[en] Deciphering the fossil record of cyanobacteria is crucial to understand their role in the chemical and biological evolution of the early Earth. They profoundly modified the redox conditions of early ecosystems more than 2.4 Ga ago, the age of the Great Oxidation Event (GOE), and provided the ancestor of the chloroplast by endosymbiosis, leading the diversification of photosynthetic eukaryotes. Here, we analyze the morphology, ultrastructure, chemical composition, and metals distribution of Polysphaeroides filiformis from the 1040–1006 Ma Mbuji-Mayi Supergroup (DR Congo). We evidence trilaminar and bilayered ultrastructures for the sheath and the cell wall, respectively, and the preservation of Ni-tetrapyrrole moieties derived from chlorophyll in intracellular inclusions. This approach allows an unambiguous interpretation of P. filiformis as a branched and multiseriate photosynthetic cyanobacterium belonging to the family of Stigonemataceae. It also provides a possible minimum age for the emergence of multiseriate true branching nitrogen-fixing and probably heterocytous cyanobacteria.
Research Center/Unit :
Synchrotron Soleil, 91190 Saint-Aubin – BP 48, France ESRF-The European Synchrotron, 38000 Grenoble, France Paul Scherrer Institut, Swiss Light Source, 5232 Villigen PSI, Switzerland CAREM - Cellule d'Appui à la Recherche et à l'Enseignement en Microscopie - ULiège Unité Matériaux et Transformations (UMR CNRS 8207), Université Lille 1 - Sciences et Technologies, 59650 Villeneuve d'Ascq, France
FP7 - 308074 - ELITE - Early Life Traces, Evolution, and Implications for Astrobiology
Funders :
ERC - European Resuscitation Council F.R.S.-FNRS - Fonds de la Recherche Scientifique BELSPO - Belgian Federal Science Policy Office ULiège - Université de Liège ERC - European Research Council EU - European Union
Funding number :
B2/212/PI/PORTAL; FP7/308074; EOS ET-Home grant 30442502
Javaux, E.J., Eukaryotes, Appearance and Early Evolution of. Gargaud, M., Irvine, W.M., Amils, R., Claeys, P., Cleaves, H.J., Gerin, M., Rouan, D., Spohn, T., Tirard, S., Viso, M., (eds.) Encyclopedia of Astrobiology, 2021, Springer, 1–5 chapter 538-4.
Gueneli, N., McKenna, A.M., Ohkouchi, N., Boreham, C.J., Beghin, J., Javaux, E.J., Brocks, J.J., 1.1-billion-year-old porphyrins establish a marine ecosystem dominated by bacterial primary producers. Proc. Natl. Acad. Sci. USA 115 (2018), E6978–E6986.
Vinnichenko, G., Jarrett, A.J.M., Hope, J.M., Brocks, J.J., Discovery of the oldest known biomarkers provides evidence for phototrophic bacteria in the 1.73 Ga Wollogorang Formation, Australia. Geobiology 18 (2020), 544–559.
Osterhout, J.T., Schopf, J.W., Williford, K.H., McKeegan, K.D., Kudryavtsev, A.B., Liu, M.C., Carbon isotopes of Proterozoic filamentous microfossils: SIMS analyses of ancient cyanobacteria from two disparate shallow-marine cherts. Geomicrobiol. J. 38 (2021), 719–731.
Bosak, T., Greene, S.E., Newman, D.K., A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites. Geobiology 5 (2007), 119–126.
Bosak, T., Knoll, A.H., Petroff, A.P., The meaning of stromatolites. Annu. Rev. Earth Planet Sci. 41 (2013), 21–44.
Golubic, S., Hofmann, H.J., Comparison of Holocene and mid-Precambrian Entophysalidaceae (Cyanophyta) in stromatolitic algal mats: cell division and degradation. J. Paleontol., 1976, 1074–1082.
Hofmann, H.J., Precambrian microflora, Belcher Islands, Canada: significance and systematics. J. Paleontol., 1976, 1040–1073.
