Electrons, life and the evolution of Earth's oxygen cycle

Falkowski, Paul G; Godfrey, Linda V

doi:10.1098/rstb.2008.0054

Cited by 144Paleontology and Stratigraphy of FossilsEarth Systems and Cosmic EvolutionOrigins and Evolution of Life

Electrons, life and the evolution of Earth's oxygen cycle

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Falkowski, Paul G, Godfrey, Linda V·2008·Philosophical Transactions of the Royal Society B: Biological Sciences

DOI 10.1098/rstb.2008.0054PMC PMC2606772

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Abstract

The biogeochemical cycles of H, C, N, O and S are coupled via biologically catalysed electron transfer (redox) reactions. The metabolic processes responsible for maintaining these cycles evolved over the first ca 2.3 Ga of Earth's history in prokaryotes and, through a sequence of events, led to the production of oxygen via the photobiologically catalysed oxidation of water. However, geochemical evidence suggests that there was a delay of several hundred million years before oxygen accumulated in Earth's atmosphere related to changes in the burial efficiency of organic matter and fundamental alterations in the nitrogen cycle. In the latter case, the presence of free molecular oxygen allowed ammonium to be oxidized to nitrate and subsequently denitrified. The interaction between the oxygen and nitrogen cycles in particular led to a negative feedback, in which increased production of oxygen led to decreased fixed inorganic nitrogen in the oceans. This feedback, which is supported by isotopic analyses of fixed nitrogen in sedimentary rocks from the Late Archaean, continues to the present. However, once sufficient oxygen accumulated in Earth's atmosphere to allow nitrification to out-compete denitrification, a new stable electron 'market' emerged in which oxygenic photosynthesis and aerobic respiration ultimately spread via endosymbiotic events and massive lateral gene transfer to eukaryotic host cells, allowing the evolution of complex (i.e. animal) life forms. The resulting network of electron transfers led a gas composition of Earth's atmosphere that is far from thermodynamic equilibrium (i.e. it is an emergent property), yet is relatively stable on geological time scales. The early coevolution of the C, N and O cycles, and the resulting non-equilibrium gaseous by-products can be used as a guide to search for the presence of life on terrestrial planets outside of our Solar System.

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The rise of atmospheric O2 during the Great Oxidation Event at 2.4 Ga enabled the production of nitrate through the microbial process of nitrification.
“The rise of atmospheric O2 during the Great Oxidation Event at 2.4 Ga enabled the production of nitrate (NO3−) through the microbial process of nitrification (the oxidation of NH4+ to NO3−) (Falkowski and Godfrey, 2008).”
From The Astrobiology Primer v2.0 (2016) · cites this paper as Falkowski and Godfrey, 2008

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Self-citation
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Biogeochemical Cycles
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Self-citation
Using the multiple isotopes of sulfur to constrain microbial processes in the Proterozoic ocean
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Missing the biotech boat
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3 of the 115 references couldn’t be matched to a known paper.

