Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-02T20:47:48.026Z Has data issue: false hasContentIssue false

Assessing the effects of ultraviolet radiation on the photosynthetic potential in Archean marine environments

Published online by Cambridge University Press:  09 September 2016

Dailé Avila-Alonso*
Affiliation:
Planetary Science Laboratory, Department of Physics, Universidad Central ‘Marta Abreu’ de Las Villas, Camajuani Road, 51/2 Km, Postal Code 54830, Santa Clara, Villa Clara, Cuba KERMIT, Department of Mathematical Modelling, Statistics and Bioinformatics, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, 9000 Ghent, Belgium
Jan M. Baetens
Affiliation:
KERMIT, Department of Mathematical Modelling, Statistics and Bioinformatics, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, 9000 Ghent, Belgium
Rolando Cardenas
Affiliation:
Planetary Science Laboratory, Department of Physics, Universidad Central ‘Marta Abreu’ de Las Villas, Camajuani Road, 51/2 Km, Postal Code 54830, Santa Clara, Villa Clara, Cuba
Bernard De Baets
Affiliation:
KERMIT, Department of Mathematical Modelling, Statistics and Bioinformatics, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, 9000 Ghent, Belgium

Abstract

In this work, the photosynthesis model presented by Avila et al. in 2013 is extended and more scenarios inhabited by ancient cyanobacteria are investigated to quantify the effects of ultraviolet (UV) radiation on their photosynthetic potential in marine environments of the Archean eon. We consider ferrous ions as blockers of UV during the Early Archean, while the absorption spectrum of chlorophyll a is used to quantify the fraction of photosynthetically active radiation absorbed by photosynthetic organisms. UV could have induced photoinhibition at the water surface, thereby strongly affecting the species with low light use efficiency. A higher photosynthetic potential in early marine environments was shown than in the Late Archean as a consequence of the attenuation of UVC and UVB by iron ions, which probably played an important role in the protection of ancient free-floating bacteria from high-intensity UV radiation. Photosynthetic organisms in Archean coastal and ocean environments were probably abundant in the first 5 and 25 m of the water column, respectively. However, species with a relatively high efficiency in the use of light could have inhabited ocean waters up to a depth of 200 m and show a Deep Chlorophyll Maximum near 60 m depth. We show that the electromagnetic radiation from the Sun, both UV and visible light, could have determined the vertical distribution of Archean marine photosynthetic organisms.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agardy, T. et al. (2005). Coastal systems. In Ecosystems and Human Well-being: Current State and Trends, ed. Hassan, R., Scholes, R. & Ash, N., pp. 513549. Inland Press, Washington, DC.Google Scholar
ASTMG173–03e1 (2012). Standard tables for reference solar spectral irradiances. http://www.astm.org/Standards/G173.htm Google Scholar
Avila, D., Cardenas, R. & Martin, O. (2013). On the photosynthetic potential in the very early Archean oceans. Orig. Life Evol. Biosph. 43, 6775.Google Scholar
Awramik, S.M. & Sprinkle, J. (1999). Proterozoic stromatolites: the first marine evolutionary biota. Hist. Biol. 13, 241253.CrossRefGoogle Scholar
Bishop, J.L., Louris, S.K., Rogoff, D.A. & Rothschild, L.J. (2006). Nanophase iron oxides as a key ultraviolet sunscreen for ancient photosynthetic microbes. Int. J. Astrobiol. 5, 112.CrossRefGoogle Scholar