Hodgskiss, M.S., Dagnaud, O.M., Frost, J.L., Halverson, G.P., Schmitz, M.D., Swanson-Hysell, N.L., Sperling, E.A., New insights on the Orosirian carbon cycle, early Cyanobacteria, and the assembly of Laurentia from the Paleoproterozoic Belcher Group. Earth Planet Sci. Lett. 520 (2019), 141–152.
Demoulin, C.F., Lara, Y.J., Cornet, L., François, C., Baurain, D., Wilmotte, A., Javaux, E.J., Cyanobacteria evolution: Insight from the fossil record. Free Radic. Biol. Med. 140 (2019), 206–223.
Huber, A.L., Factors affecting the germination of akinetes of Nodularia spumigena (Cyanobacteriaceae). Appl. Environ. Microbiol. 49 (1985), 73–78.
Baker, P.D., Bellifemine, D., Environmental influences on akinete germination of Anabaena circinalis and implications for management of cyanobacterial blooms. Hydrobiologia 427 (2000), 65–73.
Kaplan-Levy, R.N., Hadas, O., Summers, M.L., Rücker, J., Sukenik, A., Lubzens, E., Cerda, J., Clark, M., (eds.) “Akinetes: dormant cells of cyanobacteria” in Dormancy and resistance in harsh environments, 2010, Springer, 5–27.
Haselkorn, R., Annu. Rev. Plant Physiol. 29 (1978), 319–344.
Rippka, R., Stanier, R.Y., Deruelles, J., Herdman, M., Waterbury, J.B., Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111 (1979), 1–61.
Hammerschmidt, K., Landan, G., Domingues Kümmel Tria, F., Alcorta, J., Dagan, T., The order of trait emergence in the evolution of cyanobacterial multicellularity. Genome Biol. Evol., 13, 2021, evaa249.
Strunecký, O., Ivanova, A.P., Mareš, J., An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis. J. Phycol. 59 (2023), 12–51.
Timofeev, B.V., Hermann, T.N., Michailova, N.S., Mikrofitofossilii Dokembria, Kembriaiordovika (Microphytofossils of the Precambrian, Cambrian and Ordovician). 1976, Scientific Institute of Precambrian Geology and Geochronology, 106 p [in Russian].
Amard, B., Bertrand-Sarfati, J., Microfossils in 2000 Ma old cherty stromatolites of the Franceville Group. Precambrian Res. 81 (1997), 197–221.
Tomitani, A., Knoll, A.H., Cavanaugh, C.M., Ohno, T., The evolutionary diversification of cyanobacteria: molecular–phylogenetic and paleontological perspectives. Proc. Natl. Acad. Sci. USA 103 (2006), 5442–5447.
Pang, K., Tang, Q., Chen, L., Wan, B., Niu, C., Yuan, X., Xiao, S., Nitrogen-fixing heterocystous cyanobacteria in the Tonian period. Curr. Biol. 28 (2018), 616–622.e1.
Krings, M., Stigonema (Nostocales, Cyanobacteria) in the Rhynie chert (Lower Devonian, Scotland). Rev. Palaeobot. Palynol., 295, 2021, 104505.
Hermann, T.N., Organic World One Billion Years Ago. 1990, Nauka, Leningrad, 50 [in Russian with English summary].
Vorob'eva, N.G., Sergeev, V.N., Knoll, A.H., Neoproterozoic microfossils from the northeastern margin of the East European Platform. J. Paleontol. 83 (2009), 161–196.
Hofmann, H.J., Jackson, G.D., Shale-facies microfossils from the Proterozoic Bylot Supergroup, Baffin Island, Canada. J. Paleontol. 68 (1994), 1–35.
Vorob'eva, N.G., Sergeev, V.N., Petrov, P.Y., Kotuikan Formation assemblage: a diverse organic-walled microbiota in the Mesoproterozoic Anabar succession, northern Siberia. Precambrian Res. 256 (2015), 201–222.
