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Oxygen produced by cyanobacteria in simulated Archaean conditions partly oxidizes ferrous iron but mostly escapes—conclusions about early evolution

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Abstract

The Earth has had a permanently oxic atmosphere only since the great oxygenation event (GOE) 2.3–2.4 billion years ago but recent geochemical research has revealed short periods of oxygen in the atmosphere up to a billion years earlier before the permanent oxygenation. If these “whiffs” of oxygen truly occurred, then oxygen-evolving (proto)cyanobacteria must have existed throughout the Archaean aeon. Trapping of oxygen by ferrous iron and other reduced substances present in Archaean oceans has often been suggested to explain why the oxygen content of the atmosphere remained negligible before the GOE although cyanobacteria produced oxygen. We tested this hypothesis by growing cyanobacteria in anaerobic high-CO2 atmosphere in a medium with a high concentration of ferrous iron. Microcystins are known to chelate iron, which prompted us also to test the effects of microcystins and nodularins on iron tolerance. The results show that all tested cyanobacteria, especially nitrogen-fixing species grown in the absence of nitrate, and irrespective of the ability to produce cyanotoxins, were iron sensitive in aerobic conditions but tolerated high concentrations of iron in anaerobicity. This result suggests that current cyanobacteria would have tolerated the high-iron content of Archaean oceans. However, only 1 % of the oxygen produced by the cyanobacterial culture was trapped by iron, suggesting that large-scale cyanobacterial photosynthesis would have oxygenated the atmosphere even if cyanobacteria grew in a reducing ocean. Recent genomic analysis suggesting that ability to colonize seawater is a secondary trait in cyanobacteria may offer a partial explanation for the sustained inefficiency of cyanobacterial photosynthesis during the Archaean aeon, as fresh water has always covered a very small fraction of the Earth’s surface. If oxygenic photosynthesis originated in fresh water, then the GOE marks the adaptation of cyanobacteria to seawater, and the late-Proterozoic increase in oxygen concentration of the atmosphere is caused by full oxidation of the oceans.

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References

  • Alexova R, Fujii M, Birch D, Cheng J, Waite TD, Ferrari BC, Neilan BA (2011) Iron uptake and toxin synthesis in the bloom-forming Microcystis aeruginosa under iron limitation. Environ Microbiol 13:1064–1077

    Article  CAS  PubMed  Google Scholar 

  • Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef from the early Archaean era of Australia. Nature 441:714–718

    Article  CAS  PubMed  Google Scholar 

  • Anbar AD, Duan Y, Lyons TW, Arnold GL, Kendall B, Creaser RA, Kaufman AJ, Gordon GW, Scott C, Garvin J, Buick R (2007) A whiff of oxygen before the great oxidation event. Science 317:1903–1906

    Article  CAS  PubMed  Google Scholar 

  • Arnold GL, Anbar AD, Barling J, Lyons TW (2004) Molybdenum isotope evidence for widespread anoxia in mid-Proterozoic oceans. Science 304:87–90

    Article  CAS  PubMed  Google Scholar 

  • Bekker A, Holland HD, Wang PL, Rumble D III, Stein HJ, Hannah JL, Goetzee LL, Beukes NJ (2004) Dating the rise of atmospheric oxygen. Nature 427:117–120

    Article  CAS  PubMed  Google Scholar 

  • Blank CE, Sánchez-Baracaldo P (2010) Timing of morphological and ecological innovations in the cyanobacteria—a key to understanding the rise in atmospheric oxygen. Geobiology 8:1–23

    Article  CAS  PubMed  Google Scholar 

  • Blount ZD, Borland CZ, Lenski RE (2008) Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci USA 105:7899–7906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosak T, Greene SE, Newman DK (2007) A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites. Geobiology 5:119–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosak T, Bush JWM, Flynn MR, Liang B, Ono S, Petroff AP, Sim MS (2010) Formation and stability of oxygen-rich bubbles that shape photosynthetic mats. Geobiology 8:45–55

    Article  CAS  PubMed  Google Scholar 

  • Buick R (2008) When did oxygenic photosynthesis evolve. Philos Trans Royal Soc B 363:2731–2743

    Article  CAS  Google Scholar 

  • Burke SP, Banwart SA (2002) A geochemical model for removal of iron(II)(aq) from mine water discharges. Appl Geochem 17:431–443

    Article  CAS  Google Scholar 

  • Cairns-Smith A (1978) Precambrian solution photochemistry, inverse segregation, and banded iron formations. Nature 276:807–808

    Article  CAS  Google Scholar 

  • Cardona T (2015) A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth Res 126:111–134

    Article  CAS  PubMed  Google Scholar 

  • Claire MW, Catling DC, Zahnle KJ (2006) Biogeochemical modeling of the rise in the atmospheric oxygen. Geobiology 4:239–269

