation: variable phylogenetic distance and the tempo of early evolution. Mol. Biol. Evol. 37, 2332–2340 (2020).

  • Ślesak, I., Ślesak, H., Zimak-Piekarczyk, P. & Rozpądek, P. Enzymatic antioxidant systems in early anaerobes: theoretical considerations. Astrobiology 16, 348–358 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Juty, N. S., Moshiri, F., Merrick, M., Anthony, C. & Hill, S. The Klebsiella pneumoniae cytochrome bd’ terminal oxidase complex and its role in microaerobic nitrogen fixation. Microbiology 143, 2673–2683 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Jay, Z. J. et al. Predominant Acidilobus-like populations from geothermal environments in Yellowstone National Park exhibit similar metabolic potential in different hypoxic microbial communities. Appl. Environ. Microbiol. 80, 294–305 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falcón, L. I., Magallón, S. & Castillo, A. Dating the cyanobacterial ancestor of the chloroplast. ISME J. 4, 777–783 (2010).

    Article  PubMed  CAS  Google Scholar 

  • Shih, P. M., Hemp, J., Ward, L. M., Matzke, N. J. & Fischer, W. W. Crown group Oxyphotobacteria postdate the rise of oxygen. Geobiology 15, 19–29 (2017).

    Article  CAS  PubMed  Google Scholar 

  • Betts, H. C. et al. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nat. Ecol. Evol. 2, 1556–1562 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • Magnabosco, C., Moore, K. R., Wolfe, J. M. & Fournier, G. P. Dating phototrophic microbial lineages with reticulate gene histories. Geobiology 16, 179–189 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gumsley, A. P. et al. Timing and tempo of the great oxidation event. Proc. Natl Acad. Sci. USA 114, 1811–1816 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farquhar, J. & Wing, B. A. Multiple sulfur isotopes and the evolution of the atmosphere. Earth Planet. Sci. Lett. 213, 1–13 (2003).

    Article  CAS  Google Scholar 

  • Wang, X. et al. A Mesoarchean shift in uranium isotope systematics. Geochim. Cosmochim. Acta 238, 438–452 (2018).

    Article  CAS  Google Scholar 

  • Planavsky, N. J. et al. Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat. Geosci. 7, 283–286 (2014).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Eickmann, B. et al. Isotopic evidence for oxygenated Mesoarchaean shallow oceans. Nat. Geosci. 11, 133–138 (2018).

    Article  CAS  Google Scholar 

  • Albut, G. et al. Modern rather than Mesoarchaean oxidative weathering responsible for the heavy stable Cr isotopic signatures of the 2.95 Ga old Ijzermijn iron formation (South Africa). Geochim. Cosmochim. Acta 228, 157–189 (2018).

    Article  CAS  Google Scholar 

  • Catling, D. C. & Zahnle, K. J. The Archean atmosphere. Sci. Adv. 6, eaax1420 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bairoch, A. The ENZYME database in 2000. Nucleic Acids Res. 28, 304–305 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alborzi, S. Z., Devignes, M. D. & Ritchie, D. W. ECDomainMiner: discovering hidden associations between enzyme commission numbers and Pfam domains. BMC Bioinform. 18, 107 (2017).

    Article  CAS  Google Scholar 

  • Raymond, J. & Blankenship, R. E. Biosynthetic pathways, gene replacement and the antiquity of life. Geobiology 2, 199–203 (2004).

    Article  CAS  Google Scholar 

  • Gygli, G., Lucas, M. F., Guallar, V. & van Berkel, W. J. H. The ins and outs of vanillyl alcohol oxidase: identification of ligand migration paths. PLoS Comput. Biol. 13, e1005787 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

  • Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tria, F. D. K., Landan, G. & Dagan, T. Phylogenetic rooting using minimal ancestor deviation. Nat. Ecol. Evol. 1, 193 (2017).

    Article  PubMed  Google Scholar