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Photosynthesis on exoplanets and exomoons from reflected light

Published online by Cambridge University Press:  31 October 2019

Manasvi Lingam*
Affiliation:
Institute for Theory and Computation, Harvard University, 60 Garden St, Cambridge, MA02138, USA Department of Aerospace, Physics and Space Sciences, Florida Institute of Technology, 150 W University Blvd, Melbourne, FL32901, USA
Abraham Loeb
Affiliation:
Department of Aerospace, Physics and Space Sciences, Florida Institute of Technology, 150 W University Blvd, Melbourne, FL32901, USA
*
Author for correspondence: Manasv Lingam, E-mail:manasvi.lingam@cfa.harvard.edu

Abstract

Photosynthesis offers a convenient means of sustaining biospheres. We quantify the constraints for photosynthesis to be functional on the permanent nightside of tidally locked rocky exoplanets via reflected light from their exomoons. We show that the exomoons must be at least half the size of Earth's moon in order for conventional oxygenic photosynthesis to operate. This scenario of photosynthesis is unlikely for exoplanets around late-type M-dwarfs due to the low likelihood of large exomoons and their orbital instability over long timescales. Subsequently, we investigate the prospects for photosynthesis on habitable exomoons via reflected light from the giant planets that they orbit. Our analysis indicates that such photosynthetic biospheres are potentially sustainable on these moons except those around late-type M-dwarfs. We conclude our analysis by delineating certain physiological and biochemical features of photosynthesis and other carbon fixation pathways, and the likelihood of their evolution on habitable planets and moons.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019

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References

Anglada-Escudé, G, Amado, PJ, Barnes, J, Berdiñas, ZM, Butler, RP, Coleman, GAL, de La Cueva, I, Dreizler, S, Endl, M, Giesers, B, Jeffers, SV, Jenkins, JS, Jones, HRA, Kiraga, M, Kürster, M, López-González, MJ, Marvin, CJ, Morales, N, Morin, J, Nelson, RP, Ortiz, JL, Ofir, A, Paardekooper, S-J, Reiners, A, Rodríguez, E, Rodríguez-López, C, Sarmiento, LF, Strachan, JP, Tsapras, Y, Tuomi, M and Zechmeister, M (2016) A terrestrial planet candidate in a temperate orbit around Proxima Centauri. Nature 536, 437440.CrossRefGoogle Scholar
Bains, W, Seager, S and Zsom, A (2014) Photosynthesis in Hydrogen-Dominated Atmospheres. Life 4, 716744.CrossRefGoogle ScholarPubMed
Bar-Even, A, Flamholz, A, Noor, E and Milo, R (2012) Thermodynamic constraints shape the structure of carbon fixation pathways. Biochimica et Biophysica Acta - Bioenergetics 1817, 16461659.CrossRefGoogle ScholarPubMed
Bar-On, YM, Phillips, R and Milo, R (2018) The biomass distribution on Earth. Proceedings of the National Academy of Sciences of the United States of America 115, 65066511.10.1073/pnas.1711842115CrossRefGoogle ScholarPubMed
Barnes, R (2017) Tidal locking of habitable exoplanets. Celestial Mechanics and Dynamical Astronomy 129, 509536.CrossRefGoogle Scholar
Batalha, NM, Rowe, JF, Bryson, ST, Barclay, T, Burke, CJ, Caldwell, DA, Christiansen, JL, Mullally, F, Thompson, SE, Brown, TM, Dupree, AK, Fabrycky, DC, Ford, EB, Fortney, JJ, Gilliland, RL, Isaacson, H, Latham, DW, Marcy, GW, Quinn, SN, Ragozzine, D, Shporer, A, Borucki, WJ, Ciardi, DR, Gautier, III, TN, Haas, MR, Jenkins, JM, Koch, DG, Lissauer, JJ, Rapin, W, Basri, GS, Boss, AP, Buchhave, LA, Carter, JA, Charbonneau, D, Christensen-Dalsgaard, J, Clarke, BD, Cochran, WD, Demory, B-O, Desert, J-M, Devore, E, Doyle, LR, Esquerdo, GA, Everett, M, Fressin, F, Geary, JC, Girouard, FR, Gould, A, Hall, JR, Holman, MJ, Howard, AW, Howell, SB, Ibrahim, KA, Kinemuchi, K, Kjeldsen, H, Klaus, TC, Li, J, Lucas, PW, Meibom, S, Morris, RL, Prša, A, Quintana, E, Sanderfer, DT, Sasselov, D, Seader, SE, Smith, JC, Steffen, JH, Still, M, Stumpe, MC, Tarter, JC, Tenenbaum, P, Torres, G, Twicken, JD, Uddin, K, Van Cleve, J, Walkowicz, L and Welsh, WF (2013) Planetary candidates observed by Kepler. III. Analysis of the first 16 months of data. Astrophysical Journal Supplement Series 204, 24.CrossRefGoogle Scholar