Bjerrum, C. & Canfield, D. (2002). Ocean productivity before about 1.9 Gyr ago limited by phosphorus adsorption onto iron oxides. Nature 417(6885), 159162.Google Scholar
Björn, L.O., Papageorgiou, G.C., Blankenship, R.E. & Govindjee (2009). A viewpoint: why chlorophyll a? Photosynth. Res. 99, 8598.Google Scholar
Blankenship, R., Sadekar, S. & Raymond, J. (2007). The evolutionary transition from anoxygenic to oxygenic photosynthesis. In Evolution of Primary Production in the Sea, ed. Falkowski, P. & Knol, A., pp. 2135. Elsevier, Amsterdam.Google Scholar
Blankenship, R.E. (2010). Early evolution of phytosynthesis. Plant Physiol. 154(2), 434438.Google Scholar
Chen, M., Schliep, M., Willows, R.D., Cai, Z.L., Neilan, B.A. & Scheer, H. (2010). A red-shifted chlorophyll. Science 329, 13181319.CrossRefGoogle ScholarPubMed
Chen, M., Li, Y., Birch, D. & Willows, R.D. (2012). A cyanobacterium that contains chlorophyll f-a red-absorbing photopigment. FEBS Lett. 586, 32493254.CrossRefGoogle ScholarPubMed
Chisholm, S.W. (1992). Phytoplankton size. In Primary Productivity and Biogeochemical Cycles in the Sea, ed. Falkowski, P.G. & Woodhead, A.D., pp. 213237. Plenum Press, New York.Google Scholar
Cleaves, H. & Miller, S. (1998). Oceanic protection of prebiotic organic compounds from UV radiation. Proc. Natl. Acad. Sci. USA 95, 72607263.CrossRefGoogle ScholarPubMed
Cockell, C.S. (1998). The biological effects of UV radiation on early earth – a theoretical evaluation. J. Theor. Biol. 193, 719731.Google Scholar
Cockell, C.S. (2000). Ultraviolet radiation and the photobiology of Earth's early oceans. Orig. Life Evol. Biosp. 30, 467499.Google Scholar
Cockell, C.S. (2001). A photobiological history of Earth. In Ecosystems, Evolution, and Ultraviolet Radiation, ed. Cockell, C.S. & Blaustein, A.R., pp. 135. Springer-Verlag, New York.CrossRefGoogle Scholar
Cockell, C.S. (2002). The ultraviolet radiation environment of Earth and Mars: past and present. In Astrobiology the Quest for the Conditions of Life, ed. Horneck, G. & Baumstark-Khan, C., pp. 219232. Springer, New York.Google Scholar
Cockell, C.S. & Knowland, J. (1999). Ultraviolet radiation screening compounds. Biol. Rev. 74, 311345.Google Scholar
Cohen, K., Finney, S., Gibbard, P. & Fan, J. (2013). The ICS international chronostratigraphic chart. Episodes 36, 199204.CrossRefGoogle Scholar
Comar, C. & Zscheile, F. (1941). Spectroscopic analysis of plant extracts for chlorophyll a and b . Plant Physiol. 16, 651653.Google Scholar
Crowe, S.A. et al. (2008). Photoferrotrophs thrive in an Archean Ocean analogue. Proc. Natl. Acad. Sci. USA 105(41), 1593815943.Google Scholar
Cullen, J., Neale, P. & Lesser, M. (1992). Biological weighting function for the inhibition of phytoplankton photosynthesis by ultraviolet radiation. Science 258, 646650.CrossRefGoogle ScholarPubMed
Cullen, J.J., Davis, R.F. & Huot, Y. (2012). Spectral model of depth-integrated water column photosynthesis and its inhibition by ultraviolet radiation. Glob. Biogeochem. Cycles 26, GB1011.CrossRefGoogle Scholar
David, L. & Alm, E. (2011). Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469, 9396.CrossRefGoogle ScholarPubMed
Dillon, J.G. & Castenholz, R.W. (1999). Scytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosynthetic life. J. Phycol. 35, 673681.Google Scholar
