Crown group Oxyphotobacteria postdate the rise of oxygen

Shih, P. M.; Hemp, J.; Ward, L. M.; Matzke, N. J.; Fischer, W. W.

doi:10.1111/gbi.12200

Title: Crown group Oxyphotobacteria postdate the rise of oxygen

Journal Article · Fri Jul 08 00:00:00 EDT 2016 · Geobiology

DOI:https://doi.org/10.1111/gbi.12200· OSTI ID:1401457

Shih, P. M. ^[1]; Hemp, J. ^[2]; Ward, L. M. ^[2]; Matzke, N. J. ^[3]; Fischer, W. W. ^[2]

Joint BioEnergy Institute Emeryville CA USA, Physical Biosciences Division Lawrence Berkeley National Laboratory Berkeley CA USA
Division of Geological and Planetary Sciences California Institute of Technology Pasadena CA USA
National Institute for Mathematical and Biological Synthesis University of Tennessee Knoxville TN USA

Abstract The rise of oxygen ca. 2.3 billion years ago (Ga) is the most distinct environmental transition in Earth history. This event was enabled by the evolution of oxygenic photosynthesis in the ancestors of Cyanobacteria. However, long‐standing questions concern the evolutionary timing of this metabolism, with conflicting answers spanning more than one billion years. Recently, knowledge of the Cyanobacteria phylum has expanded with the discovery of non‐photosynthetic members, including a closely related sister group termed Melainabacteria, with the known oxygenic phototrophs restricted to a clade recently designated Oxyphotobacteria. By integrating genomic data from the Melainabacteria, cross‐calibrated Bayesian relaxed molecular clock analyses show that crown group Oxyphotobacteria evolved ca. 2.0 billion years ago (Ga), well after the rise of atmospheric dioxygen. We further estimate the divergence between Oxyphotobacteria and Melainabacteria ca. 2.5–2.6 Ga, which—if oxygenic photosynthesis is an evolutionary synapomorphy of the Oxyphotobacteria—marks an upper limit for the origin of oxygenic photosynthesis. Together, these results are consistent with the hypothesis that oxygenic photosynthesis evolved relatively close in time to the rise of oxygen.

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Sponsoring Organization:: USDOE

OSTI ID:: 1401457

Journal Information:: Geobiology, Journal Name: Geobiology Vol. 15 Journal Issue: 1; ISSN 1472-4677

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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References (66)