Beatty, JT, Overmann, J, Lince, MT, Manske, AK, Lang, AS, Blankenship, RE, Van Dover, CL, Martinson, TA and Plumley, FG (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proceedings of the National Academy of Sciences of the United States of America 102, 93069310.CrossRefGoogle ScholarPubMed
Berg, IA (2011) Ecological Aspects of the Distribution of Different Autotrophic CO2 Fixation Pathways. Applied and Environmental Microbiology 77, 19251936.CrossRefGoogle ScholarPubMed
Björn, LO and Govindjee, (2015) The evolution of photosynthesis and its environmental impact. In Björn, LO (ed). Photobiology: The Science of Light and Life. New York: Springer, pp. 207230.CrossRefGoogle Scholar
Blakemore, JD, Crabtree, RH and Brudvig, GW (2015) Molecular catalysts for water oxidation. Chemical Reviews 115, 1297413005.10.1021/acs.chemrev.5b00122CrossRefGoogle ScholarPubMed
Blankenship, RE (2014) Molecular Mechanisms of Photosynthesis. Wiley-Blackwell.Google Scholar
Braakman, R and Smith, E (2012) The emergence and early evolution of biological carbon-fixation. PLoS Computational Biology 8, e1002455.CrossRefGoogle ScholarPubMed
Camprubi, E, Jordan, SF, Vasiliadou, R and Lane, N (2017) Iron catalysis at the origin of life. IUBMB Life 69, 373381.10.1002/iub.1632CrossRefGoogle ScholarPubMed
Cardona, T (2019) Thinking twice about the evolution of photosynthesis. Open Biology 9, 180246.CrossRefGoogle ScholarPubMed
Chen, M and Blankenship, RE (2011) Expanding the solar spectrum used by photosynthesis. Trends in Plant Science 16, 427431.CrossRefGoogle ScholarPubMed
Cnossen, I, Sanz-Forcada, J, Favata, F, Witasse, O, Zegers, T and Arnold, NF (2007) Habitat of early life: solar X-ray and UV radiation at Earth's surface 4-3.5 billion years ago. Journal of Geophysical Research. Planets 112, E02008.Google Scholar
Cockell, CS and Airo, A (2002) On the plausibility of a UV transparent biochemistry. Origins of Life and Evolution of the Biosphere 32, 255274.CrossRefGoogle ScholarPubMed
Cockell, CS, Raven, JA, Kaltenegger, L and Logan, RC (2009) Planetary targets in the search for extrasolar oxygenic photosynthesis. Plant Ecology & Diversity 2, 207219.CrossRefGoogle Scholar
Colwell, FS and D'Hondt, S (2013) Nature and extent of the deep biosphere. Reviews in Mineralogy and Geochemistry 75, 547574.10.2138/rmg.2013.75.17CrossRefGoogle Scholar
Cummings, ME, Bernal, XE, Reynaga, R, Rand, AS and Ryan, MJ (2008) Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females. The Journal of Experimental Biology 211, 12031210.CrossRefGoogle Scholar
DasSarma, S and Schwieterman, EW (2018) Early evolution of purple retinal pigments on Earth and implications for exoplanet biosignatures. International Journal of Astrobiology 110.10.1017/S1473550418000423CrossRefGoogle Scholar
Deamer, DW (1997) The first living systems: a bioenergetic perspective. Microbiology and Molecular Biology Reviews 61, 239261.CrossRefGoogle ScholarPubMed
Dobos, V and Turner, EL (2015) Viscoelastic models of tidally heated exomoons. The Astrophysical Journal 804, 41.10.1088/0004-637X/804/1/41CrossRefGoogle Scholar
Dobos, V, Heller, R and Turner, EL (2017) The effect of multiple heat sources on exomoon habitable zones. Astronomy and Astrophysics 601, A91.CrossRefGoogle Scholar