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The Microbial Engines That Drive Earth's Biogeochemical Cycles
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Self-citation
The Evolution and Future of Earth’s Nitrogen Cycle
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Oxidative Stress in Neurodegenerative Diseases
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Oxidative Stress in Neurodegenerative Diseases
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Evolution of Photosynthesis
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Why the atmosphere became oxygenated: A proposal
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Extreme 15N‐enrichments in 2.72‐Gyr‐old sediments: evidence for a turning point in the nitrogen cycle
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Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment
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The evolution of new enzyme function: lessons from xenobiotic metabolizing bacteria versus insecticide‐resistant insects
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The Astrobiology Primer v2.0
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“4 Ga enabled the production of nitrate (NO3 ) through the microbial process of nitrification (the oxidation of NH4 + to NO3 ) (Falkowski and Godfrey, 2008).”
Influential
Global Proteomics Reveal an Atypical Strategy for Carbon/Nitrogen Assimilation by a Cyanobacterium Under Diverse Environmental Perturbations
Wegener, K. M., Singh, A. K., Jacobs, J., Elvitigala, T. R., Welsh, E. A., Keren, N., Gritsenko, M. A., Ghosh, B. K., Camp, D., Smith, R. D., et al. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.000109 · Cited by 124 · see citing works
Neuroprotective effects of natural compounds on neurotoxin-induced oxidative stress and cell apoptosis
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The Geologic History of Seawater
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The Role of Microbial Electron Transfer in the Coevolution of the Biosphere and Geosphere
Jelen, B. I., Giovannelli, D., & Falkowski, P. G. (2016) · Annual Review of Microbiology · doi:10.1146/annurev-micro-102215-095521 · Cited by 101 · see citing works
Self-citation
Bioactive Compounds of the Mediterranean Diet as Nutritional Support to Fight Neurodegenerative Disease
Franco, G. A., Interdonato, L., Cordaro, M., Cuzzocrea, S., & Paola, R. D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087318 · Cited by 100 · see citing works
Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration
Bernhard, J. M., Casciotti, K. L., McIlvin, M. R., Beaudoin, D., Visscher, P. T., & Edgcomb, V. P. (2012) · Journal of Geophysical Research Atmospheres · doi:10.1029/2012jg001949 · Cited by 93 · see citing works
Radiation of nitrogen‐metabolizing enzymes across the tree of life tracks environmental transitions in Earth history
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
Antioxidant Alternatives in the Treatment of Amyotrophic Lateral Sclerosis: A Comprehensive Review
Carrera‐Juliá, S., Moreno, M. L., Barrios, C., Ortí, J. E. D. L. R., & Drehmer, E. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00063 · Cited by 83 · see citing works
Anoxic photogeochemical oxidation of manganese carbonate yields manganese oxide
Liu, W., Hao, J., Elzinga, E. J., Piotrowiak, P., Nanda, V., Yee, N., & Falkowski, P. G. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002175117 · Cited by 74 · see citing works
Self-citation
Nitrate ammonification by Nautilia profundicola AmH: experimental evidence consistent with a free hydroxylamine intermediate
Hanson, T. E., Campbell, B., Kalis, K. M., Campbell, M., & Klotz, M. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00180 · Cited by 66 · see citing works
Redox control of N:P ratios in aquatic ecosystems
Quan, T. M., & Falkowski, P. G. (2008) · Geobiology · doi:10.1111/j.1472-4669.2008.00182.x · Cited by 74 · see citing works
Self-citation
Oxidative Stress in Neurodegenerative Diseases
Simonian, N. A. (1996) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.36.1.83 · Cited by 74 · see citing works
Major problems in evolutionary transitions: how a metabolic perspective can enrich our understanding of macroevolution
O’Malley, M. A., & Powell, R. (2015) · Biology & Philosophy · doi:10.1007/s10539-015-9513-z · Cited by 72 · see citing works
Fate of rice shoot and root residues, rhizodeposits, and microbial assimilated carbon in paddy soil - part 2: turnover and microbial utilization