Dolan, M.F. & Margulis, L. (2002). Early Life: Evolution on the Prepambrian Earth, 2nd edn. University of Masshachusetts, John and Bartlett Publishers Sudbury, Masshachusetts.Google Scholar
Dufresne, A., Garczarek, L. & Partensky, F. (2005). Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol. 6, R14.Google Scholar
Dvořák, P., Casamatta, D.A., Paulickova, A., Hasler, P., Ondrej, V. & Sanges, R. (2014). Synechococcus: 3 billion years of global dominance. Mol. Ecol. 23, 55385551.Google Scholar
Evstigneev, V.B. (1973). On evolution of the photosynthetic pigments. Orig. Life Evol. Biosph. 4(3), 448454.Google Scholar
Fairchild, T.R., Sanchez, E.A.M., Pacheco, M.L.A.F. & de Moraes Leme, J. (2016). Evolution of Precambrian life in the Brazilian geological record. Int. J. Astrobiol. 11, 309323.Google Scholar
Falkowski, P. (1997). Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272275.Google Scholar
Flombaum, P., Gallegos, J.L., Gordillo, R.A., Rincón, J., Zabala, L.L. & Jiao, N. (2013). Present and future global distributions of the marine. Proc. Natl. Acad. Sci. USA 110(24), 98249829.Google Scholar
Frazier, W.J. & Schwimmer, D.R. (1987). Regional Stratigraphy of North America. Plenum Press, New York.Google Scholar
García-Fernández, J.M., de Marsac, N.T. & Diez, J. (2004). Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol. Mol. Biol. Rev. 68(4), 630638.Google Scholar
Gauger, T., Konhauser, K. & Kappler, A. (2015). Protection of phototrophic iron(II)-oxidizing bacteria from UV irradiation by biogenic iron(III) minerals: implications for early Archean Banded Iron Formation. Geology 43, 10671070.Google Scholar
Grossman, A.R., Bhaya, D., Apt, K.E. & Kehoe, D.M. (1995). Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu. Rev. Genet. 29, 231288.Google Scholar
Grula, J. (2005). Evolution of photosynthesis and biospheric oxygenation contingent upon nitrogen fixation? Int. J. Astrobiol. 4, 251257.Google Scholar
Hawkesworth, C.J. & Kemp, A.I.S. (2006). Evolution of the continental crust. Nature 433, 811817.Google Scholar
Hawkesworth, C.J., Dhuime, B., Pietranik, A.B., Cawood, P.A., Kemp, A.I.S. & Storey, C.D. (2012). The generation and evolution of continental crust. J. Geol. Soc. Lond. 167, 229248.Google Scholar
Hessen, D. (2008). Solar radiation and the evolution of live. In Solar Radiation and the Human Health, ed. Bjertness, E., pp. 123132. The Norwegian Academy of Science and Letters, Oslo.Google Scholar
Heubeck, C. & Arndt, N. (2015). Archean environmental conditions. In Encyclopedia of Astrobiology, ed. Gardaud, M. et al. pp. 123125. Springer, Berlin.Google Scholar
Jerlov, N.G. (1976). Marine Optics. Elsevier Scientific Publishing Company, Amsterdam.Google Scholar
Johnson, C., Beard, B. & Roden, E. (2008). The iron isotope fingerprints of redox and biogeochemical cycling in modern and ancient Earth. Annu. Rev. Earth Plnet. Sci. 36, 457493.Google Scholar
Jørgensen, B.B., Cohen, Y. & Des Marais, D.J. (1987). Photosynthetic action spectra and adaptation to spectral light distribution in a benthic cyanobacterial mat. Appl. Environ. Microbiol. 53, 879886.Google Scholar
Kashiyama, Y. et al. (2008). Evidence of global chlorophyll d . Science 321(5889), 658.Google Scholar
Kirk, J.T.O. (2011). Light and Phososynthesis in Aquatic Ecosystems, 3th edn. Cambridge University Press, New York.Google Scholar
Klein, C. (2005). Some Precambrian Banded Iron-Formations (BIFs) from around the world: their age, geologic setting, mineralogy, metamorphism, geochemistry, and origin. Am. Mineral. 90, 14731499.Google Scholar