Gorokhov, I.M., Kuznetsov, A.B., Semikhatov, M.A., Vasil'eva, I.M., Rizvanova, N.G., Lipenkov, G.V., Dubinina, E.O., Early Riphean Billyakh Group of the Anabar uplift, North Siberia: C–O isotopic geochemistry and Pb–Pb age of dolomites. Stratigr. Geol. Correl. 27 (2019), 514–528.
Petrov, P.Y., Sharma, M., Vorob'eva, N.G., Sergeev, V.N., Facies-stratigraphic distribution of organic-walled and silicified microfossils in the early Billiyakh Basin (Lower Riphean, Anabar Uplift, Siberia). Paleontol. J. 53 (2019), 867–872.
Baludikay, B.K., Storme, J.Y., François, C., Baudet, D., Javaux, E.J., A diverse and exquisitely preserved organic-walled microfossil assemblage from the Meso–Neoproterozoic Mbuji-Mayi Supergroup (Democratic Republic of Congo) and implications for Proterozoic biostratigraphy. Precambrian Res. 281 (2016), 166–184.
François, C., Baludikay, B.K., Debaille, V., Birck, J.L., Limmois, D., Jourdan, F., Baudet, D., Paquette, J.L., Delvaux, D., Javaux, E.J., Multi-method dating constrains the diversification of early eukaryotes in the Proterozoic Mbuji-Mayi Supergroup of the DR Congo and the geological evolution of the Congo Basin. J. Afr. Earth Sci., 198, 2023, 104785.
Pacton, M., Gorin, G.E., Fiet, N., Unravelling the origin of ultralaminae in sedimentary organic matter: the contribution of bacteria and photosynthetic organisms. J. Sediment. Res. 78 (2008), 654–667.
Mareš, J., Strunecký, O., Bučinská, L., Wiedermannová, J., Evolutionary patterns of thylakoid architecture in cyanobacteria. Front. Microbiol., 10, 2019, 277.
Sforna, M.C., Loron, C.C., Demoulin, C.F., François, C., Cornet, Y., Lara, Y.J., Grolimund, D., Ferreira Sanchez, D., Medjoubi, K., Somogyi, A., et al. Intracellular bound chlorophyll residues identify 1 Gyr-old fossils as eukaryotic algae. Nat. Commun. 13 (2022), 146–148.
Lepot, K., Compère, P., Gérard, E., Namsaraev, Z., Verleyen, E., Tavernier, I., Hodgson, D.A., Vyverman, W., Gilbert, B., Wilmotte, A., Javaux, E.J., Organic and mineral imprints in fossil photosynthetic mats of an East-Antarctic lake. Geobiology 12 (2014), 424–450.
Storme, J.Y., Golubic, S., Wilmotte, A., Kleinteich, J., Velázquez, D., Javaux, E.J., Raman characterization of the UV-protective pigment gloeocapsin and its role in the survival of cyanobacteria. Astrobiology 15 (2015), 843–857.
Lara, Y.J., McCann, A., Malherbe, C., François, C., Demoulin, C.F., Sforna, M.C., Eppe, G., De Pauw, E., Wilmotte, A., Jacques, P., Javaux, E.J., Characterization of the Halochromic Gloeocapsin Pigment, a Cyanobacterial Biosignature for Paleobiology and Astrobiology. Astrobiology 22 (2022), 735–754.
Pang, K., Tang, Q., Schiffbauer, J.D., Yao, J., Yuan, X., Wan, B., Chen, L., Ou, Z., Xiao, S., The nature and origin of nucleus-like intracellular inclusions in Paleoproterozoic eukaryote microfossils. Geobiology 11 (2013), 499–510.
Carlisle, E.M., Jobbins, M., Pankhania, V., Cunningham, J.A., Donoghue, P.C.J., Experimental taphonomy of organelles and the fossil record of early eukaryote evolution. Sci. Adv., 7, 2021, eabe9487.
Treibs, A., Chlorophyll and haemin derivatives in organic minerals. Angew. Chem. 49 (1936), 682–686.
Tahoun, M., Gee, C.T., McCoy, V.E., Sander, P.M., Müller, C.E., Chemistry of porphyrins in fossil plants and animals. RSC Adv. 11 (2021), 7552–7563.