Zhu, Z., Ge, T., Hu, Y., Zhou, P., Wang, T., Shibistova, O. B., Guggenberger, G., Su, Y., & Wu, J. (2017) · Plant and Soil · doi:10.1007/s11104-017-3210-4 · Cited by 71 · see citing works
Materials and pathways of the organic carbon cycle through time
Galvez, M. E., Fischer, W. W., Jaccard, S. L., & Eglinton, T. I. (2020) · Nature Geoscience · doi:10.1038/s41561-020-0563-8 · Cited by 72 · see citing works
The Geochemical Record of the Ancient Nitrogen Cycle, Nitrogen Isotopes, and Metal Cofactors
Godfrey, L., & Glass, J. B. (2010) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-381294-0.00022-5 · Cited by 70 · see citing works
Self-citation
The Story of O 2
Falkowski, P. G., & Isozaki, Y. (2008) · Science · doi:10.1126/science.1162641 · Cited by 68 · see citing works
Self-citation
Integrative analysis of large scale expression profiles reveals core transcriptional response and coordination between multiple cellular processes in a cyanobacterium
Singh, A. K., Elvitigala, T. R., Cameron, J. C., Ghosh, B. K., Bhattacharyya‐Pakrasi, M., & Pakrasi, H. B. (2010) · BMC Systems Biology · doi:10.1186/1752-0509-4-105 · Cited by 67 · see citing works
Co-variation of nitrogen isotopes and redox states through glacial–interglacial cycles in the Black Sea
Quan, T. M., Wright, J. D., & Falkowski, P. G. (2013) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2013.02.029 · Cited by 68 · see citing works
Self-citation
An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms
Pamplona, R., & Barja, G. (2011) · Biogerontology · doi:10.1007/s10522-011-9348-1 · Cited by 65 · see citing works
Heme: From quantum spin crossover to oxygen manager of life
Kepp, K. P. (2016) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2016.08.008 · Cited by 64 · see citing works
Evolutionary ecology during the rise of dioxygen in the Earth's atmosphere
Sleep, N. H., & Bird, D. K. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0018 · Cited by 62 · see citing works
How to resurrect ancestral proteins as proxies for ancient biogeochemistry
Garcia, A. K., & Kaçar, B. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.03.033 · Cited by 62 · see citing works
Enhanced biofuel production using optimality, pathway modification and waste minimization
Raven, J. A., & Ralph, P. J. (2014) · Journal of Applied Phycology · doi:10.1007/s10811-014-0323-5 · Cited by 61 · see citing works
Ecological Energetic Perspectives on Responses of Nitrogen-Transforming Chemolithoautotrophic Microbiota to Changes in the Marine Environment
Dang, H., & Chen, C. A. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01246 · Cited by 59 · see citing works
Interactions of photosynthesis with genome size and function
Raven, J. A., Beardall, J., Larkum, A. W. D., & Sánchez‐Baracaldo, P. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0264 · Cited by 57 · see citing works
Impact of metabolism and growth phase on the hydrogen isotopic composition of microbial fatty acids
Heinzelmann, S. M., Villanueva, L., Sinke-Schoen, D., Damsté, J. S. S., Stefan Schouten, A., & van der Meer, M. T. J. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00408 · Cited by 50 · see citing works
Element strategy of oxygen evolution electrocatalysis based on in situ spectroelectrochemistry
Ooka, H., Takashima, T., Yamaguchi, A., Hayashi, T., & Nakamura, R. (2017) · Chemical Communications · doi:10.1039/c7cc02204b · Cited by 50 · see citing works
Role of APS reductase in biogeochemical sulfur isotope fractionation
Sim, M. S., Ogata, H., Lubitz, W., Adkins, J. F., Sessions, A. L., Orphan, V. J., & McGlynn, S. E. (2018) · Nature Communications · doi:10.1038/s41467-018-07878-4 · Cited by 49 · see citing works
Microbial Nitrogen Cycling in Antarctic Soils
Ortiz, M., Bosch, J., Coclet, C., Johnson, J., Lebre, P. H., Salawu-Rotimi, A., Vikram, S., Makhalanyane, T. P., & Cowan, D. A. (2020) · Microorganisms · doi:10.3390/microorganisms8091442 · Cited by 49 · see citing works
Sulfur isotope composition of carbonate-associated sulfate from the Mesoproterozoic Jixian Group, North China: Implications for the marine sulfur cycle
Guo, H., Du, Y., Kah, L. C., Hu, C., Huang, J., Huang, H., Yu, W., & Song, H. (2015) · Precambrian Research · doi:10.1016/j.precamres.2015.05.032 · Cited by 46 · see citing works
Habitability: from stars to cells
Javaux, E., & Dehant, V. (2010) · The Astronomy and Astrophysics Review · doi:10.1007/s00159-010-0030-4 · Cited by 46 · see citing works
How Do Subduction Zones Regulate the Carbon Cycle?