Dong, C, Lingam, M, Ma, Y and Cohen, O (2017) Is proxima centauri b habitable? A study of atmospheric loss. The Astrophysical Journal. Letters 837, L26.CrossRefGoogle Scholar
Dong, C, Jin, M, Lingam, M, Airapetian, VS, Ma, Y and van der Holst, B (2018) Atmospheric escape from the TRAPPIST-1 planets and implications for habitability. Proceedings of the National Academy of Sciences of the United States of America 115, 260265.10.1073/pnas.1708010115CrossRefGoogle ScholarPubMed
Fischer, WW, Hemp, J and Johnson, JE (2016) Evolution of oxygenic photosynthesis. Annual Review of Earth and Planetary Sciences 44, 647683.CrossRefGoogle Scholar
Forgan, D and Dobos, V (2016) Exomoon climate models with the carbonate-silicate cycle and viscoelastic tidal heating. Monthly Notices of the Royal Astronomical Society 457, 12331241.CrossRefGoogle Scholar
Forgan, DH, Mead, A, Cockell, CS and Raven, JA (2015) Surface flux patterns on planets in circumbinary systems and potential for photosynthesis. International Journal of Astrobiology 14, 465478.CrossRefGoogle Scholar
Fuchs, G (2011) Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annual Review of Microbiology 65, 631658.CrossRefGoogle ScholarPubMed
Gillon, M, Triaud, AHMJ, Demory, B-O, Jehin, E, Agol, E, Deck, KM, Lederer, SM, de Wit, J, Burdanov, A, Ingalls, JG, Bolmont, E, Leconte, J, Raymond, SN, Selsis, F, Turbet, M, Barkaoui, K, Burgasser, A, Burleigh, MR, Carey, SJ, Chaushev, A, Copperwheat, CM, Delrez, L, Fernandes, CS, Holdsworth, DL, Kotze, EJ, Van Grootel, V, Almleaky, Y, Benkhaldoun, Z, Magain, P and Queloz, D (2017) Seven temperate terrestrial planets around the nearby ultracool dwarf star TRAPPIST-1. Nature 542, 456460.10.1038/nature21360CrossRefGoogle ScholarPubMed
Gorbunov, MY and Falkowski, PG (2002) Photoreceptors in the cnidarian hosts allow symbiotic corals to sense blue moonlight. Limnology and Oceanography 47, 309315.10.4319/lo.2002.47.1.0309CrossRefGoogle Scholar
Haas, JR (2010) The potential feasibility of chlorinic photosynthesis on exoplanets. Astrobiology 10, 953963.CrossRefGoogle ScholarPubMed
Heath, MJ, Doyle, LR, Joshi, MM and Haberle, RM (1999) Habitability of planets around red dwarf stars. Origins of Life and Evolution of the Biosphere 29, 405424.CrossRefGoogle ScholarPubMed
Heller, R (2012) Exomoon habitability constrained by energy flux and orbital stability. Astronomy and Astrophysics 545, L8.10.1051/0004-6361/201220003CrossRefGoogle Scholar
Heller, R and Barnes, R (2015) Runaway greenhouse effect on exomoons due to irradiation from hot, young giant planets. International Journal of Astrobiology 14, 335343.CrossRefGoogle Scholar
Heller, R, Williams, D, Kipping, D, Limbach, MA, Turner, E, Greenberg, R, Sasaki, T, Bolmont, É, Grasset, O, Lewis, K, Barnes, R and Zuluaga, JI (2014) Formation, habitability, and detection of extrasolar moons. Astrobiology 14, 798835.10.1089/ast.2014.1147CrossRefGoogle ScholarPubMed
Hill, R and Bendall, F (1960) Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature 186, 136137.10.1038/186136a0CrossRefGoogle Scholar
Hill, R and Rich, PR (1983) A physical interpretation for the natural photosynthetic process. Proceedings of the National Academy of Sciences of the United States of America 80, 978982.CrossRefGoogle ScholarPubMed
Hohmann-Marriott, MF and Blankenship, RE (2011) Evolution of photosynthesis. Annual Review of Plant Biology 62, 515548.CrossRefGoogle ScholarPubMed
Hügler, M and Sievert, SM (2011) Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annual Review of Marine Science 3, 261289.CrossRefGoogle ScholarPubMed
Johnsen, S, Kelber, A, Warrant, E, Sweeney, AM, Widder, EA, Lee, RL and Hernandez-Andres, J (2006) Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. The Journal of Experimental Biology 209, 789800.CrossRefGoogle ScholarPubMed