The Metagenome of an Anaerobic Microbial Community Decomposing Poplar Wood Chips van der Lelie, Daniel; Taghavi, Safiyh; McCorkle, Sean M. PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0036740	journal	May 2012
A Phylogenomic Approach to Bacterial Phylogeny: Evidence of a Core of Genes Sharing a Common History Daubin, V. Genome Research, Vol. 12, Issue 7 https://doi.org/10.1101/gr.187002	journal	July 2002
Exceptional preservation of fossils in an Upper Proterozoic shale Butterfield, N. J.; Knoll, A. H.; Swett, K. Nature, Vol. 334, Issue 6181 https://doi.org/10.1038/334424a0	journal	August 1988
Proterozoic photosynthesis - a critical review Butterfield, Nicholas J. Palaeontology, Vol. 58, Issue 6 https://doi.org/10.1111/pala.12211	journal	October 2015
Phylogenetic analysis of HpnP reveals the origin of 2-methylhopanoid production in Alphaproteobacteria Ricci, J. N.; Michel, A. J.; Newman, D. K. Geobiology, Vol. 13, Issue 3 https://doi.org/10.1111/gbi.12129	journal	January 2015
Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis Turner, SeÁN; Pryer, Kathleen M.; Miao, Vivian P. W. The Journal of Eukaryotic Microbiology, Vol. 46, Issue 4 https://doi.org/10.1111/j.1550-7408.1999.tb04612.x	journal	July 1999
Bootstrap, Bayesian probability and maximum likelihood mapping: exploring new tools for comparative genome analyses Zhaxybayeva, Olga; Gogarten, J. Peter BMC Genomics, Vol. 3, Issue 1 https://doi.org/10.1186/1471-2164-3-4	journal	February 2002
The evolutionary diversification of cyanobacteria: Molecular-phylogenetic and paleontological perspectives Tomitani, A.; Knoll, A. H.; Cavanaugh, C. M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 14 https://doi.org/10.1073/pnas.0600999103	journal	March 2006
Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle Nakayama, T.; Kamikawa, R.; Tanifuji, G. Proceedings of the National Academy of Sciences, Vol. 111, Issue 31 https://doi.org/10.1073/pnas.1405222111	journal	July 2014
A Neoproterozoic Transition in the Marine Nitrogen Cycle Sánchez-Baracaldo, Patricia; Ridgwell, Andy; Raven, John A. Current Biology, Vol. 24, Issue 6 https://doi.org/10.1016/j.cub.2014.01.041	journal	March 2014
Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago Luo, Genming; Ono, Shuhei; Beukes, Nicolas J. Science Advances, Vol. 2, Issue 5 https://doi.org/10.1126/sciadv.1600134	journal	May 2016
Proterozoic and Living Cyanobacteria Knoll, Andrew H.; Golubic, Stejepko Early Organic Evolution https://doi.org/10.1007/978-3-642-76884-2_35	book	January 1992
Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium Tripp, H. James; Bench, Shellie R.; Turk, Kendra A. Nature, Vol. 464, Issue 7285 https://doi.org/10.1038/nature08786	journal	February 2010
Reappraisal of hydrocarbon biomarkers in Archean rocks French, Katherine L.; Hallmann, Christian; Hope, Janet M. Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1419563112	journal	April 2015
An Expanded Genomic Representation of the Phylum Cyanobacteria Soo, Rochelle M.; Skennerton, Connor T.; Sekiguchi, Yuji Genome Biology and Evolution, Vol. 6, Issue 5 https://doi.org/10.1093/gbe/evu073	journal	May 2014
Evolution of Photosynthesis Hohmann-Marriott, Martin F.; Blankenship, Robert E. Annual Review of Plant Biology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev-arplant-042110-103811	journal	June 2011
Photosynthetic microbial mats in the 3,416-Myr-old ocean Tice, Michael M.; Lowe, Donald R. Nature, Vol. 431, Issue 7008 https://doi.org/10.1038/nature02888	journal	September 2004
A Whiff of Oxygen Before the Great Oxidation Event? Anbar, A. D.; Duan, Y.; Lyons, T. W. Science, Vol. 317, Issue 5846 https://doi.org/10.1126/science.1140325	journal	September 2007
ProtTest: selection of best-fit models of protein evolution Abascal, F.; Zardoya, R.; Posada, D. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti263	journal	January 2005
Ribosomal Database Project: data and tools for high throughput rRNA analysis Cole, James R.; Wang, Qiong; Fish, Jordan A. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1244	journal	November 2013
Evolution of Oxygenic Photosynthesis Fischer, Woodward W.; Hemp, James; Johnson, Jena E. Annual Review of Earth and Planetary Sciences, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-earth-060313-054810	journal	June 2016
BEAST: Bayesian evolutionary analysis by sampling trees Drummond, Alexei J.; Rambaut, Andrew BMC Evolutionary Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2148-7-214	journal	January 2007
Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing Shih, P. M.; Wu, D.; Latifi, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 3, p. 1053-1058 https://doi.org/10.1073/pnas.1217107110	journal	December 2012
Obesity alters gut microbial ecology Ley, R. E.; Backhed, F.; Turnbaugh, P. Proceedings of the National Academy of Sciences, Vol. 102, Issue 31 https://doi.org/10.1073/pnas.0504978102	journal	July 2005
Cyanobacterial Evolution: Fresh Insight into Ancient Questions Shih, Patrick M. Current Biology, Vol. 25, Issue 5 https://doi.org/10.1016/j.cub.2014.12.046	journal	March 2015
A novel scenario for the evolution of haem–copper oxygen reductases Pereira, Manuela M.; Santana, Margarida; Teixeira, Miguel Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1505, Issue 2-3 https://doi.org/10.1016/S0005-2728(01)00169-4	journal	June 2001
Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago Kump, Lee R.; Barley, Mark E. Nature, Vol. 448, Issue 7157 https://doi.org/10.1038/nature06058	journal	August 2007
Questioning the evidence for Earth's oldest fossils Brasier, Martin D.; Green, Owen R.; Jephcoat, Andrew P. Nature, Vol. 416, Issue 6876 https://doi.org/10.1038/416076a	journal	March 2002
Support for the Lunar Cataclysm Hypothesis from Lunar Meteorite Impact Melt Ages Cohen, B. A. Science, Vol. 290, Issue 5497 https://doi.org/10.1126/science.290.5497.1754	journal	December 2000
Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event Schirrmeister, B. E.; de Vos, J. M.; Antonelli, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 5 https://doi.org/10.1073/pnas.1209927110	journal	January 2013
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Timescales of Oxygenation Following the Evolution of Oxygenic Photosynthesis Ward, Lewis M.; Kirschvink, Joseph L.; Fischer, Woodward W. Origins of Life and Evolution of Biospheres, Vol. 46, Issue 1 https://doi.org/10.1007/s11084-015-9460-3	journal	August 2015
U-rich Archaean sea-floor sediments from Greenland – indications of >3700 Ma oxygenic photosynthesis Rosing, Minik T.; Frei, Robert Earth and Planetary Science Letters, Vol. 217, Issue 3-4 https://doi.org/10.1016/S0012-821X(03)00609-5	journal	January 2004
O ₂ constraints from Paleoproterozoic detrital pyrite and uraninite Johnson, Jena E.; Gerpheide, Aya; Lamb, Michael P. Geological Society of America Bulletin, Vol. 126, Issue 5-6 https://doi.org/10.1130/B30949.1	journal	February 2014
Whole-Genome Analysis of Photosynthetic Prokaryotes Raymond, J. Science, Vol. 298, Issue 5598 https://doi.org/10.1126/science.1075558	journal	November 2002
Photosynthesis and early Earth Shih, Patrick M. Current Biology, Vol. 25, Issue 19 https://doi.org/10.1016/j.cub.2015.04.046	journal	October 2015
The cycling and redox state of nitrogen in the Archaean ocean Godfrey, Linda V.; Falkowski, Paul G. Nature Geoscience, Vol. 2, Issue 10 https://doi.org/10.1038/ngeo633	journal	September 2009
Archean Molecular Fossils and the Early Rise of Eukaryotes Brocks, J. J. Science, Vol. 285, Issue 5430 https://doi.org/10.1126/science.285.5430.1033	journal	August 1999
The Great Oxidation and a Siderian snowball Earth: MIF-S based correlation of Paleoproterozoic glacial epochs Hoffman, Paul F. Chemical Geology, Vol. 362 https://doi.org/10.1016/j.chemgeo.2013.04.018	journal	December 2013
An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants Smith, S. A.; Beaulieu, J. M.; Donoghue, M. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 13 https://doi.org/10.1073/pnas.1001225107	journal	March 2010
How did life survive Earth's great oxygenation? Fischer, Woodward W.; Hemp, James; Valentine, Joan Selverstone Current Opinion in Chemical Biology, Vol. 31 https://doi.org/10.1016/j.cbpa.2016.03.013	journal	April 2016
Why the atmosphere became oxygenated: A proposal Holland, Heinrich D. Geochimica et Cosmochimica Acta, Vol. 73, Issue 18 https://doi.org/10.1016/j.gca.2009.05.070	journal	September 2009
A Major Clade of Prokaryotes with Ancient Adaptations to Life on Land Battistuzzi, F. U.; Hedges, S. B. Molecular Biology and Evolution, Vol. 26, Issue 2 https://doi.org/10.1093/molbev/msn247	journal	November 2008
Nitrite-driven anaerobic methane oxidation by oxygenic bacteria Ettwig, Katharina F.; Butler, Margaret K.; Le Paslier, Denis Nature, Vol. 464, Issue 7288 https://doi.org/10.1038/nature08883	journal	March 2010