Galvez, M. E., & Pubellier, M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108677950.010 · Cited by 44 · see citing works
Nose-to-Brain Delivery of Antioxidants as a Potential Tool for the Therapy of Neurological Diseases
Bonferoni, M. C., Rassu, G., Gavini, E., Sorrenti, M., Catenacci, L., & Giunchedi, P. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12121246 · Cited by 42 · see citing works
Evolutionary Aspects and Regulation of Tetrapyrrole Biosynthesis in Cyanobacteria under Aerobic and Anaerobic Environments
Fujita, Y., Tsujimoto, R., & Aoki, R. (2015) · Life · doi:10.3390/life5021172 · Cited by 42 · see citing works
Spatiotemporal variations of nitrogen isotopic records in the Arabian Sea
Kao, S. J., Wang, B.-Y., Zheng, L., Selvaraj, K., Hsu, S. C., Wan, X. S., Xu, M., & Chen, C. A. (2015) · Biogeosciences · doi:10.5194/bg-12-1-2015 · Cited by 39 · see citing works
Plant-microbial fuel cells - A bibliometric analysis
Prasad, P. N., & Kalla, S. (2021) · Process Biochemistry · doi:10.1016/j.procbio.2021.10.001 · Cited by 39 · see citing works
Engineered Photosystem II Reaction Centers Optimize Photochemistry versus Photoprotection at Different Solar Intensities
Vinyard, D. J., Gimpel, J. A., Ananyev, G., Mayfield, S. P., & Dismukes, G. C. (2014) · Journal of the American Chemical Society · doi:10.1021/ja5002967 · Cited by 38 · see citing works
Contrasting Microbial Community Assembly Hypotheses: A Reconciling Tale from the Río Tinto
Palacios, C., Zettler, E., Amils, R., & Amaral‐Zettler, L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003853 · Cited by 38 · see citing works
Evolution of Aquatic Photoautotrophs
Raven, J. A. (2022) · doi:10.1002/9781119986782.ch2 · Cited by 36 · see citing works
The Architecture of Thiol Antioxidant Systems among Invertebrate Parasites
Guevara‐Flores, A., Martínez-González, J. D. J., Rendón, J. D. C., & Mena, I. P. D. A. (2017) · Molecules · doi:10.3390/molecules22020259 · Cited by 32 · see citing works
Rubisco, the imperfect winner: it’s all about the base
Badger, M. R., & Sharwood, R. E. (2022) · Journal of Experimental Botany · doi:10.1093/jxb/erac458 · Cited by 29 · see citing works
Geoscience for Understanding Habitability in the Solar System and Beyond
Dehant, V., Debaille, V., Dobos, V., Gaillard, F., Gillmann, C., Goderis, S., Grenfell, J. L., Höning, D., Javaux, E. J., Karatekin, Ö., et al. (2019) · Space Science Reviews · doi:10.1007/s11214-019-0608-8 · Cited by 26 · see citing works
Proton-Coupled Electron Transfer and Tyrosine D of Photosystem II
Jenson, D. L., Evans, A., & Barry, B. A. (2007) · The Journal of Physical Chemistry B · doi:10.1021/jp075726x · Cited by 28 · see citing works
Inhibition of autotrophic nitrifiers in a nitrogen-rich paddy soil by elevated CO2
Zhang, K.-H., Lei, W., Zhang, H., Xu, C.-C., Xiao, J., Li, S., Liang, M.-J., He, J.-P., Lai, Y.-C., Li, R., et al. (2024) · Nature Geoscience · doi:10.1038/s41561-024-01583-2 · Cited by 21 · see citing works
Introduction. Photosynthetic and atmospheric evolution
Bendall, D. S., Howe, C. J., Nisbet, E. G., & Nisbet, R. E. R. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0058 · Cited by 27 · see citing works
Circadian clocks' interactions with oxygen sensing and signalling
Adamovich, Y., Dandavate, V., & Asher, G. (2022) · Acta Physiologica · doi:10.1111/apha.13770 · Cited by 26 · see citing works
The Carbon Cycle: With a Brief Introduction to Global Biogeochemistry
Cole, J. J., Hararuk, O., & Solomon, C. T. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-812762-9.00007-1 · Cited by 25 · see citing works
Magnetic fields and apoptosis: a possible mechanism
Tofani, S. (2022) · Electromagnetic Biology and Medicine · doi:10.1080/15368378.2022.2073547 · Cited by 24 · see citing works
Nitrogen isotope compositions of the Upper Triassic Chang 7 Shale, Ordos Basin, North China: Implications for depositional redox conditions
Chen, R., Liu, G., Shang, F., & Cao, Y. (2019) · Marine and Petroleum Geology · doi:10.1016/j.marpetgeo.2019.06.027 · Cited by 22 · see citing works
Nitrogen isotope signatures of microfossils suggest aerobic metabolism 3.0 Gyr ago
Delarue, F., Robert, F., Sugitani, K., Tartèse, R., Duhamel, R., & Derenne, S. (2018) · Geochemical Perspectives Letters · doi:10.7185/geochemlet.1816 · Cited by 21 · see citing works
Dinitrogenase-Driven Photobiological Hydrogen Production Combats Oxidative Stress in Cyanothece sp. Strain ATCC 51142
