Dating phototrophic microbial lineages with reticulate gene histories
Open accessAbstract
Phototrophic bacteria are among the most biogeochemically significant organisms on Earth and are physiologically related through the use of reaction centers to collect photons for energy metabolism. However, the major phototrophic lineages are not closely related to one another in bacterial phylogeny, and the origins of their respective photosynthetic machinery remain obscured by time and low sequence similarity. To better understand the co‐evolution of Cyanobacteria and other ancient anoxygenic phototrophic lineages with respect to geologic time, we designed and implemented a variety of molecular clocks that use horizontal gene transfer (HGT) as additional, relative constraints. These HGT constraints improve the precision of phototroph divergence date estimates and indicate that stem green non‐sulfur bacteria are likely the oldest phototrophic lineage. Concurrently, crown Cyanobacteria age estimates ranged from 2.2 Ga to 2.7 Ga, with stem Cyanobacteria diverging ~2.8 Ga. These estimates provide a several hundred Ma window for oxygenic photosynthesis to evolve prior to the Great Oxidation Event (GOE) ~2.3 Ga. In all models, crown green sulfur bacteria diversify after the loss of the banded iron formations from the sedimentary record (~1.8 Ga) and may indicate the expansion of the lineage into a new ecological niche following the GOE. Our date estimates also provide a timeline to investigate the temporal feasibility of different photosystem HGT events between phototrophic lineages. Using this approach, we infer that stem Cyanobacteria are unlikely to be the recipient of an HGT of photosystem I proteins from green sulfur bacteria but could still have been either the HGT donor or the recipient of photosystem II proteins with green non‐sulfur bacteria, prior to the GOE. Together, these results indicate that HGT‐constrained molecular clocks are useful tools for the evaluation of various geological and evolutionary hypotheses, using the evolutionary histories of both genes and organismal lineages.
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Most studies suggest an earlier Paleoarchean or Mesoarchean age for oxygenic photosynthesis.
“While some argue that oxygenic photosynthesis evolved only 50 to 100 Ma before the GOE (115), most studies suggest an earlier Paleoarchean or Mesoarchean age [e.g., (3, 118, 119)].”
From The Archean atmosphere (2020) · cites this paper as [119]
The Results and Discussion section (page unavailable) dates stem Cyanobacteria to about 2.8 Ga and says that this allows time for oxygenic photosynthesis to evolve before the GOE. It does not date the evolution of oxygenic photosynthesis itself to the Paleoarchean or Mesoarchean, or establish that most studies favor those ages. (LLM, conf=0.84)
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Cites
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · see citing works
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
Stamatakis, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu033 · Cited by 32,291 · see citing works
Woese, C. R. (1987) · Microbiological Reviews · doi:10.1128/mr.51.2.221-271.1987 · Cited by 5,042 · cited 16× · see citing works
“In recent years, several date estimates for the origins of Cyanobacteria (Blank & Sanchez- Baracaldo, 2010; Dvořák et al., 2014; Falcón, Magallón, & Castillo, 2010; Sánchez- Baracaldo, 2015; Schirrmeister, de Vos, Antonelli, & Bagheri, 2013; Schirrmeister, Gugger, & Donoghue, 2015; Shih, Hemp, Ward, Matzke, & Fischer,…”
BackgroundMethodInfluentialThe rise of oxygen in Earth's early ocean and atmosphere
Lyons, T. W., Reinhard, C. T., & Planavsky, N. J. (2014) · Nature · doi:10.1038/nature13068 · Cited by 2,810 · cited 2× · see citing works
“Although a more complex picture of oceanic Fe/S ratios throughout the Proterozoic is coming to light (Lyons et al., 2014), increased rates of anoxygenic photosynthesis and aerobic heterotrophy are believed to have maintained the low levels of O2 throughout this period (Johnston, Wolfe- Simon, Pearson, & Knoll, 2009).”