Callot, H.J., Ocampo, R., Albrecht, P., Sedimentary porphyrins: Correlations with biological precursors. Energy Fuels 4 (1990), 635–639.
Jiang, K., Siahrostami, S., Zheng, T., Hu, Y., Hwang, S., Stavitski, E., Peng, Y., Dynes, J., Gangisetty, M., Su, D., et al. Isolated Ni single atoms in graphene nanosheets for high-performance CO 2 reduction. Energy Environ. Sci. 11 (2018), 893–903.
Xia, K., Bleam, W., Helmke, P.A., Studies of the nature of binding sites of first row transition elements bound to aquatic and soil humic substances using X-ray absorption spectroscopy. Geochem. Cosmochim. Acta 61 (1997), 2223–2235.
Lytle, F.W., Data from “Cold Lake Asphaltene V. And Ni X. A. S. Spectra.”. 1983, International X-ray Absorption Society XAFS Database.
West, J.A., de Goër, S.L., Zuccarello, G.C., A new species of Bangiopsis: B. franklynottii sp. nov. (Stylonematophyceae, Rhodophyta) from Australia and India and comments on the genus. ALGAE 29 (2014), 101–109.
Hoiczyk, E., Hansel, A., Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J. Bacteriol. 182 (2000), 1191–1199.
Komárek, J., Cyanoprokaryota. 3. Teil/3rd part: heterocytous genera. Büdel, B., Gärtner, G., Krienitz, L., Schagerl, M., (eds.) Süßwasserflora von Mitteleuropa freshwater flora of Central Europe, 2013, Springer Spektrum, 1130.
Bartley, J.K., Actualistic taphonomy of cyanobacteria: implications for the Precambrian fossil record. Palaios 11 (1996), 571–586.
Strullu-Derrien, C., Fercoq, F., Gèze, M., Kenrick, P., Martos, F., Selosse, M.-A., Benzerara, K., Knoll, A.H., Hapalosiphonacean cyanobacteria (Nostocales) thrived amid emerging embryophytes in an early Devonian (407-million-year-old) landscape. iScience, 26, 2023, 107338.
Coates, J., Interpretation of Infrared Spectra, a Practical Approach. Meyers, R.A., (eds.) Encyclopedia of Analytical Chemistry, 2000, John Wiley & Sons Ltd, 10815–10837.
Marshall, C., Javaux, E., Knoll, A., Walter, M., Combined micro-Fourier transform infrared (FTIR) spectroscopy and micro-Raman spectroscopy of Proterozoic acritarchs: a new approach to palaeobiology. Precambrian Res. 138 (2005), 208–224.
Sharma, M., Mishra, S., Dutta, S., Banerjee, S., Shukla, Y., On the affinity of Chuaria–Tawuia complex: a multidisciplinary study. Precambrian Res. 173 (2009), 123–136.
Loron, C.C., François, C., Rainbird, R.H., Turner, E.C., Borensztajn, S., Javaux, E.J., Early fungi from the Proterozoic era in Arctic Canada. Nature 570 (2019), 232–235.
Gómez-Ordóñez, E., Rupérez, P., FTIR-ATR spectroscopy as a tool for polysaccharide identification in edible brown and red seaweeds. Food Hydrocolloids 25 (2011), 1514–1520.
Varnali, T., Edwards, H.G., Hargreaves, M.D., Scytonemin: molecular structural studies of a key extremophilic biomarker for astrobiology. Int. J. Astrobiol. 8 (2009), 133–140.
Michel, H., Behr, J., Harrenga, A., Kannt, A., Cytochrome c oxidase: structure and spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 27 (1998), 329–356.
Denisov, I.G., Makris, T.M., Sligar, S.G., Schlichting, I., Structure and chemistry of cytochrome P450. Chem. Rev. 105 (2005), 2253–2277.
Helliwell, K.E., Lawrence, A.D., Holzer, A., Kudahl, U.J., Sasso, S., Kräutler, B., Scanlan, D.J., Warren, M.J., Smith, A.G., Cyanobacteria and eukaryotic algae use different chemical variants of vitamin B12. Curr. Biol. 26 (2016), 999–1008.
