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Origin and Early Evolution of the Eukaryotes: Perspectives from the Fossil Record

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Prebiotic Chemistry and the Origin of Life

Part of the book series: Advances in Astrobiology and Biogeophysics ((ASTROBIO))

Abstract

The emergence of a complex, eukaryotic cell is one of the major steps in the evolution of life on Earth. Eukaryotic organisms include a range of macroscopic life such as animals, plants, fungi, as well as a plethora of microscopic single-celled or colonial protists. The first evidence for eukaryotic life appears in the geologic record around 1650 million years ago (Ma), as organic-walled microfossils—cellular vesicles often preserved as carbonaceous compressions in siliciclastic rocks. Early eukaryotes were predominantly single-celled and minute for about a billion years, until the onset of macroscopic multicellularity in algae and animals in the Ediacaran Period (635–538 Ma). Here I review the earliest evidence of eukaryotic life, including a range of Proterozoic organic-walled microfossils and problematica. These fossils contain a suite of morphological and geochemical characters that offer clues about their palaeobiology. Complex microfossil morphology like spines can be considered a proxy for the appearance of a cytoskeleton, very early in eukaryote history, in the late Paleoproterozoic. Multidisciplinary studies on fossil features such as cell morphology, cell wall ultrastructure and its chemical composition, ancient forms of multicellularity, as well as understanding the environments these microorganisms inhabited, enable the use of the fossil record to inform the timing and mode of eukaryogenesis.

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References

  • Adam, Z.R., Skidmore, M.L., Mogk, D.W., Butterfield, N.J.: A Laurentian record of the earliest fossil eukaryotes. Geology. 45, 387–390 (2017)

    Article  ADS  Google Scholar 

  • Adl, S.M., Bass, D., Lane, E.C., Lukeš, J., Schoch, C.L., Smirnov, A., Agatha, S., Berney, C., Brown, M.W., Burki, F., Cárdenas, P.: Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Euk. Microbiol. 66, 4–119 (2019)

    Article  Google Scholar 

  • Agić, H., Cohen, P.A.: Non-pollen palynomorphs in deep time: unravelling the evolution of early eukaryotes, vol. 511, pp. 321–342. Geological Society, London, Special Publications (2021)

    Google Scholar 

  • Agić, H., Moczydłowska, M., Yin, L.: Affinity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi. China. J. Paleontol. 89, 28–50 (2015)

    Article  Google Scholar 

  • Agić, H., Moczydłowska, M., Canfield, D.E.: Reproductive cyst and operculum formation in the Cambrian-Ordovician galeate-plexus microfossils. GFF. 138, 278–294 (2016)

    Article  Google Scholar 

  • Agić, H., Moczydłowska, M., Yin, L.: Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang group, North China craton: a window into the early eukaryote evolution. Precambrian Res. 297, 101–130 (2017)

    Article  ADS  Google Scholar 

  • Akıl, C., Kitaoku, Y., Tran, L.T., Liebl, D., Choe, H., Muengsaen, D., Suginta, W., Schulte, A., Robinson, R.C.: Mythical origins of the actin cytoskeleton. Curr. Opin. Cell Biol. 68, 55–63 (2020)

    Article  Google Scholar 

  • Alberts, B., Johnson, A., Lewis, J., Morgan, D., Raff, M., Keith Roberts, P.W.: Molecular Biology of the Cell, 6th edn, p. 1464. W. W. Norton & Company, Boca Raton (2014)

    Google Scholar 

  • Anderson, R.P., Tosca, N.J., Cinque, G., Frogley, M.D., Lekkas, I., Akey, A., Hughes, G.M., Bergmann, K.D., Knoll, A.H., Briggs, D.E.: Aluminosilicate haloes preserve complex life approximately 800 million years ago. Interface Focus. 10, 20200011 (2020)

    Article  Google Scholar 

  • 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, 166–184 (2016)

    Article  ADS  Google Scholar 

  • Beghin, J., Storme, J.Y., Blanpied, C., Gueneli, N., Brocks, J.J., Poulton, S.W., Javaux, E.J.: Microfossils from the late Mesoproterozoic–early Neoproterozoic Atar/El Mreïti group, Taoudeni Basin, Mauritania, northwestern Africa. Precambrian Res. 291, 63–82 (2017)

    Article  ADS  Google Scholar 

  • Belmonte, G., Miglietta, A., Rubino, F., Boero, F.: Morphological convergence of resting stages of planktonic organisms: a review. Hydrobiologia. 355, 159–165 (1997)