BackgroundAnoxygenic Photosynthetic Bacteria
Blankenship, R. E., Bauer, C. E., & Madigan, M. T. (1995) · Advances in photosynthesis and respiration · doi:10.1007/0-306-47954-0 · Cited by 1,912 · see citing works
The Chemical Evolution of the Atmosphere and Oceans
Holland, H. D. (1984) · doi:10.1515/9780691220239 · Cited by 1,836 · see citing works
Atmospheric Influence of Earth's Earliest Sulfur Cycle
Farquhar, J., Bao, H., & Thiemens, M. (2000) · Science · doi:10.1126/science.289.5480.756 · Cited by 1,805 · see citing works
Wilde, S. A., Valley, J. W., Peck, W. H., & Graham, C. M. (2001) · Nature · doi:10.1038/35051550 · Cited by 1,744 · see citing works
Desikan, R., Last, K., Harrett‐Williams, R., Tagliavia, C., Harter, K., Hooley, R., Hancock, J. T., & Neill, S. J. (2006) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02842.x · Cited by 1,713 · see citing works
Gray, M. W., Burger, G., & Lang, B. F. (1999) · Science · doi:10.1126/science.283.5407.1476 · Cited by 1,710 · see citing works
Dating the rise of atmospheric oxygen
Bekker, A., Holland, H. D., Wang, P.-L., Rumble, D., Stein, H. J., Hannah, J. L., Coetzee, L. L., & Beukes, N. J. (2004) · Nature · doi:10.1038/nature02260 · Cited by 1,435 · cited 2× · see citing works
“It is generally accepted that the loss of the mass- independent sulfur isotope fractionations from the sedimentary record ~2.4 to ~2.3 Ga (Bekker et al., 2004; Farquhar, Bao, & Thiemens, 2000; Luo et al., 2016) marks the transitional period prior to the stabilization of an oxygenated atmosphere…”
BackgroundInfluentialHorizontal gene transfer: building the web of life
Soucy, S. M., Huang, J.-L., & Gogarten, J. (2015) · Nature reviews genetics · doi:10.1038/nrg3962 · Cited by 1,304 · see citing works
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating
Lartillot, N., Lepage, T., & Blanquart, S. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp368 · Cited by 1,297 · see citing works
Littlewood, D. T. J., Rohde, K., & Clough, K. A. (1999) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.1999.tb01918.x · Cited by 745 · see citing works
Hohmann-Marriott, M. F., & Blankenship, R. E. (2011) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042110-103811 · Cited by 744 · see citing works
Early Archean (3.3-Billion to 3.5-Billion-Year-Old) Microfossils from Warrawoona Group, Australia
Schopf, J. W., & Packer, B. M. (1987) · Science · doi:10.1126/science.11539686 · Cited by 655 · see citing works
Atmospheric oxygenation three billion years ago
Crowe, S. A., Døssing, L. N., Beukes, N. J., Bau, M., Kruger, S. J., Frei, R., & Canfield, D. E. (2013) · Nature · doi:10.1038/nature12426 · Cited by 640 · see citing works
Photosynthetic microbial mats in the 3,416-Myr-old ocean
Tice, M. M., & Lowe, D. R. (2004) · Nature · doi:10.1038/nature02888 · Cited by 545 · see citing works
Origin and early evolution of photosynthesis
Blankenship, R. E. (1992) · Photosynthesis Research · doi:10.1007/bf00039173 · Cited by 505 · see citing works
Oceanic Euxinia in Earth History: Causes and Consequences
Meyer, K. M., & Kump, L. R. (2008) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.36.031207.124256 · Cited by 475 · see citing works
Morphological and ecological complexity in early eukaryotic ecosystems
Javaux, E. J., Knoll, A. H., & Walter, M. R. (2001) · Nature · doi:10.1038/35083562 · Cited by 418 · see citing works
Rienzi, S. C. D., Sharon, I., Wrighton, K. C., Koren, O., Hug, L. A., Thomas, B. C., Goodrich, J. K., Bell, J. T., Spector, T. D., Banfield, J. F., et al. (2013) · eLife · doi:10.7554/elife.01102 · Cited by 404 · see citing works
Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago
Kump, L. R., & Barley, M. E. (2007) · Nature · doi:10.1038/nature06058 · Cited by 403 · see citing works
On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria
Soo, R. M., Hemp, J., Parks, D. H., Fischer, W. W., & Hugenholtz, P. (2017) · Science · doi:10.1126/science.aal3794 · Cited by 383 · see citing works
Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago
Luo, G., Ono, S., Beukes, N. J., Wang, D. T., Xie, S., & Summons, R. E. (2016) · Science Advances · doi:10.1126/sciadv.1600134 · Cited by 371 · cited 3× · see citing works
“…age of Cyanobacteria is estimated to be younger than GOE (2172 Ma) but the stem age of Cyanobacteria (2892 Ma) allows sufficient time for the evolution of oxygenic photosynthesis within the Cyanobacteria stem lineage prior to the peak of the GOE 2.33 Ma (Luo et al., 2016) (Figure 2, Table S5).”