Knoll, A.H. (2014). Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6, a016121.Google Scholar
Kulasooriya, S. (2011). Cyanobacteria: pioneers of planet Earth. Ceylon J. Sci. Biol. Sci. 40, 7188.Google Scholar
Lane, N. (2014). Bioenergetic constraints on the evolution of complex life. In The Origin and Evolution of Eukaryotes, ed. Keeling, P.J. & Koonin, E.V., pp. 7996. E. Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York.Google Scholar
Lane, N. & Martin, W. (2010). The energetics of genome complexity. Nature 467, 929934.Google Scholar
Larkum, A.W.D. (2006). The evolution of chlorophylls and photosynthesis. In Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications, ed. Grimm, B., Porra, R.J., Rüdiger, W. & Scheer, H., pp. 261282. Springer, Netherlands.Google Scholar
Larkum, A.W.D., Chen, M., Li, Y., Schliep, M., Trampe, E., West, J., Salih, A. & Kühl, M. (2012). A novel epiphytic chlorophyll d-containing cyanobacterium isolated from a mangrove-associated red alga. J. Phycol. 48, 13201327.Google Scholar
Litchman, E., Neale, P. & Banaszak, A. (2002). Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limmnol. Oceanogr. 47, 8694.Google Scholar
Lowe, D.R. (1994). Early environments: constraints and opportunities for early evolution. In Early life on Earth, ed. Bengtson, S., pp. 2535. Columbia University Press, New York.Google Scholar
Lunine, J. (2013). Earth: Evolution of a Habitable World, 2dn edn. Cambridge University Press, Cambridge, UK.Google Scholar
Martín, O., Peñate, L., Cárdenas, R. & Horvath, J.E. (2012). The photobiological regime in the very early earth and the emergence of life. In Genesis-in the Beginning: Precursors of Life, Chemical Models and Early Biological Evolution, ed. Seckbach, J., pp. 145156. Springer, Dordrecht, Netherlands.Google Scholar
Miyashita, H., Ikemoto, H., Kurano, N., Miyachi, S. & Chihara, M. (2003). Acaryochloris marina gen. etsp. nov. (Cyanobacteria), anoxygenic photosynthetic prokaryote containing Chl d as a major pigment. J. Phycol. 39, 12471253.Google Scholar
Mloszewska, A., Lalonde, S.V., Whitford, D., Owttrim, G. & Konhauser, K.O. (2014). Archean seawater as a sunscreen: UV attenuation and cyanobacterial growth in Fe-and Si-rich media. In Goldschmidt Geochemistry Conf., 8–13 June, 2014, Sacremento, USA, Abstract no. 1711.Google Scholar
Mloszewska, A., Owttrim, G., Whitford, D., Lalonde, S., Kappler, A. & Konhauser, K. (2015). Silica saved our earliest marine cyanobacteria. In Geochemistry Conf., 16–21 August, 2015, Prague, Czech Republic, Abstract 2153.Google Scholar
Mohr, R., Björn, V., Schliep, M., Kurz, T., Maldener, I., Adams, D.G., Larkum, A.D.W., Chen, M. & Hess, W.R. (2010). A new chlorophyll d-containing cyanobacterium: evidence for niche adaptation in the genus Acaryochloris . ISME J. 4, 14561469.Google Scholar
Morel, A. (1978). Available, usable, and stored radiant energy in relation to marine photosynthesis. Deep Sea Res. 25, 673688.Google Scholar
Neale, P. & Kieber, D. (2000). Assessing biological and chemical effects of UV in the marine environment: spectral weighting functions. In Causes and Environmental Implications of Increased U.V.-B. Radiation, ed. Hester, R. & Harrison, R., pp. 6183. Royal Society of Chemistry Cambridge, Cambridge.Google Scholar
Neale, P.J., Helbling, E.W. & Zagarese, H.E. (2003). Modulation of UVR exposure and effects by vertical mixing and advection. In UV Effects in Aquatic Organisms and Ecosystems, ed. Helbling, E.W., pp. 109134. Royal Society of Chemistry, Cambridge.Google Scholar