    Article  Google Scholar 

  • Bernhard, J.M.: Experimental and field evidence of Antarctic foraminiferal tolerance to anoxia and hydrogen sulfide. Mar. Micropal. 20, 203–213 (1993)

    Article  Google Scholar 

  • Betts, H.C., Puttick, M.N., Clark, J.W., Williams, T.A., Donoghue, P.C., Pisani, D.: Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nat. Ecol. Evol. 2, 1556–1562 (2018)

    Article  Google Scholar 

  • Bhattacharya, D., Archibald, J.M., Weber, A.P., Reyes-Prieto, A.: How do endosymbionts become organelles? Understanding early events in plastid evolution. BioEssays. 29, 1239–1246 (2007)

    Article  Google Scholar 

  • Bogus, K., Harding, I.C., King, A., Charles, A.J., Zonneveld, K.A., Versteegh, G.J.: The composition and diversity of dinosporin in species of the Apectodinium complex (Dinoflagellata). Rev. Palaeobotany Palynol. 183, 21–31 (2012)

    Article  Google Scholar 

  • Bonner, J.T.: Aggregation and differentiation in the cellular slime molds. Ann. Rev. Microbiol. 25, 75–92 (1971)

    Article  Google Scholar 

  • Briggs, D.E., Summons, R.E.: Ancient biomolecules: their origins, fossilization, and role in revealing the history of life. BioEssays. 36, 482–490 (2014)

    Article  Google Scholar 

  • Brocks, J.J., Jarrett, A.J., Sirantoine, E., Hallmann, C., Hoshino, Y., Liyanage: The rise of algae in Cryogenian oceans and the emergence of animals. Nature. 548, 578–581 (2017)

    Article  ADS  Google Scholar 

  • Brooks, J., Shaw, G.: Sporopollenin: a review of its chemistry, palaeochemistry and geochemistry. Grana. 17, 91–97 (1978)

    Article  Google Scholar 

  • Burki, F., Roger, A.J., Brown, M.W., Simpson, A.G.: The new tree of eukaryotes. Trends Ecol. Evol. 35, 43–55 (2020)

    Article  Google Scholar 

  • Butterfield, N.J.: Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology. 26, 386–404 (2000)

    Article  Google Scholar 

  • Butterfield, N.J.: Probable proterozoic fungi. Paleobiology. 31, 65–182 (2005)

    Article  Google Scholar 

  • Butterfield, N.J.: Modes of pre-Ediacaran multicellularity. Precambrian Research. 173, 201–211 (2009)

    Article  ADS  Google Scholar 

  • Butterfield, N.J.: Early evolution of the Eukaryota. Palaeontology. 58, 5–17 (2015a)

    Article  Google Scholar 

  • Butterfield, N.J.: Proterozoic photosynthesis—a critical review. Palaeontology. 58, 953–972 (2015b)

    Article  Google Scholar 

  • Butterfield, N.J., Knoll, A.H., Swett, K.: Paleobiology of the Neoproterozoic Svanbergfjellet formation, Spitsbergen. Fossils Strata. 34, 1–84 (1994)

    Google Scholar 

  • Calderón, E., Tavera, R.: New observations on the sexual and asexual reproductive stages of Staurastrum gracile (Desmidiaceae, Zygnematophyceae). Phycologia. 59, 409–421 (2020)

    Article  Google Scholar 

  • Cohen, P.A., Macdonald, F.A.: The Proterozoic record of eukaryotes. Paleobiology. 41, 610–632 (2015)

    Article  Google Scholar 

  • Cohen, P.A., Strauss, J.V., Rooney, A.D., Sharma, M., Tosca, N.: Controlled hydroxyapatite biomineralization in an ~810 million-year-old unicellular eukaryote. Sci. Adv. 3, e1700095 (2017)

    Article  ADS  Google Scholar 

  • Colbath, G.K., Grenfell, H.R.: Review of biological affinities of Paleozoic acid-resistant, organic-walled eukaryotic algal microfossils (including “acritarchs”). Rev. Palaeobot. Palynol. 86, 287–314 (1995)

    Article  Google Scholar 

  • Corliss, J.O.: Protozoan cysts and spores. eLS. 1, 1–8 (2001)

    Google Scholar 

  • Courties, C., Vaquer, A., Troussellier, A., Lautier, J., Chrétiennot-Dinet, M.J., Neveux, J., Machado, C., Claustre: Smallest eukaryotic organism. Nature. 370, 255–255 (1994)

    Article  ADS  Google Scholar 

  • Dacks, J.B., Field, M.C., Buick, R., Eme, L., Gribaldo, S., Roger, A.J., Brochier-Armanet, C., Devos, D.P.: The changing view of eukaryogenesis–fossils, cells, lineages and how they all come together. J. Cell Sci. 129, 3695–3703 (2016)