Didyk, B., Alturki, Y.I.A., Pillinger, C.T., Eglinton, G., The petroporphyrins of a Cretaceous oil. Chem. Geol. 15 (1975), 193–208.
Zhang, Y., Schulz, F., Rytting, B.M., Walters, C.C., Kaiser, K., Metz, J.N., Harper, M.R., Merchant, S.S., Mennito, A.S., Qian, K., et al. Elucidating the geometric substitution of petroporphyrins by spectroscopic analysis and atomic force microscopy molecular imaging. Energy Fuels 33 (2019), 6088–6097.
Pleyer, H.L., Moeller, R., Fujimori, A., Fox, S., Strasdeit, H., Chemical, Thermal, and Radiation Resistance of an Iron Porphyrin: A Model Study of Biosignature Stability. Astrobiology 22 (2022), 776–799.
Swingley, W.D., Blankenship, R.E., Raymond, J., Neil Hunter, C., Daldal, F., Thurnauer, M.C., Thomas Beatty, J., (eds.) “Evolutionary relationship among purple photosynthetic bacteria and the origin of proteobacterial photosynthetic systems” in The Purple Phototrophic Bacteria, 2009, Springer, 17–29.
Gaisin, V.A., Kalashnikov, A.M., Grouzdev, D.S., Sukhacheva, M.V., Kuznetsov, B.B., Gorlenko, V.M., Chloroflexus islandicus sp. nov., a thermophilic filamentous anoxygenic phototrophic bacterium from a geyser. Int. J. Syst. Evol. Microbiol. 67 (2017), 1381–1386.
Mareš, J., Lara, Y., Dadáková, I., Hauer, T., Uher, B., Wilmotte, A., Kaštovský, J., Phylogenetic analysis of cultivation-resistant terrestrial cyanobacteria with massive sheaths (Stigonema spp. and Petalonema alatum, Nostocales, Cyanobacteria) using single-cell and filament sequencing of environmental samples. J. Phycol. 51 (2015), 288–297.
Stewart, K.D., Mattox, K.R., Comparative cytology, evolution and classification of the green algae with some consideration of the origin of other organisms with chlorophylls a and b. Bot. Rev. 41 (1975), 104–135.
Wehr, J.D., Brown algae (Phaeophyceae) in rivers. Necchi, O. Jr., (eds.) River Algae, 2016, Springer, 129–152.
Butterfield, N.J., Knoll, A.H., Swett, K., A bangiophyte red alga from the Proterozoic of arctic Canada. Science 250 (1990), 104–107.
Sutherland, J.E., Lindstrom, S.C., Nelson, W.A., Brodie, J., Lynch, M.D.J., Hwang, M.S., Choi, H.G., Miyata, M., Kikuchi, N., Oliveira, M.C., et al. A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J. Phycol. 47 (2011), 1131–1151.
Albis-Salas, M.R., Gavio, B., Notes on the marine algae of the international biosphere reserve seaflower, Caribbean Colombia IV: new records of macroalgal epiphytes on the seagrass Thalassia testudinum. Bot. Mar. 54 (2011), 537–543.
Croce, M.E., Parodi, E.R., The japanese alga Polysiphonia morrowii (Rhodomelaceae, Rhodophyta) on the South Atlantic ocean: first report of an invasive macroalga inhabiting oyster reefs. Helgol. Mar. Res. 68 (2014), 241–252.
Gonzalez-Esquer, C.R., Smarda, J., Rippka, R., Axen, S.D., Guglielmi, G., Gugger, M., Kerfeld, C.A., Cyanobacterial ultrastructure in light of genomic sequence data. Photosynth. Res. 129 (2016), 147–157.
Yaylayan, V.A., Ismail, A.A., Investigation of the enolization and carbonyl group migration in reducing sugars by FTIR spectroscopy. Carbohydr. Res. 276 (1995), 253–265.