BackgroundInfluentialEarly Evolution of Photosynthesis
Blankenship, R. E. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.161687 · Cited by 368 · see citing works
Schirrmeister, B. E., de Vos, J. M., Antonelli, A., & Bagheri, H. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209927110 · Cited by 354 · see citing works
A working model of the primitive Earth
Cloud, P. E. (1972) · American Journal of Science · doi:10.2475/ajs.272.6.537 · Cited by 345 · see citing works
Atmospheric oxygenation caused by a change in volcanic degassing pressure
Gaillard, F., Scaillet, B., & Arndt, N. (2011) · Nature · doi:10.1038/nature10460 · Cited by 336 · see citing works
Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age
Johnston, D. T., Wolfe-Simon, F., Pearson, A., & Knoll, A. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909248106 · Cited by 329 · see citing works
Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils
Schirrmeister, B. E., Gugger, M., & Donoghue, P. C. J. (2015) · Palaeontology · doi:10.1111/pala.12178 · Cited by 304 · cited 3× · see citing works
“Although several molecular clocks have been generated for Cyanobacteria (Dvořák et al., 2014; Falcón et al., 2010; SánchezBaracaldo, 2015; Schirrmeister et al., 2013, 2015; Shih et al., 2017), large differences in outgroup, root prior, and internal calibration selection in these models have…”
BackgroundMethodBLANK, C. E., & SÁNCHEZ‐BARACALDO, P. (2010) · Geobiology · doi:10.1111/j.1472-4669.2009.00220.x · Cited by 298 · see citing works
Ecology of Phototrophic Sulfur Bacteria
van Gemerden, H., & Mas, J. (1995) · Advances in photosynthesis and respiration · doi:10.1007/0-306-47954-0_4 · Cited by 271 · see citing works
Photoferrotrophs thrive in an Archean Ocean analogue
Crowe, S. A., Jones, C., Katsev, S., Magen, C., O'Neill, A. H., Sturm, A., Canfield, D. E., Haffner, G. D., Mucci, A., Sundby, B., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805313105 · Cited by 264 · see citing works
Brocks, J. J., & Schaeffer, P. (2007) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2007.12.006 · Cited by 260 · see citing works
Exploring uncertainty in the calibration of the molecular clock
Warnock, R. C. M., Yang, Z., & Donoghue, P. C. J. (2012) · Biology Letters · doi:10.1098/rsbl.2011.0710 · Cited by 238 · see citing works
Prokaryotic evolution and the tree of life are two different things
Bapteste, E. P., O’Malley, M. A., Beiko, R. G., Ereshefsky, M., Gogarten, J. P., Franklin-Hall, L. R., Lapointe, F., Dupré, J., Dagan, T., Boucher, Y., et al. (2009) · Biology Direct · doi:10.1186/1745-6150-4-34 · Cited by 226 · see citing works
Heising, S., Richter, L., Ludwig, W., & Schink, B. (1999) · Archives of Microbiology · doi:10.1007/s002030050748 · Cited by 218 · see citing works
Fossil calibrations for the arthropod Tree of Life
Wolfe, J. M., Daley, A. C., David, L., & Edgecombe, G. D. (2016) · Earth-Science Reviews · doi:10.1016/j.earscirev.2016.06.008 · Cited by 213 · see citing works
Self-citationBiogenesis and origin of thylakoid membranes
Vothknecht, U. C., & Westhoff, P. (2001) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(01)00153-7 · Cited by 206 · see citing works
Origin of marine planktonic cyanobacteria
Sánchez‐Baracaldo, P. (2015) · Scientific Reports · doi:10.1038/srep17418 · Cited by 201 · see citing works
Szöllősi, G. J., Boussau, B., Abby, S. S., Tannier, É., & Daubin, V. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202997109 · Cited by 194 · see citing works
The Evolution of Photosynthesis
Olson, J. M. (1970) · Science · doi:10.1126/science.168.3930.438 · Cited by 190 · see citing works