    Google Scholar 

  • Darwin, C.: On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, p. 502. John Murray, London (1859)

    Book  Google Scholar 

  • de Leeuw, J.W., Versteegh, G.J., van Bergen, P.F.: Biomacromolecules of algae and plants and their fossil analogues. Plant Ecol. 182, 209–233 (2006)

    Article  Google Scholar 

  • Desmond, E., Gribaldo, S.: Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature. GBE. 1, 364–381 (2009)

    Google Scholar 

  • Dodds, W.K., Castenholz, R.W.: Effects of grazing and light on the growth of Nostoc pruniforme (cyanobacteria). Br. Phycol. J. 23, 219–227 (1988)

    Article  Google Scholar 

  • Edgcomb, V.P., Leadbetter, E.R., Bourland, W., Beaudoin, D., Bernhard, J.: Structured multiple endosymbiosis of bacteria and archaea in a ciliate from marine sulfidic sediments: a survival mechanism in low oxygen, sulfidic sediments? Front. Microbiol. 2, 1344–1356 (2011)

    Article  Google Scholar 

  • Eme, L., Ettema, T.J.: The eukaryotic ancestor shapes up. Nature. 562, 352–353 (2018)

    Article  ADS  Google Scholar 

  • Eme, L., Sharp, S.C., Brown, M.W., Roger, A.J.: On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. CSH Perspect. Biol. 6, a016139 (2014)

    Google Scholar 

  • Erwin, D.H., Laflamme, M., Tweedt, S.M., Sperling, E.A., Pisani, D., Peterson, K.J.: The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science. 334, 1091–1097 (2011)

    Article  ADS  Google Scholar 

  • Ettema, T.J., Lindås, A.C., Bernander, R.: An actin-based cytoskeleton in archaea. Mol. Microbiol. 80, 1052–1061 (2011)

    Article  Google Scholar 

  • Fischer, W.W., Hemp, J., Valentine, J.S.: How did life survive Earth’s great oxygenation? Curr. Opin. Chem. Biol. 31, 166–178 (2016)

    Article  Google Scholar 

  • Gibson, T.M., Shih, P.M., Cumming, V.M., Fischer, W.W., Crockford, P.W., Hodgskiss, M.S., Wörndle, S., Creaser, R.A., Rainbird, R.H., Skulski, T.M., Halverson, G.P.: Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology. 46, 135–138 (2018)

    Article  ADS  Google Scholar 

  • Gold, D.A., Caron, A., Fournier, G.P., Summons, R.E.: Paleoproterozoic sterol biosynthesis and the rise of oxygen. Nature. 543, 420–423 (2017)

    Article  ADS  Google Scholar 

  • Golubic, S., Seong-Joo, L.: Early cyanobacterial fossil record: preservation, palaeoenvironments and identification. Eur. J. Phycol. 34, 339–348 (1999)

    Article  Google Scholar 

  • Goodenough, U., Heitman: Origins of eukaryotic sexual reproduction. CSH Perspect. Biol. 6, a016154 (2014)

    Google Scholar 

  • Grant, C.R., Wan, J., Komeili, A.: Organelle formation in Bacteria and archaea. Annu. Rev. Cell Dev. Biol. 34, 217–238 (2018)

    Article  Google Scholar 

  • Grey, K.: A modified palynological preparation technique for the extraction of large Neoproterozoic acanthomorph acritarchs and other acid insoluble microfossils, vol. 10, pp. 1–23. Geological Survey of Western Australia Record, Nottingham (1999)

    Google Scholar 

  • Grey, K.: Ediacaran palynology of Australia. Mem. Assoc. Austral. Palaeontol. 31, 1–439 (2005)

    Google Scholar 

  • Gross, J., Bhattacharya, D.: Uniting sex and eukaryote origins in an emerging oxygenic world. Biol. Dir. 5, 53 (2010)

    Article  Google Scholar 

  • Gumsley, A.P., Chamberlain, K.R., Bleeker, W., Söderlund, U., de Kock, M.O., Larsson, E.R., Bekker, A.: Timing and tempo of the great oxidation event. PNAS. 114, 1811–1816 (2017)

    Article  ADS  Google Scholar 

  • Hagen, C., Siegmund, S., Braune, W.: Ultrastructural and chemical changes in the cell wall of Haematococcus pluvialis (Volvocales, Chlorophyta) during aplanospore formation. Eur. J. Phycol. 37 217–226 (2002)