Kaplan Can, H., Gurbuz, F., Odabaşı, M., Partial characterization of cyanobacterial extracellular polymeric substances for aquatic ecosystems. Aquat. Ecol. 53 (2019), 431–440.
Pereira, L., Amado, A.M., Critchley, A.T., Van de Velde, F., Ribeiro-Claro, P.J., Identification of selected seaweed polysaccharides (phycocolloids) by vibrational spectroscopy (FTIR-ATR and FT-Raman). Food Hydrocolloids 23 (2009), 1903–1909.
Wallace, M.D., Guée, L., Ropartz, D., Fanuel, M., Lannuzel, G., Correc, G., Stubbs, K.A., Ficko-Blean, E., Characterisation of an exo-(α-1, 3)-3, 6-anhydro-D-galactosidase produced by the marine bacterium Zobellia galactanivorans DsijT: Insight into enzyme preference for natural carrageenan oligosaccharides and kinetic characterisation on a novel chromogenic substrate. Int. J. Biol. Macromol. 163 (2020), 1471–1479.
Usov, A.I., Horton, D., (eds.) “Polysaccharides of the red algae” In Advances in carbohydrate chemistry and biochemistry, 2011, Academic Press, 115–217.
Pereira, S., Zille, A., Micheletti, E., Moradas-Ferreira, P., De Philippis, R., Tamagnini, P., Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol. Rev. 33 (2009), 917–941.
Honey, D.J., Heme B in Marine Cyanobacteria and the (Sub-) Tropical North Atlantic. 2012, Doctoral dissertation, University of Southampton.
Chia, M.A., Kramer, B.J., Jankowiak, J.G., Bittencourt-Oliveira, M.D.C., Gobler, C.J., The individual and combined effects of the cyanotoxins, anatoxin-a and microcystin-LR, on the growth, toxin production, and nitrogen fixation of prokaryotic and eukaryotic algae. Toxins, 11, 2019, 43.
Maraóón, E., Cermeóo, P., Rodríguez, J., Zubkov, M.V., Harris, R.P., Scaling of phytoplankton photosynthesis and cell size in the ocean. Limnol. Oceanogr. 52 (2007), 2190–2198.
Baludikay, B.K., François, C., Sforna, M.C., Beghin, J., Cornet, Y., Storme, J.Y., Fagel, N., Fontaine, F., Littke, R., Baudet, D., et al. Raman microspectroscopy, bitumen reflectance and illite crystallinity scale: comparison of different geothermometry methods on fossiliferous Proterozoic sedimentary basins (DR Congo, Mauritania and Australia). Int. J. Coal Geol. 191 (2018), 80–94.
Lewan, M.D., Maynard, J.B., Factors controlling enrichment of vanadium and nickel in the bitumen of organic sedimentary rocks. Geochem. Cosmochim. Acta 46 (1982), 2547–2560.
Saito, M.A., Sigman, D.M., Morel, F.M., The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean–Proterozoic boundary?. Inorg. Chim. Acta. 356 (2003), 308–318.
Russell, M.J., Cobalt: A must-have element for life and livelihood. Proc. Natl. Acad. Sci. USA, 119, 2022, e2121307119.
Saito, M.A., Moffett, J.W., Chisholm, S.W., Waterbury, J.B., Cobalt limitation and uptake in Prochlorococcus. Limnol. Oceanogr. 47 (2002), 1629–1636.
Sunda, W.G., Huntsman, S.A., Cobalt and zinc interreplacement in marine phytoplankton: Biological and geochemical implications. Limnol. Oceanogr. 40 (1995), 1404–1417.
Huertas, M.J., López-Maury, L., Giner-Lamia, J., Sánchez-Riego, A.M., Florencio, F.J., Metals in cyanobacteria: analysis of the copper, nickel, cobalt and arsenic homeostasis mechanisms. Life 4 (2014), 865–886.
Cavet, J.S., Borrelly, G.P.M., Robinson, N.J., Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol. Rev. 27 (2003), 165–181.