Lo, N. C. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg097 · Cited by 187 · see citing works
Allen, J. F., & Martin, W. F. (2007) · Nature · doi:10.1038/445610a · Cited by 178 · see citing works
Crown group Oxyphotobacteria postdate the rise of oxygen
Shih, P. M., Hemp, J., Ward, L. M., Matzke, N. J., & Fischer, W. W. (2016) · Geobiology · doi:10.1111/gbi.12200 · Cited by 173 · see citing works
Horizontal gene transfer constrains the timing of methanogen evolution
Wolfe, J. M., & Fournier, G. P. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0513-7 · Cited by 160 · see citing works
Self-citationDating the cyanobacterial ancestor of the chloroplast
Falcón, L. I., Magallón, S., & Castillo, A. (2010) · The ISME Journal · doi:10.1038/ismej.2010.2 · Cited by 159 · see citing works
Cyanobacterial evolution during the Precambrian
Schirrmeister, B. E., Sánchez‐Baracaldo, P., & Wacey, D. (2016) · International Journal of Astrobiology · doi:10.1017/s1473550415000579 · Cited by 158 · see citing works
Cavalier‐Smith, T. (2001) · Journal of Molecular Evolution · doi:10.1007/s002390010245 · Cited by 156 · see citing works
Tice, M. M., & Lowe, D. R. (2006) · Earth-Science Reviews · doi:10.1016/j.earscirev.2006.03.003 · Cited by 154 · see citing works
Microfossils from the Middle Proterozoic Dismal Lakes Groups, Arctic Canada
Horodyski, R. J., & Donaldson, J. A. (1980) · Precambrian Research · doi:10.1016/0301-9268(80)90043-1 · Cited by 137 · see citing works
Culver, D. A., & Brunskill, G. J. (1969) · Limnology and Oceanography · doi:10.4319/lo.1969.14.6.0862 · Cited by 119 · see citing works
A fresh look at the evolution and diversification of photochemical reaction centers
Cardona, T. (2014) · Photosynthesis Research · doi:10.1007/s11120-014-0065-x · Cited by 106 · see citing works
Synechococcus: 3 billion years of global dominance
Dvořák, P., Casamatta, D. A., Poulíčková, A., Hašler, P., Ondřej, V., & Sanges, R. (2014) · Molecular Ecology · doi:10.1111/mec.12948 · Cited by 102 · see citing works
Sousa, F. L., Shavit-Grievink, L., Allen, J. F., & Martin, W. F. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evs127 · Cited by 95 · see citing works
Evolution of Reaction Centers in Photosynthetic Prokaryotes
Olson, J. M., & Pierson, B. K. (1987) · International review of cytology · doi:10.1016/s0074-7696(08)61439-4 · Cited by 91 · see citing works
Compared structure of plant and bacterial photosynthetic reaction centers. Evolutionary implications
Mathis, P. (1990) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(90)90240-5 · Cited by 70 · see citing works
Origin and evolution of photosynthetic reaction centers
Olson, J. M., & Pierson, B. K. (1987) · Origins of Life and Evolution of Biospheres · doi:10.1007/bf02386479 · Cited by 65 · see citing works
Comparison of Photosynthesis Gene Clusters Retrieved from Total Genome Sequences of Purple Bacteria
Nagashima, S., & Nagashima, K. V. P. (2013) · Advances in botanical research · doi:10.1016/b978-0-12-397923-0.00005-9 · Cited by 38 · see citing works
Ancient Gene Transfer as a Tool in Phylogenetic Reconstruction
Huang, J., & Gogarten, J. P. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-853-9_7 · Cited by 22 · see citing works
Properties and Evolutionary Implications of the Heliobacterial Genome
Sattley, W. M., & Swingley, W. D. (2013) · Advances in botanical research · doi:10.1016/b978-0-12-397923-0.00003-5 · Cited by 15 · see citing works
Small-sized akinetes from the Mesoproterozoic Salkhan Limestone, Semri Group, Bihar, India
Шарма, М. (2006) · Journal of the Palaeontological Society of India · doi:10.1177/0971102320060209 · Cited by 12 · see citing works