    Article  Google Scholar 

  • Hairston Jr., N.G., Van Brunt, R.A., Kearns, C.M., Engstrom, D.R.: Age and survivorship of diapausing eggs in a sediment egg bank. Ecology. 76, 1706–1711 (1995)

    Article  Google Scholar 

  • Han, T.M., Runnegar, B.: Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee iron-formation, Michigan. Science. 257, 232–235 (1992)

    Article  ADS  Google Scholar 

  • Hedges, J.I.: Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar. Chem. 49, 81–115 (1995)

    Article  Google Scholar 

  • Hermann, T.N.: Organic world billion years ago. Nauka, Leningrad (1990)

    Google Scholar 

  • Herskowitz, I.: Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 52, 536 (1988)

    Article  Google Scholar 

  • 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, 141–152 (2019)

    Article  ADS  Google Scholar 

  • Hoffman, P.F., Abbot, D.S., Ashkenazy, Y., Benn, D.I., Brocks, J.J., Cohen, P.A., Cox, G.M., Creveling, J.R., Donnadieu, Y., Erwin, D.H., Fairchild, I.J.: Snowball Earth climate dynamics and cryogenian geology-geobiology. Sci. Adv. 3, e1600983 (2017)

    Article  ADS  Google Scholar 

  • Holland, H.D.: The oxygenation of the atmosphere and oceans. Philos. Trans. R. Soc. B. 361, 903–915 (2006)

    Article  Google Scholar 

  • Hoops, H.J., Brighton, M.C., Stickles, S.M., Clement, P.R.: A test of two possible mechanisms for phototactic steering in Volvox carteri (Chlorophyceae). J Phycol. 35(3), 539–547 (1999)

    Article  Google Scholar 

  • Hoshino, Y., Poshibaeva, A., Meredith, W., Snape, C., Poshibaev, V., Versteegh, G.J., Kuznetsov, N., Leider, A., van Maldegem, L., Neumann, M., Naeher, S., Moczydłowska, M., Brocks, J.J., Jarret, A.J.M., Tang, Q., Xiao, S., McKirdy, D., Kumar, S., Alvaro, J.J., Sansjofre, P., Hallmann, C.: Cryogenian evolution of stigmasteroid biosynthesis. Sci. Adv. 3, e1700887 (2017)

    Article  ADS  Google Scholar 

  • Huntley, J.W., Xiao, S., Kowalewski, M.: 1.3 billion years of acritarch history: an empirical morphospace approach. Precambrian Res. 144, 52–68 (2006)

    Article  ADS  Google Scholar 

  • Imachi, H., Nobu, M.K., Nakahara, N., Morono, Y., Ogawara, M., Takaki, Y., Takano, Y., Uematsu, K., IkutaT, I.M., Matsui, Y.: Isolation of an archaeon at the prokaryote–eukaryote interface. Nature. 577, 519–525 (2019)

    Article  ADS  Google Scholar 

  • Isson, T.T., Love, G.D., Dupont, C.L., Reinhard, C.T., Zumberge, A.J., Asael, D., Gueguen, B., McCrow, J., Gill, B.C., Owens, J., Rainbird, R.H.: Tracking the rise of eukaryotes to ecological dominance with zinc isotopes. Geobiology. 16, 341–352 (2018)

    Article  Google Scholar 

  • Javaux, E.J., Knoll, A.H.: Micropaleontology of the lower Mesoproterozoic Roper Group, Australia, and implications for early eukaryotic evolution. J. Paleontol. 91, 199–229 (2017)

    Article  Google Scholar 

  • Javaux, E.J., Lepot, K.: The Paleoproterozoic fossil record: implications for the evolution of the biosphere during Earth’s middle-age. Earth Sci. Rev. 176, 68–86 (2018)

    Article  ADS  Google Scholar 

  • Javaux, E.J., Knoll, A.H., Walter, M.R.: Morphological and ecological complexity in early eukaryotic ecosystems. Nature. 412, 66–69 (2001)

    Article  ADS  Google Scholar 

  • Javaux, E.J., Knoll, A.H., Walter, M.R.: TEM evidence for eukaryotic diversity in mid-Proterozoic oceans. Geobiology. 2, 121–132 (2004)

    Article  Google Scholar 

  • Javaux, E.J., Marshall, C.P., Bekker, A.: Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature. 463, 934–938 (2010)

    Article  ADS  Google Scholar 

  • Knoll, A.H., Javaux, E.J., Hewitt, D., Cohen, P.: Eukaryotic organisms in Proterozoic oceans. Philos. Trans. R. Soc. B. 361, 1023–1038 (2006)