    Article  CAS  Google Scholar 

  • Cloud PE (1968) Atmospheric and hydrospheric evolution on the primitive Earth. Science 160:729–736

    Article  CAS  PubMed  Google Scholar 

  • Croal LR, Jiao Y, Kappler A, Newman DK (2009) Phototrophic Fe(II) oxidation in an atmosphere of H2: implications for Archean banded iron formations. Geobiology 7:21–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crowe SA, Døssing LN, Beukes NJ, Bau M, Kruger SJ, Frei R, Canfield DE (2013) Atmospheric oxygenation three billion years ago. Nature 501:535–539

    Article  CAS  PubMed  Google Scholar 

  • De Baar HJW, De Jong JTM (2001) Distributions, sources and sinks of iron in seawater. In: Turner DR, Hunter KA (eds) Biogeochemistry of iron in seawater. Wiley, Chichester, pp 123–253

    Google Scholar 

  • Debelius B, Forja JM, DelValls TA, Lubián LM (2009) Toxicity of copper in natural marine picoplankton populations. Ecotoxicology 18:1095–1103

    Article  CAS  PubMed  Google Scholar 

  • Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, Tyryshkin A (2001) The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98:2170–2175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dittmann E, Neilan B, Erhard M, von Döhren H, Börner T (1997) Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol Microbiol 26:779–787

    Article  CAS  PubMed  Google Scholar 

  • Downing JA, Pairie YT, Cole JJ, Duarte CM, Tranvik LJ, Striegl RG, McDowell WH, Kortelainen P, Caraco NF, Melack JM, Middelburg JJ (2006) The global abundance and size distribution of lakes, ponds and impoundments. Limnol Oceanogr 51:2388–2397

    Article  Google Scholar 

  • Farquhar J, Bao H, Thiemens M (2000) Atmospheric influence of Earth’s earliest sulfur cycle. Science 289:756–758

    Article  CAS  PubMed  Google Scholar 

  • Farquhar J, Zerkle AL, Bekker A (2011) Geological constraints on the origin of oxygenic photosynthesis. Photosynth Res 107:11–36

    Article  CAS  PubMed  Google Scholar 

  • Farrimond P, Talbot HM, Watson DF, Schulz LK, Wilhelms A (2004) Methylhopanoids: molecular indicators of ancient bacteria and a petroleum correlation tool. Geochim Cosmochim Acta 68:3873–3882

    Article  CAS  Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  CAS  PubMed  Google Scholar 

  • Fulton RS, Paerl HW (1987) Toxic and inhibitory effects of the blue-green-alga Microcystis aeruginosa on herbivorus zooplankton. J Plankton Res 9:837–855

    Article  Google Scholar 

  • Hughes EO, Gorham PR, Zehnder A (1958) Toxicity of a unialgal culture of Microcystis aeruginosa. Can J Microbiol 4:225–236

    Article  CAS  PubMed  Google Scholar 

  • Humble AV, Gadd GM, Codd GA (1997) Binding of copper and zinc to three cyanobacterial microcystins quantified by differential pulse polarography. Water Res 31:1679–1686

    Article  CAS  Google Scholar 

  • Isley A, Abbot D (1999) Plume-related mafic volcanism and the deposition of banded iron formation. J Geophys Res 104:15461–15477

    Article  CAS  Google Scholar 

  • Jackson TA (2015) Variations in the abundance of photosynthetic oxygen through Precambrian and Paleozoic time in relation to biotic evolution and mass extinctions: evidence from Mn/Fe ratios. Precambr Res 264:30–35

    Article  CAS  Google Scholar 

  • James HL (1954) Sedimentary facies of iron formation. Econ Geol 49:235–293

    Article  CAS  Google Scholar 

  • Jang M, Ha K, Joo G-J, Takamura N (2003) Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshw Biol 48:1540–1550

    Article  Google Scholar 

  • Järvenpää S, Lundberg-Niinistö C, Spoof L, Sjövall O, Tyystjärvi E, Meriluoto J (2007) Effects of microcystins on broccoli and mustard, and analysis of accumulated toxin by liquid chromatography-mass spectrometry. Toxicon 49:865–874

    Article  PubMed  Google Scholar 

  • Kappler A, Pasquero C, Konhauser KO, Newman DK (2005) Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidazing baxcteria. Geology 33:865–868

    Article  CAS  Google Scholar 

  • Kirschwink JL, Kopp RE (2008) Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II. Philos Trans Royal Soc B 363:2755–2765

    Article  Google Scholar 

  • Klein C, Beukes NJ (1992) Proterozoic iron-formations. In: Condie KC (ed) Proterozoic crustal evolution. Elsevier, Amsterdam, pp 383–418