Kane, SR (2017) Worlds without moons: exomoon constraints for compact planetary systems. The Astrophysical Journal. Letters 839, L19.10.3847/2041-8213/aa6bf2CrossRefGoogle Scholar
Kasting, JF, Whitmire, DP and Reynolds, RT (1993) Habitable zones around main sequence stars. Icarus 101, 108128.CrossRefGoogle ScholarPubMed
Kiang, NY, Segura, A, Tinetti, G, Govindjee, , Blankenship, RE, Cohen, M, Siefert, J, Crisp, D and Meadows, VS (2007a) Spectral signatures of photosynthesis. II. Coevolution with other stars and the atmosphere on extrasolar worlds. Astrobiology 7, 252274.CrossRefGoogle Scholar
Kiang, NY, Siefert, J, Govindjee, and Blankenship, RE (2007b) Spectral signatures of photosynthesis. I. Review of earth organisms. Astrobiology 7, 222251.CrossRefGoogle Scholar
Knoll, AH (2015) Life on a Young Planet: The First Three Billion Years of Evolution on Earth. Princeton Science Library. Princeton: Princeton University Press.CrossRefGoogle Scholar
Kreidberg, L, Luger, R and Bedell, M (2019) No evidence for lunar transit in new analysis of hubble space telescope observations of the Kepler-1625 system. The Astrophysical Journal. Letters 877, L15.CrossRefGoogle Scholar
Lehmer, OR, Catling, DC, Parenteau, MN and Hoehler, TM (2018) The productivity of oxygenic photosynthesis around cool, M Dwarf stars. The Astrophysical Journal 859, 171.10.3847/1538-4357/aac104CrossRefGoogle Scholar
Li, J, Güttinger, R, Moré, R, Song, F, Wan, W and Patzke, GR (2017) Frontiers of water oxidation: the quest for true catalysts. Chemical Society Reviews 46, 61246147.CrossRefGoogle ScholarPubMed
Lingam, M and Loeb, A (2018a) Is life most likely around Sun-like stars? Journal of Cosmology and Astroparticle Physics 5, 020.CrossRefGoogle Scholar
Lingam, M and Loeb, A (2018b) Optimal target stars in the search for life. The Astrophysical Journal. Letters 857, L17.CrossRefGoogle Scholar
Lingam, M and Loeb, A (2018c) Physical constraints on the likelihood of life on exoplanets. International Journal of Astrobiology 17, 116126.CrossRefGoogle Scholar
Lingam, M and Loeb, A (2019a) Brown Dwarf atmospheres as the potentially most detectable and abundant sites for life. The Astrophysical Journal (arXiv:1905.11410).CrossRefGoogle Scholar
Lingam, M and Loeb, A (2019b) Colloquium: physical constraints for the evolution of life on exoplanets. Reviews of Modern Physics 91, 021002.CrossRefGoogle Scholar
Lingam, M and Loeb, A (2019c) Dependence of biological activity on the surface water fraction of planets. The Astronomical Journal 157, 25.10.3847/1538-3881/aaf420CrossRefGoogle Scholar
Lingam, M and Loeb, A (2019d) Photosynthesis on habitable planets around low-mass stars. Monthly Notices of the Royal Astronomical Society 485, 59245928.CrossRefGoogle Scholar
Martin, W and Russell, MJ (2006) On the origin of biochemistry at an alkaline hydrothermal vent. Philosophical Transactions of the Royal Society B 362, 18871926.CrossRefGoogle Scholar
Martin, WF, Bryant, DA and Beatty, JT (2017) A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiology Reviews 42, 205231.CrossRefGoogle Scholar
Meadows, VS, Reinhard, CT, Arney, GN, Parenteau, MN, Schwieterman, EW, Domagal-Goldman, SD, Lincowski, AP, Stapelfeldt, KR, Rauer, H, DasSarma, S, Hegde, S, Narita, N, Deitrick, R, Lustig-Yaeger, J, Lyons, TW, Siegler, N and Grenfell, JL (2018) Exoplanet biosignatures: understanding oxygen as a biosignature in the context of its environment. Astrobiology 18, 630662.CrossRefGoogle ScholarPubMed
Muchowska, KB, Varma, SJ, Chevallot-Beroux, E, Lethuillier-Karl, L, Li, G and Moran, J (2017) Metals promote sequences of the reverse Krebs cycle. Nature Ecology and Evolution 1, 17161721.CrossRefGoogle ScholarPubMed