    Article  Google Scholar 

  • Kodner, R.B., Summons, R.E., Knoll, A.H.: Phylogenetic investigation of the aliphatic, non-hydrolyzable biopolymer algaenan, with a focus on green algae. Org. Geochem. 40, 854–862 (2009)

    Article  Google Scholar 

  • Kokinos, J. P., Anderson, D. M.: Morphological development of resting cysts in cultures of the marine dinoflagellate Lingulodinium polyedrum (= L. machaerophorum). Palynology. 19, 143–166 (1995)

    Article  Google Scholar 

  • Koonin, E.V.: The origin and early evolution of eukaryotes in the light of phylogenomics. Genome. Biol. 11, 209 (2010)

    Article  Google Scholar 

  • Kremp, A., Rengefors, K., Montresorc, M.: Species specific encystment patterns in three Baltic cold-water dinoflagellates: the role of multiple cues in resting cyst formation. Limnol. Oceanogr. 54, 1125–1138 (2009)

    Article  ADS  Google Scholar 

  • Lane, N.: Energetics and genetics across the prokaryote-eukaryote divide. Biol. Dir. 6, 1–31 (2011)

    Article  Google Scholar 

  • Li, C., Planavsky, N.J., Love, G.D., Reinhard, C.T., Hardisty, D., Feng, L., Bates, S.M., Huang, J., Zhang, Q., Chu, X., Lyons, T.W.: Marine redox conditions in the middle Proterozoic Ocean and isotopic constraints on authigenic carbonate formation: insights from the Chuanlinggou formation, Yanshan Basin, North China. Geochim. Cosmochim. Acta. 150, 90–105 (2015)

    Article  ADS  Google Scholar 

  • López-García, P., Eme, L., Moreira, D.: Symbiosis in eukaryotic evolution. J. Theor. Biol. 434, 20–33 (2017)

    Article  ADS  Google Scholar 

  • 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, 232–235 (2019)

    Article  ADS  Google Scholar 

  • Love, G.D., Grosjean, E., Stalvies, C., Fike, D.A., Grotzinger, J.P., Bradley, A.S., Kelly, A.E., Bhatia, M., Meredith, W., Snape, C.E., Bowring, S.A.: Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature. 457, 718–721 (2009)

    Article  ADS  Google Scholar 

  • Lyons, T.W., Reinhard, C.T., Planavsky, N.J.: The rise of oxygen in Earth’s early ocean and atmosphere. Nature. 506, 307–315 (2014)

    Article  ADS  Google Scholar 

  • Marshall, C.P., Javaux, E.J., Knoll, A.H., Walter, M.: Combined micro-Fourier transform infrared (FTIR) spectroscopy and micro-Raman spectroscopy of Proterozoic acritarchs: a new approach to palaeobiology. Precambrian Res. 138, 208–224 (2005)

    Article  ADS  Google Scholar 

  • Martin, W.F., Garg, S., Zimorski, V.: Endosymbiotic theories for eukaryote origin. Philos. Trans. R. Soc. B. 370, 20140330 (2015)

    Article  Google Scholar 

  • McFadden, G.I., Preisig, H.R., Melkonian, M.: Golgi apparatus activity and membrane flow during scale biogenesis in the green flagellate Scherffelia dubia (Prasinophyceae). II: Cell wall secretion and assembly. Protoplasma. 131, 174–184 (1986)

    Article  Google Scholar 

  • Miao, L., Moczydłowska, M., Zhu, S., Zhu, M.: New record of organic-walled, morphologically distinct microfossils from the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China. Precambrian Res. 321, 172–198 (2019)

    Article  ADS  Google Scholar 

  • Möbius, K.: Das Sterben der einzelligen und der vielzelligen Tiere. Vergleichend betrachtet. Biologisches Centralblatt. 4, 389–392 (1884)

    Google Scholar 

  • Moczydłowska, M., Willman, S.: Ultrastructure of cell walls in ancient microfossils as a proxy to their biological affinities. Precambrian Res. 173, 27–38 (2009)

    Article  ADS  Google Scholar 

  • Moczydłowska, M., Landing, E.D., Zang, W., Palacios, T.: Proterozoic phytoplankton and timing of chlorophyte algae origins. Palaeontology. 54, 721–733 (2011)

    Article  Google Scholar 

  • Morozov, A.A., Likhoshway, Y.V.: Evolutionary history of the chitin synthases of eukaryotes. Glycobiology. 26, 635–639 (2016)

    Article  Google Scholar 

  • Nagovitsin, K.: Tappania-bearing association of the Siberian platform: biodiversity, stratigraphic position and geochronological constraints. Precambrian Res. 173, 137–145 (2009)