    Chapter  Google Scholar 

  • Konhauser K, Hamede T, Raiswell R, Morris R, Ferris F, Southam G, Canfield D (2002) Could bacteria have formed the Precambrian banded iron formations. Geology 30:1079–1082

    Article  CAS  Google Scholar 

  • Konhauser K, Amskold L, Lalonde S, Posth N, Kappler Anbas A (2007) Decoupling photochemical oxidation from shallow-water BIF deposition. Earth Planet Sci Lett 258:87–100

    Article  CAS  Google Scholar 

  • Kopp R, Kirschvink J, Hilburn I, Nash C (2005) The paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc Natl Acad Sci USA 102:11131–11136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotai J (1972) Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research: Blindern, Oslo, Publication B-l l/69

  • Lambert W (1981) Inhibitory and toxic effects of blue green algae on Daphnia. Int Rev Hydrobiol 66:285–298

    Article  Google Scholar 

  • Larkum AWD (2007) Evolution of photosynthesis. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Vol 2, Royal Society of Chemistry, pp 489–521

  • Lehtimäki N, Shunmugam S, Jokela J, Wahlsten M, Carmel D, Keränen M, Sivonen K, Aro E-M, Allahverdieva Y, Mulo P (2011) Nodularin uptake and induction of oxidative stress in spinach (Spinacia oleracea). J Plant Physiol 168:594–600

    Article  PubMed  Google Scholar 

  • Lewis WM Jr (2011) Global primary production of lakes: 19th Baldi memorial lecture. Inl Waters 1:1–28

    Article  Google Scholar 

  • Lukač M, Aegerter R (1993) Influence of trace metals on growth and toxin production of Microcystis aeruginosa. Toxicon 31:293–305

    Article  PubMed  Google Scholar 

  • Lyons TW, Reinhard CT, Planavsky NJ (2014) The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506:307–315

    Article  CAS  PubMed  Google Scholar 

  • MacKintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitos of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett 264:187–192

    Article  CAS  PubMed  Google Scholar 

  • Mattila H, Khorobrykh S, Havurinne V, Tyystjärvi E (2015) Reactive oxygen species: reactions and detection from photosynthetic tissues. J Photochem Photobiol B 152:176–214

    Article  CAS  PubMed  Google Scholar 

  • Meriluoto J, Codd GA (2005) TOXIC: cyanobacterial monitoring and cyanotoxin analysis. Åbo Akademi University Press, Turku

    Google Scholar 

  • Nikkinen HL, Hakkila K, Gunnelius L, Huokko T, Pollari M, Tyystjärvi T (2012) The SigB sigma factor regulates multiple salt acclimation responses of the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 158:514–523

    Article  CAS  PubMed  Google Scholar 

  • Olson JM (2006) Photosynthesis in the Archean era. Photosynth Res 88:109–117

    Article  CAS  PubMed  Google Scholar 

  • Parekh P, Follows MJ, Boyle E (2004) Modeling the global ocean iron cycle. Global biogeochemical cycles 18: GB1002

  • Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pflugmacher S, Olin M, Kankaanpää H (2007) Nodularin induces oxidative stress in the Baltic Sea brown alga Fucus vesiculosus (Phaeophyceae). Marine Environ Res 64:149–159

    Article  CAS  Google Scholar 

  • Planavsky NJ, Asael D, Hofmann A, Reinhard CT, Lalonde SV, Knudsen A, Wang X, Ossa FO, Pecoits E, Smith AJB, Beukes NJ, Bekker A, Johnson TM, Konhauser KO, Lyons TW, Rouxel OJ (2014) Evidence for oxygenic photosynthesis half a billion years before the great oxidation event. Nat Geosci 7:283–286

    Article  CAS  Google Scholar 

  • Rai LC, Gaur JP, Kumar HD (1981) Phycology and heavy-metal pollution. Biol Rev 56:99–151

    Article  CAS  Google Scholar 

  • Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Valtomaa J, Börner T, Sivonen K (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci USA 101:568–573

    Article  CAS  PubMed  Google Scholar 

  • Rashby SE, Sessions AL, Summons RE, Newman DK (2007) Biosynthesis of 2-methylbacteriohopanepolyols by an anoxygenic phototroph. Proc Natl Acad Sci USA 104:15099–15104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raven JA, Larkum AWD (2007) Are there ecological implications for the proposed energetic restrictions on photosynthetic oxygen evolution at high oxygen concentrations. Photosynth Res 94:31–42

    Article  CAS  PubMed  Google Scholar 

  • Sessions AL, Doughty DM, Welander PV, Summons RE, Newman DK (2009) The continuing puzzle of the great oxidation event. Curr Biol 19:R567–R574