Muchowska, KB, Varma, SJ and Moran, J (2019) Synthesis and breakdown of universal metabolic precursors promoted by iron. Nature 569, 104107.10.1038/s41586-019-1151-1CrossRefGoogle ScholarPubMed
Murray, CD and Dermott, SF (1999) Solar System Dynamics. Cambridge, UK: Cambridge University Press.Google Scholar
Nelson, N and Junge, W (2015) Structure and energy transfer in photosystems of oxygenic photosynthesis. Annual Review of Biochemistry 84, 659683.CrossRefGoogle ScholarPubMed
Nisbet, EG, Cann, JR, Lee, C and Dover, V (1995) Origins of photosynthesis. Nature 373, 479480.CrossRefGoogle Scholar
Nunoura, T, Chikaraishi, Y, Izaki, R, Suwa, T, Sato, T, Harada, T, Mori, K, Kato, Y, Miyazaki, M, Shimamura, S, Yanagawa, K, Shuto, A, Ohkouchi, N, Fujita, N, Takaki, Y, Atomi, H and Takai, K (2018) A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile. Science 359, 559563.10.1126/science.aao3407CrossRefGoogle Scholar
Nürnberg, DJ, Morton, J, Santabarbara, S, Telfer, A, Joliot, P, Antonaru, LA, Ruban, AV, Cardona, T, Krausz, E, Boussac, A, Fantuzzi, A and Rutherford, AW (2018) Photochemistry beyond the red limit in chlorophyll f-containing photosystems. Science 360, 12101213.CrossRefGoogle ScholarPubMed
O'Malley-James, JT, Raven, JA, Cockell, CS and Greaves, JS (2012) Life and light: exotic photosynthesis in binary and multiple-star systems. Astrobiology 12, 115124.CrossRefGoogle ScholarPubMed
Pietrocola, F, Galluzzi, L, Bravo-San Pedro, JM, Made, F and Kroemer, G (2015) Acetyl coenzyme a: a central metabolite and second messenger. Cell Metabolism 21, 805821.CrossRefGoogle ScholarPubMed
Piro, AL (2018) Exoplanets torqued by the combined tides of a moon and parent star. The Astronomical Journal 156, 54.CrossRefGoogle Scholar
Pollard, WG (1979) The prevalence of earthlike planets. American Scientist 67, 653659.Google Scholar
Ragsdale, SW and Pierce, E (2008) Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation. Biochimica et Biophysica Acta - Proteins and Proteomics 1784, 18731898.CrossRefGoogle Scholar
Ramirez, RM (2018) A more comprehensive habitable zone for finding life on other planets. Geosciences 8, 280.CrossRefGoogle Scholar
Rappaport, F, Guergova-Kuras, M, Nixon, PJ, Diner, BA and Lavergne, J (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41, 85188527.CrossRefGoogle ScholarPubMed
Raven, JA and Cockell, C (2006) Influence on photosynthesis of starlight, moonlight, planetlight, and light pollution (reflections on photosynthetically active radiation in the universe). Astrobiology 6, 668675.10.1089/ast.2006.6.668CrossRefGoogle Scholar
Raven, JA and Donnelly, S (2013) Brown Dwarfs and black smokers: the potential for photosynthesis using radiation from low-temperature black bodies. In de Vera, J-P and Seckbach, J (eds). Habitability of Other Planets and Satellites. New York: Springer, pp. 267284.CrossRefGoogle Scholar
Raven, JA, Kübler, JE and Beardall, J (2000) Put out the light, and then put out the light. Journal of the Marine Biological Association of the United Kingdom 80, 125.CrossRefGoogle Scholar
Ritchie, RJ, Larkum, AWD and Ribas, I (2018) Could photosynthesis function on Proxima Centauri b? International Journal of Astrobiology 17, 147176.10.1017/S1473550417000167CrossRefGoogle Scholar
Sasaki, T and Barnes, JW (2014) Longevity of moons around habitable planets. International Journal of Astrobiology 13, 324336.CrossRefGoogle Scholar
Schoepp-Cothenet, B, Van Lis, R, Atteia, A, Baymann, F, Capowiez, L, Ducluzeau, A-L, Duval, S, Ten Brink, F, Russell, MJ and Nitschke, W (2013) On the universal core of bioenergetics. Biochimica et Biophysica Acta - Bioenergetics 1827, 7993.CrossRefGoogle ScholarPubMed