    Article  ADS  Google Scholar 

  • Neuhaus-Url, G., Schweiger, H.G.: The lid forming apparatus in cysts of the green alga Acetabularia mediterranea. Protoplasma. 122, 120–124 (1984)

    Article  Google Scholar 

  • Pace, N.R.: Mapping the tree of life: progress and prospects. Microbiol Mol Biol Rev. 73(4), 565–576 (2009)

    Article  Google Scholar 

  • Pahlow, M., Riebesell, U., Wolf-Gladrow, D.A.: Impact of cell shape and chain formation on nutrient acquisition by marine diatoms. Limnol. Oceanogr. 42, 1660–1672 (1997)

    Article  ADS  Google Scholar 

  • Pang, K., Tang, Q., Yuan, X.L., Wan, B., Xiao, S.: A biomechanical analysis of the early eukaryotic fossil Valeria and new occurrence of organic-walled microfossils from the paleo-Mesoproterozoic Ruyang Group. Palaeoworld. 24, 251–262 (2015)

    Article  Google Scholar 

  • Payne, J.L., Boyer, A.G., Brown, J.H., Finnegan, S., Kowalewski, M., Krause, R.A., Lyons, S.K., McClain, C.R., McShea, D.W., Novack-Gottshall, P.M., Smith, F.A.: Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. PNAS. 106, 24–27 (2009)

    Article  ADS  Google Scholar 

  • Pederson, T.: The nucleus introduced. CSH Perspect. Biol. 3, a000521 (2011)

    Google Scholar 

  • Peng, Y., Bao, H., Yuan, X.: New morphological observations for paleoproterozoic acritarchs from the Chuanlinggou formation, North China. Precambrian Res. 168, 223–232 (2009)

    Article  ADS  Google Scholar 

  • Porter, S.M.: Tiny vampires in ancient seas: evidence for predation via perforation in fossils from the 780–740 million-year-old Chuar group, grand canyon, USA. Proc. R. Soc. B. 283, 20160221 (2016)

    Article  Google Scholar 

  • Porter, S.M.: Insights into eukaryogenesis from the fossil record. Interface Focus. 10, 20190105 (2020)

    Article  Google Scholar 

  • Porter, S.M., Knoll, A.H.: Testate amoebae in the Neoproterozoic era: evidence from vase-shaped microfossils in the Chuar Group, Grand Canyon. Paleobiology. 26, 360–385 (2000)

    Article  Google Scholar 

  • Porter, S.M., Riedman, L.A.: Systematics of organic-walled microfossils from the ca. 780–740 Ma Chuar Group, Grand Canyon. Arizona. J. Paleontol. 90, 815–853 (2016)

    Article  Google Scholar 

  • Porter, S.M., Agić, H., Riedman, L.A.: Anoxic ecosystems and early eukaryotes. Emerg. Top. Life Sci. 2, 299–309 (2018)

    Article  Google Scholar 

  • Prasad, B., Uniyal, S.N., Asher, R.: Organic-walled microfossils from the Proterozoic Vindhyan Supergroup of Son Valley, Madhya Pradesh, India. Palaeobotanist. 54, 13–60 (2005)

    Google Scholar 

  • Quigg, A., Irwin, A.J., Finkel, Z.V.: Evolutionary inheritance of elemental stoichiometry in phytoplankton. Proc. R. Soc. B. 278, 526–534 (2011)

    Article  Google Scholar 

  • Reinhard, C.T., Planavsky, N.J., Ward, B.A., Love, G.D., Le Hir, G., Ridgwell, A.: The impact of marine nutrient abundance on early eukaryotic ecosystems. Geobiology. 18, 139–151 (2020)

    Article  Google Scholar 

  • Riedman, L.A., Porter, S.: Organic-walled microfossils of the mid-Neoproterozoic Alinya Formation, Officer Basin, Australia. J Paleontol. 90(5), 854–887 (2016)

    Article  Google Scholar 

  • Sadoff, H.L.: Encystment and germination in Azotobacter vinelandii. Microbiol. Rev. 39, 516–539 (1975)

    Google Scholar 

  • Sagan, L.: On the origin of mitosing cells. J. Theor. Biol. 14, 225–274 (1967)

    Article  ADS  Google Scholar 

  • Samuelsson, J., Butterfield, N. J.: Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications. Precambrian Research. 107, 235–251 (2001)

    Article  ADS  Google Scholar 

  • Schaap, P., Schilde, C.: Encystation: the most prevalent and underinvestigated differentiation pathway of eukaryotes. Microbiology. 164, 727–739 (2018)