Sforna, M.C., Daye, M., Philippot, P., Somogyi, A., van Zuilen, M.A., Medjoubi, K., Gérard, E., Jamme, F., Dupraz, C., Braissant, O., et al. Patterns of metal distribution in hypersaline microbialites during early diagenesis: implications for the fossil record. Geobiology 15 (2017), 259–279.
Pedersén, M., Saenger, P., Rowan, K.S., Hofsten, A.V., Bromine, bromophenols and floridorubin in the red alga Lenormandia prolifera. Physiol. Plantarum 46 (1979), 121–126.
Gribble, G.W., The diversity of naturally occurring organobromine compounds. Chem. Soc. Rev. 28 (1999), 335–346.
Caspi, R., Billington, R., Keseler, I.M., Kothari, A., Krummenacker, M., Midford, P.E., Ong, W.K., Paley, S., Subhraveti, P., Karp, P.D., The MetaCyc database of metabolic pathways and enzymes-a 2019 update. Nucleic Acids Res. 48 (2020), D445–D453.
Croft, W.N., George, E.A., Blue-green algae from the Middle Devonian of Rhynie. Aberdeenshire. Bull. Brit. Mus. Nat. Hist. Geol. 3 (1959), 341–353.
Komárek, J., Kaštovský, J., Mareš, J., Johansen, J.R., Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86 (2014), 295–335.
Dos Santos, P.C., Fang, Z., Mason, S.W., Setubal, J.C., Dixon, R., Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genom. 13 (2012), 1–12.
Stüeken, E.E., Buick, R., Guy, B.M., Koehler, M.C., Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr. Nature 520 (2015), 666–669.
Schirrmeister, B.E., de Vos, J.M., Antonelli, A., Bagheri, H.C., Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc. Natl. Acad. Sci. USA 110 (2013), 1791–1796.
Uyeda, J.C., Harmon, L.J., Blank, C.E., A comprehensive study of cyanobacterial morphological and ecological evolutionary dynamics through deep geologic time. PLoS One, 11, 2016, e0162539.
Sánchez-Baracaldo, P., Raven, J.A., Pisani, D., Knoll, A.H., Early photosynthetic eukaryotes inhabited low-salinity habitats. Proc. Natl. Acad. Sci. USA 114 (2017), E7737–E7745.
Schirrmeister, B.E., Gugger, M., Donoghue, P.C.J., Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils. Palaeontology (Prague) 58 (2015), 769–785.
Solé, V., Papillon, E., Cotte, M., Walter, P., Susini, J., A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim. Acta B Atom Spectrosc. 62 (2007), 63–68.
Ravel, B., Newville, M., ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Radiat. 12 (2005), 537–541.
Cahen, L., Snelling, N.J., Delhal, J., Vail, J.R., Bonhomme, M., Ledent, D., The Geochronology and Evolution of Africa. 1984, Clarendon), 512.
Delvaux, D., Maddaloni, F., Tesauro, M., Braitenberg, C., The Congo Basin: stratigraphy and subsurface structure defined by regional seismic reflection, refraction and well data. Global Planet. Change, 198, 2021, 103407.
Grey, K., A Modified Palynological Preparation Technique for the Extraction of Large Neoproterozoic Acanthomorph Acritarchs and Other Acid-Insoluble Microfossils. 1999, Western Australia Geological Survey Record 1999/10.
Lin, R., Patrick Ritz, G., Studying individual macerals using i.r. microspectroscopy, and implications on oil versus gas/condensate proneness and “low-rank” generation. Org. Geochem. 20 (1993), 695–706.
Sekkal, M., Huvenne, J.P., Legrand, P., Sombret, B., Mollet, J.C., Mouradi-Givernaud, A., Verdus, M.C., Direct structural identification of polysaccharides from red algae by FTIR microspectroscopy I: Localization of agar in Gracilaria verrucosa, sections. Mikrochim. Acta 112 (1993), 1–10.
Alstadt, K.N., Katti, D.R., Katti, K.S., An in situ FTIR step-scan photoacoustic inverstigation of kerogen and minerals in oil shale. Spectrochim. Acta A Mol. Biomol. Spectrosc., Spectrochim Acta A 89 (2012), 105–113.