Nisbet, E. (1995). Archaean ecology: a review of evidence for the early development of bacterial biomes, and speculations on the development of a global-scale biosphere. In Early Precambrian Processes, ed. Coward, M. & Rtes, A., pp. 2751. The Geological Society, London.Google Scholar
Nisbet, E., Cann, J. & van Dover, C. (1995). Origins of photosynthesis. Nature 373, 479480.Google Scholar
Noffke, N., Christian, D., Wacey, D. & Hazen, R. (2013). Microbially induced sedimentary structures recording an ancient ecosystem in the ca. 3.48 billion-year-old dresser formation, Pilbara, Western Australia. Astrobiology 12, 11031124.Google Scholar
Olson, J. (2006). Photosynthesis in the Archean era. Photosynth. Res. 88, 109117.Google Scholar
Olson, J.M. & Pierson, B.K. (1986). Photosynthesis 3.5 thousand million years ago. Photosynth. Res. 9, 251259.Google Scholar
Pasek, M.A., Harnmeijer, J.P., Buick, R., Gull, M. & Atlas, Z. (2013). Evidence for reactive reduced phosphorus species in the early Archean ocean. Proc. Natl. Acad. Sci. USA 110(25), 1008910094.Google Scholar
Phoenix, V.R., Konhauser, K.O., Adams, D.G. & Bottrell, S.H. (2001). Role of biomineralization as an ultraviolet shield: implications for Archean life. Geology 29, 823826.Google Scholar
Proteau, P.J., Gerwick, W.H., Garcia-Pichel, F. & Castenholz, R. (1993). The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia 49, 825829.Google Scholar
Raven, J.A. (1990). Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and C assimilation pathway. New Phytol. 116, 118.Google Scholar
Santosh, M. (2013). Evolution of continents, cratons and supercontinents: building the habitable Earth. Curr. Sci. 104(7), 871879.Google Scholar
Schirrmeister, B.E., Gugger, M. & Donoghue, P.C.J. (2015). Cyanobacteria and the great oxidation event: evidence from genes and fossils. Palaeontology 58(5), 769785.Google Scholar
Schirrmeister, B.E., Sanchez-Baracaldo, P. & Wacey, D. (2016). Cyanobacterial evolution during the Precambrian. Int. J. Astrobiol. CJO2016, 118.Google Scholar
Singh, S., Kumari, S., Rastogi, R., Singh, K. & Sinha, R. (2008). Mycosporine-like amino acids (MAAs): chemical structure, biosynthesis and significance as UV-absorbing/screening compounds. Indian J. Exp. Biol. 46, 717.Google Scholar
Smith, R. & Baker, K. (1981). Optical properties of the clearest natural waters. App. Optics 20, 177184.Google Scholar
Stern, C.R. (2011). Subduction erosion: rates, mechanisms, and its role in arc magmatism and the evolution of the continental crust and mantle. Gondwana Res. 20, 284308.Google Scholar
Sunda, W.G. & Huntsman, S.A. (2015). High iron requirement for growth, photosynthesis, and low-light acclimation in the coastal cyanobacterium Synechococcus bacillaris . Front. Microbiol. 6, 113.CrossRefGoogle ScholarPubMed
Taylor, S.R. & McLennan, S.M. (1995). The geochemical evolution of the continental crust. Rev. Geophys. 33, 241265.Google Scholar
Taylor, S.R., & McLennan, S.M. (1997). The origin and evolution of the Earth's continental crust. AGSO J. Aust. Geol. Geophys. 17(1), 5562.Google Scholar
Wong, H.L., Smith, D.L., Visscher, P.T. & Burns, B.P. (2015). Niche differentiation of bacterial communities at a millimeter scale in Shark Bay microbial mats. Sci. Rep. 5, 15607.CrossRefGoogle Scholar
Xiong, J. & Bauer, C. (2002). Complex evolution of photosynthesis. Annu. Rev. Plant. Biol. 53, 503521.Google Scholar