    Article  CAS  PubMed  Google Scholar 

  • Sevilla E, Martin-Luna B, Vela L, Bes MT, Fillat MF, Peleato ML (2008) Iron availibility affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environ Microbiol 10:2476–2483

    Article  CAS  PubMed  Google Scholar 

  • Shiklomanov IA (1993) World fresh water resources. In: Gleick PH (ed) Water in crisis. A guide to the world’s fresh water resources. Oxford University Press, Oxford, pp 13–24

    Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water—a guide to their public health consequences, monitoring and management. E and FF Spon ltd, London, pp 41–111

    Google Scholar 

  • Sivonen K, Kononen K, Esala AL, Niemelä SI (1989) Toxicity and isolation of the cyanobacterium Nodularia spumigena from the southern Baltic Sea in 1986. Hydrobiologia 185:3–8

    Article  CAS  Google Scholar 

  • Smith RC, Baker KS (1981) Optical properties of the clearest natural waters (200–800 nm). Appl Opt 20:177–184

    Article  CAS  PubMed  Google Scholar 

  • Summons RE, Jahnke LL, Hope JM, Logan GA (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:554–557

    Article  CAS  PubMed  Google Scholar 

  • Swanner ED, Mloszewska AM, Cirpka OA, Schoenberg R, Konhauser KO, Kappler A (2015) Modulation of oxygen production in Archaean oceans by episodes of Fe(II) toxicity. Nat Geosci 8:126–130

    Article  CAS  Google Scholar 

  • Taylor SR, McLennan SM (1995) The geochemical evolution of the continental-crust. Rev Geophys 33:241–265

    Article  Google Scholar 

  • Tice MM, Lowe DR (2004) Photosynthetic microbial mats in the 3416-Myr-old ocean. Nature 431:549–552

    Article  CAS  PubMed  Google Scholar 

  • Trouwborst RE, Johnston A, Koch G, Luther GW III, Pierson BK (2007) Biogeochemistry of Fe(II) oxidation in a photosynthetic microbial mat: implications for Precambrian Fe(II) oxidation. Geochim Cosmochim Acta 71:4629–4643

    Article  CAS  Google Scholar 

  • Utkilen H, Gjolme N (1995) Iron-stimulated toxin production in Microcystis aeruginosa. Appl Environ Microbiol 61:797–800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vintila S, El-Shehawy R (2007) Ammonium ions inhibit nitrogen fixation but do not affect heterocyst frequency in the bloom-forming cyanobacterium Nodularia spumigenia strain AV1. Microbiology 153:3704–3712

    Article  CAS  PubMed  Google Scholar 

  • Vogel AI (1962) A text-book of quantitative inorganic analysis. Wiley, New York

    Google Scholar 

  • Walter MR, Buick R, Dunlop JSR (1980) Stromatolites 3400–3,5000 Myr old from the North Pole area, Western Australia. Nature 248:443–445

    Article  Google Scholar 

  • Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647

    Article  CAS  PubMed  Google Scholar 

  • Wang XJ, Behrenfeld M, Le Borgne R, Murtugudde R, Boss E (2009) Regulation of phytoplankton carbon to chlorophyll ratio by light, nutrients and temperature in the Equatorial Pacific Ocean: a basin-scale model. Biogeosciences 6:391–404

    Article  CAS  Google Scholar 

  • Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764

    Article  CAS  PubMed  Google Scholar 

  • Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B, Schink B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362:834–836

    Article  CAS  Google Scholar 

  • Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol Appl Pharmacol 203:201–218

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Turun yliopistosäätiö (SR, ET, 2008–2011), Academy of Finland (ET, TT; Grants 259075, 271832, 265807) and Svenska Litteratursällskapet i Finland (LS). COST action ESI1105 “CYANOCOST—cyanobacterial blooms and toxins in water resources: occurrence, impacts and management” is acknowledged for adding value to this study through networking and knowledge sharing with European experts.

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  1. Department of Biochemistry/Molecular Plant Biology, University of Turku, 20014, Turku, Finland

    Susanne Rantamäki, Eeva-Maija Puputti, Taina Tyystjärvi & Esa Tyystjärvi

  2. Biochemistry, Faculty of Biosciences, Åbo Akademi University, Tykistökatu 6 A, 20520, Turku, Finland

    Jussi Meriluoto & Lisa Spoof

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  1. Susanne Rantamäki
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Rantamäki, S., Meriluoto, J., Spoof, L. et al. Oxygen produced by cyanobacteria in simulated Archaean conditions partly oxidizes ferrous iron but mostly escapes—conclusions about early evolution. Photosynth Res 130, 103–111 (2016). https://doi.org/10.1007/s11120-016-0231-4

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