    Article  Google Scholar 

  • Schiffbauer, J.D., Wallace, A.F., Hunter Jr., J.L., Kowalewski, M., Bodnar, R.J., Xiao, S.: Thermally-induced structural and chemical alteration of organic-walled microfossils: an experimental approach to understanding fossil preservation in metasediments. Geobiology. 10, 402–423 (2012)

    Article  Google Scholar 

  • Schirrmeister, B.E., Sanchez-Baracaldo, P., Wacey, D.: Cyanobacterial evolution during the Precambrian. Int. J. Astrobiol. 15, 187–204 (2016)

    Article  ADS  Google Scholar 

  • Schopf, J.W.: Atlas of representative Proterozoic microfossils. In: Schopf, J.W., Klein, C. (eds.) The Proterozoic biosphere: a multidisciplinary study, pp. 1055–1117. Cambridge University Press, Cambridge (1992)

    Chapter  Google Scholar 

  • Schopf, J.W., Kudryavtsev, A.B., Agresti, D.G., Czaja, A.D., Wdowiak, T.J.: Raman imagery: a new approach to assess the geochemical maturity and biogenicity of permineralized Precambrian fossils. Astrobiology. 5, 333–371 (2005)

    Article  ADS  Google Scholar 

  • Schulz, H.N., Brinkhoff, T., Ferdelman, T.G., Marine, M.H., Teske, A., Jørgensen, B.B.: Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science. 284, 493–495 (1999)

    Article  ADS  Google Scholar 

  • Sergeeva, N.G., Gooday, A.J., Mazlumyan, S.A., Kolesnikova, E.A., Lichtschlag, A., Kosheleva, T.N., Anikeeva, O.V.: Meiobenthos of the oxic/anoxic interface in the southwestern region of the Black Sea: abundance and taxonomic composition. In: Altenbach, A.V., Bernhard, J.M., Seckbach, J. (eds.) Anoxia, pp. 369–401. Springer, Dordrecht (2012)

    Chapter  Google Scholar 

  • Sergeev, V. N., Knoll, A. H., Vorob’eva, N. G., Sergeeva, N. D.: Microfossils from the lower Mesoproterozoic Kaltasy Formation, East European Platform. Precambrian Research. 278, 87–107 (2016)

    Article  ADS  Google Scholar 

  • Smith, M.R.: Cord-forming Palaeozoic fungi in terrestrial assemblages. Bot. J. Linn. Soc. 180, 452–460 (2016)

    Article  Google Scholar 

  • Spang, A., Saw, J.H., Jørgensen, S.L., Zaremba-Niedzwiedzka, K., Martijn, J., Lind, A.E., Van Eijk, R., Schleper, C., Guy, L., Ettema, T.J.: Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature. 521, 173–179 (2015)

    Article  ADS  Google Scholar 

  • Speijer, D.: What can we infer about the origin of sex in early eukaryotes? Philos. Trans. R. Soc. B. 371, 20150530 (2016)

    Article  Google Scholar 

  • Sperling, E.A., Rooney, A.D., Hays, L., Sergeev, V.N., Vorob’Eva, N.G., Sergeeva, N.D., Selby, D., Johnston, D.T., Knoll, A.H.: Redox heterogeneity of subsurface waters in the Mesoproterozoic ocean. Geobiology. 12, 373–386 (2014)

    Article  Google Scholar 

  • Stockner, J.G.: Phototrophic picoplankton: an overview from marine and freshwater ecosystems. Limnol. Oceanogr. 33, 765–775 (1988)

    ADS  Google Scholar 

  • Strullu-Derrien, C., Kenrick, P., Knoll, A.H.: The Rhynie chert. Curr. Biol. 29, R1218–R1223 (2019)

    Article  Google Scholar 

  • Stüeken, E.E.: A test of the nitrogen-limitation hypothesis for retarded eukaryote radiation: nitrogen isotopes across a Mesoproterozoic basinal profile. Geochim. Cosmochim. Acta. 120, 121–139 (2013)

    Article  ADS  Google Scholar 

  • Suda, S., Watanabe, M.M., Inouye, I.: Electron microscopy of sexual reproduction in Nephroselmis olivacea (Prasinophyceae, Chlorophyta). Phycol. Res. 52, 273–283 (2004)

    Article  Google Scholar 

  • Tang, Q., Pang, K., Xiao, S., Yuan, X., Ou, Z., Wan, B.: Organic-walled microfossils from the early Neoproterozoic Liulaobei Formation in the Huainan region of North China and their biostratigraphic significance. Precambrian Res. 236, 157–181 (2013)