Creating the CIPRES Science Gateway for inference of large phylogenetic trees Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri 2010 Gateway Computing Environments Workshop (GCE) https://doi.org/10.1109/GCE.2010.5676129	conference	November 2010
Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins Shih, P. M.; Matzke, N. J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 30 https://doi.org/10.1073/pnas.1305813110	journal	June 2013
Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event Planavsky, Noah J.; Asael, Dan; Hofmann, Axel Nature Geoscience, Vol. 7, Issue 4 https://doi.org/10.1038/ngeo2122	journal	March 2014
Manganese-oxidizing photosynthesis before the rise of cyanobacteria Johnson, J. E.; Webb, S. M.; Thomas, K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 28 https://doi.org/10.1073/pnas.1305530110	journal	June 2013
Life before the rise of oxygen Fischer, Woodward W. Nature, Vol. 455, Issue 7216 https://doi.org/10.1038/4551051a	journal	October 2008
Early Archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona Group, Australia Schopf, J.; Packer, B. Science, Vol. 237, Issue 4810 https://doi.org/10.1126/science.11539686	journal	July 1987
Atmospheric oxygenation three billion years ago Crowe, Sean A.; Døssing, Lasse N.; Beukes, Nicolas J. Nature, Vol. 501, Issue 7468 https://doi.org/10.1038/nature12426	journal	September 2013
The geological consequences of evolution Knoll, Andrew H. Geobiology, Vol. 1, Issue 1 https://doi.org/10.1046/j.1472-4669.2003.00002.x	journal	July 2003
The Paleoproterozoic snowball Earth: A climate disaster triggered by the evolution of oxygenic photosynthesis Kopp, R. E.; Kirschvink, J. L.; Hilburn, I. A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 32 https://doi.org/10.1073/pnas.0504878102	journal	August 2005
MAFFT version 5: improvement in accuracy of multiple sequence alignment Katoh, K. Nucleic Acids Research, Vol. 33, Issue 2 https://doi.org/10.1093/nar/gki198	journal	January 2005
The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria Di Rienzi, Sara C.; Sharon, Itai; Wrighton, Kelly C. eLife, Vol. 2 https://doi.org/10.7554/eLife.01102	journal	October 2013
Reply to Jones and Crowe: Correcting mistaken views of sedimentary geology, Mn-oxidation rates, and molecular clocks Johnson, J. E.; Webb, S. M.; Thomas, K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 44 https://doi.org/10.1073/pnas.1315376110	journal	October 2013
Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy Letunic, I.; Bork, P. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr201	journal	April 2011
Infernal 1.0: inference of RNA alignments Nawrocki, E. P.; Kolbe, D. L.; Eddy, S. R. Bioinformatics, Vol. 25, Issue 10 https://doi.org/10.1093/bioinformatics/btp157	journal	March 2009
Production of hydrogen peroxide in the atmosphere of a Snowball Earth and the origin of oxygenic photosynthesis Liang, M. -C.; Hartman, H.; Kopp, R. E. Proceedings of the National Academy of Sciences, Vol. 103, Issue 50 https://doi.org/10.1073/pnas.0608839103	journal	November 2006
A Molecular Timeline for the Origin of Photosynthetic Eukaryotes Yoon, Hwan Su; Hackett, Jeremiah D.; Ciniglia, Claudia Molecular Biology and Evolution, Vol. 21, Issue 5 https://doi.org/10.1093/molbev/msh075	journal	May 2004
Dating the cyanobacterial ancestor of the chloroplast Falcón, Luisa I.; Magallón, Susana; Castillo, Amanda The ISME Journal, Vol. 4, Issue 6 https://doi.org/10.1038/ismej.2010.2	journal	March 2010
A bangiophyte red alga from the Proterozoic of arctic Canada Butterfield, N.; Knoll, A.; Swett, K. Science, Vol. 250, Issue 4977 https://doi.org/10.1126/science.11538072	journal	October 1990
A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea Wu, Dongying; Hugenholtz, Philip; Mavromatis, Konstantinos Nature, Vol. 462, Issue 7276 https://doi.org/10.1038/nature08656	journal	December 2009
Acidophilic and thermophilic Bacillus strains from geothermally heated antarctic soil Andrew Hudson, J.; Daniel, Roy M.; Morgan, Hugh W. FEMS Microbiology Letters, Vol. 60, Issue 3 https://doi.org/10.1111/j.1574-6968.1989.tb03486.x	journal	August 1989
The cyanobacterial genome core and the origin of photosynthesis Mulkidjanian, A. Y.; Koonin, E. V.; Makarova, K. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 35 https://doi.org/10.1073/pnas.0605709103	journal	August 2006

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