Schwander, T, Schada von Borzyskowski, L, Burgener, S, Cortina, NS and Erb, TJ (2016) A synthetic pathway for the fixation of carbon dioxide in vitro. Science 354, 900904.10.1126/science.aah5237CrossRefGoogle ScholarPubMed
Schwieterman, EW, Kiang, NY, Parenteau, MN, Harman, CE, DasSarma, S, Fisher, TM, Arney, GN, Hartnett, HE, Reinhard, CT, Olson, SL, Meadows, VS, Cockell, CS, Walker, SI, Grenfell, JL, Hegde, S, Rugheimer, S, Hu, R and Lyons, TW (2018) Exoplanet biosignatures: a review of remotely detectable signs of life. Astrobiology 18, 663708.CrossRefGoogle ScholarPubMed
Seager, S, Turner, EL, Schafer, J and Ford, EB (2005) Vegetation's red edge: a possible spectroscopic biosignature of extraterrestrial plants. Astrobiology 5, 372390.CrossRefGoogle ScholarPubMed
Smith, E and Morowitz, HJ (2016) The Origin and Nature of Life on Earth: The Emergence of the Fourth Geosphere. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Suen, N-T, Hung, S-F, Quan, Q, Zhang, N, Xu, Y-J and Chen, HM (2017) Electrocatalysis for the oxygen evolution reaction: recent development and future perspectives. Chemical Society Reviews 46, 337365.CrossRefGoogle ScholarPubMed
Teachey, A and Kipping, DM (2018) Evidence for a large exomoon orbiting Kepler-1625b. Science Advances 4, eaav1784.CrossRefGoogle ScholarPubMed
Unterborn, CT, Desch, SJ, Hinkel, NR and Lorenzo, A (2018) Inward migration of the TRAPPIST-1 planets as inferred from their water-rich compositions. Nature Astronomy 2, 297302.CrossRefGoogle Scholar
Varma, SJ, Muchowska, KB, Chatelain, P and Moran, J (2018) Native iron reduces CO2 to intermediates and end-products of the acetyl-CoA pathway. Nature Ecology and Evolution 2, 10191024.CrossRefGoogle ScholarPubMed
Venturini, J and Helled, R (2017) The formation of mini-neptunes. The Astrophysical Journal 848, 95.CrossRefGoogle Scholar
Vinyard, DJ, Ananyev, GM and Dismukes, GC (2013) Photosystem II: the reaction center of oxygenic photosynthesis. Annual Review of Biochemistry 82, 577606.10.1146/annurev-biochem-070511-100425CrossRefGoogle ScholarPubMed
Ward, LM and Shih, PM (2019) The evolution and productivity of carbon fixation pathways in response to changes in oxygen concentration over geological time. Free Radical Biology & Medicine. DOI: 10.1016/j.freeradbiomed.2019.01.049.CrossRefGoogle ScholarPubMed
Ward, LM, Rasmussen, B and Fischer, WW (2019) Primary productivity was limited by electron donors prior to the advent of oxygenic photosynthesis. Journal of Geophysical Research. Biogeosciences 124, 211226.CrossRefGoogle Scholar
Weiss, MC, Preiner, M, Xavier, JC, Zimorski, V and Martin, WF (2018) The last universal common ancestor between ancient Earth chemistry and the onset of genetics. PLoS Genetics 14, e1007518.CrossRefGoogle ScholarPubMed
Wiechen, M, Najafpour, MM, Allakhverdiev, SI and Spiccia, L (2014) Water oxidation catalysis by manganese oxides: learning from evolution. Energy & Environmental Science 7, 22032212.CrossRefGoogle Scholar
Williams, DM, Kasting, JF and Wade, RA (1997) Habitable moons around extrasolar giant planets. Nature 385, 234236.CrossRefGoogle ScholarPubMed
Winn, JN and Fabrycky, DC (2015) The occurrence and architecture of exoplanetary systems. Annual Review of Astronomy and Astrophysics 53, 409447.CrossRefGoogle Scholar
Wolstencroft, RD and Raven, JA (2002) Photosynthesis: likelihood of occurrence and possibility of detection on earth-like planets. Icarus 157, 535548.CrossRefGoogle Scholar
Zhang, B and Sun, L (2019) Artificial photosynthesis: opportunities and challenges of molecular catalysts. Chemical Society Reviews 48, 22162264.CrossRefGoogle ScholarPubMed
Zollinger, RR, Armstrong, JC and Heller, R (2017) Exomoon habitability and tidal evolution in low-mass star systems. Monthly Notices of the Royal Astronomical Society 472, 825.CrossRefGoogle Scholar