Sadler, N., Bernstein, H. C., Melnicki, M. R., Charania, M. A., Hill, E. A., Anderson, L. N., Monroe, M. E., Smith, R. D., Beliaev, A. S., & Wright, A. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.02098-16 · Cited by 20 · see citing works
Theory of the Origin, Evolution, and Nature of Life
Andrulis, E. D. (2011) · Life · doi:10.3390/life2010001 · Cited by 21 · see citing works
The Never-Ending Story-The Origin and Diversification of Life
Kumala, M. (2010) · Evolution Education and Outreach · doi:10.1007/s12052-010-0278-1 · Cited by 20 · see citing works
The Great Oxygenation Event
Ligrone, R. (2019) · Springer eBooks · doi:10.1007/978-3-030-16057-9_5 · Cited by 19 · see citing works
Mastering methodological pitfalls for surviving the metagenomic jungle
Delmont, T. O., Simonet, P., & Vogel, T. M. (2013) · BioEssays · doi:10.1002/bies.201200155 · Cited by 18 · see citing works
The biological and geological contingencies for the rise of oxygen on Earth
Falkowski, P. G. (2010) · Photosynthesis Research · doi:10.1007/s11120-010-9602-4 · Cited by 18 · see citing works
Self-citation
Did natural reactors form as a consequence of the emergence of oxygenic photosynthesis during the Archean?
Coogan, L. A. (2009) · GSA Today · doi:10.1130/gsatg41a.1 · Cited by 18 · see citing works
Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase
Kaur, D., Cai, X., Khaniya, U., Zhang, Y., Mao, J., Mandal, M., & Gunner, M. R. (2019) · Inorganics · doi:10.3390/inorganics7020014 · Cited by 17 · see citing works
Earth Orbit v2.1: a 3-D visualization and analysis model of Earth's orbit, Milankovitch cycles and insolation
Kostadinov, T. S., & Gilb, R. (2014) · Geoscientific model development · doi:10.5194/gmd-7-1051-2014 · Cited by 16 · see citing works
Redox constraints on a Cenozoic imbalance in the organic carbon cycle
Galvez, M. E. (2020) · American Journal of Science · doi:10.2475/10.2020.03 · Cited by 13 · see citing works
The Carbon Cycle
Cole, J. J. (2012) · Elsevier eBooks · doi:10.1016/b978-0-08-091680-4.00006-8 · Cited by 13 · see citing works
Approaches to understanding the ecology and evolution of understudied terrestrial archaeal ammonia-oxidisers
Gubry‐Rangin, C., Williams, W., & Prosser, J. I. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20180018 · Cited by 13 · see citing works
Redox capacity of rocks and sediments by high temperature chalcometric titration
Galvez, M. E., & Jaccard, S. L. (2020) · Chemical Geology · doi:10.1016/j.chemgeo.2020.120016 · Cited by 12 · see citing works
Ecological Perspectives on Soil Microbial Community Involved in Nitrogen Cycling
Shukla, S., Shukla, K., Mishra, A., Jindal, T., Sharma, S. S., Upadhyay, D., & Singh, V. (2021) · Soil biology · doi:10.1007/978-3-030-71206-8_3 · Cited by 12 · see citing works
Oxidative stress and the early coevolution of life and biospheric oxygen
Taverne, Y. J. H. J., Caron, A. M., Diamond, C., Fournier, G. P., & Lyons, T. W. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-818606-0.00005-5 · Cited by 12 · see citing works
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Authors: Falkowski, P. G., & Godfrey, L. V.
Affiliations: Rutgers, The State University of New Jersey (US)
Corresponding author: Falkowski, Paul G
ORCID: Falkowski, Paul G
Godfrey, Linda V
Venue: Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher: The Royal Society
Published: 2008-05-16
Volume: 363
Issue: 1504
Pages: 2705-2716
ISSN: 0962-8436 (ISSN-L)
1471-2970
DOI: 10.1098/rstb.2008.0054
PMC: PMC2606772
OpenAlex: W2115585878
Cited by: 144
References: 115
Citations by year: 2026: 5 · 2025: 7 · 2024: 10 · 2023: 4 · 2022: 8 · 2021: 6 · 2020: 10 · 2019: 10 · 2018: 6 · 2017: 9 · 2016: 7 · 2015: 7 · 2014: 6 · 2013: 6 · 2012: 7
FWCI: 2.21
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations: Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
Physical Sciences › Earth and Planetary Sciences › Atmospheric Science › Earth Systems and Cosmic Evolution
Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
Keywords: oxygen cycle, Great Oxidation Event, biogeochemical cycles, redox reactions, electron transfer, nitrogen cycling, denitrification, nitrification, ammonia oxidation, organic matter burial, oxygenic photosynthesis, aerobic respiration, endosymbiosis, horizontal gene transfer, eukaryotic evolution, atmospheric composition, biosignatures, exoplanet habitability
MeSH terms: Carbon, Electrons, Eukaryotic Cells, Biological Evolution, Microbiology, Models, Biological, Nitrogen, Oxygen, Photosynthesis, Earth, Planet, Feedback, Physiological

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