Horizontal Gene Transfer Constrains the Timing of Methanogen EvolutionPreprint
Wolfe, J. M., & Fournier, G. P. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/129494 · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Cardona, T., Sanchez‐Baracaldo, P., Rutherford, A. W., & Larkum, A. (2017). Molecular evidence for the early evolution of photosynthetic water oxidation. bioRxiv, 109447 https://doi.org/10.1101/109447 · DOI
Cited by
Sorted by citations
Catling, D. C., & Zahnle, K. J. (2020) · Science Advances · doi:10.1126/sciadv.aax1420 · Cited by 568 · see citing works
Cyanobacteria and biogeochemical cycles through Earth history
Sánchez-Baracaldo, P., Bianchini, G., Wilson, J. D., & Knoll, A. H. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2021.05.008 · Cited by 279 · see citing works
Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview
Lyons, T. W., Diamond, C. W., Planavsky, N. J., Reinhard, C. T., & Li, C. (2021) · Astrobiology · doi:10.1089/ast.2020.2418 · Cited by 211 · see citing works
“, 2007) and geochemical archives of environmental change (Dupont et al., 2006; Magnabosco et al., 2018) have and will continue to yield essential fruit.”
BackgroundEarly Archean origin of Photosystem <scp>II</scp>
Cardona, T., Sánchez‐Baracaldo, P., Rutherford, A. W., & Larkum, A. W. (2019) · Geobiology · doi:10.1111/gbi.12322 · Cited by 144 · see citing works
Parsons, C., Stüeken, E. E., Rosen, C. J., Mateos, K., & Anderson, R. E. (2021) · Geobiology · doi:10.1111/gbi.12419 · Cited by 91 · see citing works
The Evolution and Evolvability of Photosystem II
Oliver, T., Kim, T. D., Trinugroho, J. P., Cordón-Preciado, V., Wijayatilake, N., Bhatia, A., Rutherford, A. W., & Cardona, T. (2023) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-070522-062509 · Cited by 52 · see citing works
The evolution and spread of sulfur cycling enzymes reflect the redox state of the early Earth
Mateos, K., Chappell, G., Klos, A., Le, B., Boden, J., Stüeken, E., & Anderson, R. (2023) · Science Advances · doi:10.1126/sciadv.ade4847 · Cited by 43 · see citing works
Relative Time Constraints Improve Molecular Dating
Szöllõsi, G. J., Höhna, S., Williams, T. A., Schrempf, D., Daubin, V., & Boussau, B. (2022) · Systematic Biology · doi:10.1093/sysbio/syab084 · Cited by 23 · see citing works
- Authors
- Magnabosco, C., Moore, K. R., Wolfe, J. M., & Fournier, G. P.
- Affiliations
- Simons Foundation (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Magnabosco, C.
- Venue
- Geobiology
- Publisher
- Wiley
- Published
- 2018-01-31
- Volume
- 16
- Issue
- 2
- Pages
- 179-189
- ISSN
- 1472-4669 (ISSN-L)
- 1472-4677
- PMC
- PMC5873394
- OpenAlex
- W2791650506
- Cited by
- 83
- References
- 64
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 6 · 2023: 9 · 2022: 9 · 2021: 13 · 2020: 10 · 2019: 17 · 2018: 9
- FWCI
- 4.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Geobiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- Wiley eBooks
- ETH Zürich Research Collection (cc-by)
- Funders
- Simons Foundation (339603)
- National Science Foundation (EAR‐1615426)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- phototrophic bacteria, cyanobacteria, green sulfur bacteria, horizontal gene transfer, molecular clock, divergence time estimation, photosystem I, photosystem II, Great Oxidation Event, banded iron formations, reaction center, anoxygenic photosynthesis
- MeSH terms
- Cyanobacteria, Evolution, Molecular, Chlorobi, Gene Transfer, Horizontal, Chloroflexi, Phototrophic Processes, Metabolic Networks and Pathways
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