    Article  ADS  Google Scholar 

  • Tang, Q., Pang, K., Yuan, X., Wan, B., Xiao, S.: Organic-walled microfossils from the Tonian Gouhou formation, Huaibei region, North China Craton, and their biostratigraphic implications. Precambrian Res. 266, 296–318 (2015)

    Article  ADS  Google Scholar 

  • Tang, Q., Pang, K., Yuan, X., Xiao, S.: A one-billion-year-old multicellular chlorophyte. Nat. Ecol. Evol. 4, 543–549 (2020)

    Article  Google Scholar 

  • Torruella, G., De Mendoza, A., Grau-Bove, X., Anto, M., Chaplin, M.A., Del Campo, J., Eme, L., Pérez-Cordón, G., Whipps, C.M., Nichols, K.M., Paley, R.: Phylogenomics reveals convergent evolution of lifestyles in close relatives of animals and fungi. Curr. Biol. 25, 2404–2410 (2015)

    Article  Google Scholar 

  • Tyler, S.A., Barghoorn, E.S.: Occurrence of structurally preserved plants in pre-Cambrian rocks of the Canadian shield. Science. 119, 606–608 (1954)

    Article  ADS  Google Scholar 

  • Wacey, D., Kilburn, M.R., Saunders, M., Cliff, J., Brasier, M.D.: Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nat. Geosci. 4, 698–702 (2011)

    Article  ADS  Google Scholar 

  • Wang, Y., Wang, Y., Du, W.: The long-ranging macroalga Grypania spiralis from the Ediacaran Doushantuo Formation, Guizhou, South China. Alcheringa: An Australasian Journal of Palaeontology. 40, 303–312 (2016)

    Article  Google Scholar 

  • Waterbury, J., Stanier, R.: Two unicellular cyanobacteria which reproduce by budding. Arch. Microbiol. 115, 249–257 (1977)

    Article  Google Scholar 

  • Wei, J.H., Yin, X., Welander, P.V.: Sterol synthesis in diverse bacteria. Front. Microbiol. 7, 990 (2016)

    Article  Google Scholar 

  • Woltz, C.R., Porter, S.M., Agić, H., Dehler, C.M., Junium, C.K., Riedman, L.A., Hodgskiss, M.S.W., Wörndle, S. and Halverson, G.P.: Total organic carbon and the preservation of organic-walled microfossils in Precambrian shale. Geology. 49, 556–560 (2021)

    Google Scholar 

  • Wood, R.: Exploring the drivers of early biomineralization. Emerg. Top. Life Sci. 2, 201–212 (2018)

    Article  Google Scholar 

  • Wörndle, S., Crockford, P.W., Kunzmann, M., Bui, T.H., Halverson, G.P.: Linking the Bitter Springs carbon isotope anomaly and early neoproterozoic oxygenation through I/[Ca+ Mg] ratios. Chem. Geol. 524, 119–135 (2019)

    Article  ADS  Google Scholar 

  • Xiao, S., Knoll, A.H., Kaufman, A.J., Yin, L., Zhang, Y.: Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China platform. Precambrian Res. 84, 197–220 (1997)

    Article  ADS  Google Scholar 

  • Xiao, S., Muscente, A.D., Chen, L., Zhou, C., Schiffbauer, J.D., Wood, A.D., Polys, N.F., Yuan, X.: The Weng’an biota and the Ediacaran radiation of multicellular eukaryotes. Nat. Sci. Rev. 1, 498–520 (2014)

    Article  Google Scholar 

  • Ye, Q., Tong, J., Xiao, S., Zhu, S., An, Z., Tian, L., Hu, J.: The survival of benthic macroscopic phototrophs on a Neoproterozoic snowball earth. Geology. 43, 507–510 (2015)

    Article  ADS  Google Scholar 

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Acknowledgements

The editors Sean McMahon and Anna Neubeck are thanked for their kind invitation to contribute to this book. Constructive discussions about prokaryotic and protistan evolution and ecology with David Chapman and Susannah Porter (UC Santa Barbara) greatly benefitted the manuscript. Corentin Loron (U. Liège) kindly provided additional fossil images. I am grateful to Ross Anderson, Ben Slater, and Sebastian Willman for providing valuable reviews which improved this chapter. This work was supported by NSF grant EAR-1855092.

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Agić, H. (2021). Origin and Early Evolution of the Eukaryotes: Perspectives from the Fossil Record. In: Neubeck, A., McMahon, S. (eds) Prebiotic Chemistry and the Origin of Life. Advances in Astrobiology and Biogeophysics. Springer, Cham. https://doi.org/10.1007/978-3-030-81039-9_11

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