1932

Abstract

The origin of modern eukaryotes is one of the key transitions in life's history, and also one of the least understood. Although the fossil record provides the most direct view of this process, interpreting the fossils of early eukaryotes and eukaryote-grade organisms is not straightforward. We present two end-member models for the evolution of modern (i.e., crown) eukaryotes—one in which modern eukaryotes evolved early, and another in which they evolved late—and interpret key fossils within these frameworks, including where they might fit in eukaryote phylogeny and what they may tell us about the evolution of eukaryotic cell biology and ecology. Each model has different implications for understanding the rise of complex life on Earth, including different roles of Earth surface oxygenation, and makes different predictions that future paleontological studies can test.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-032421-113254
2023-09-15
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/77/1/annurev-micro-032421-113254.html?itemId=/content/journals/10.1146/annurev-micro-032421-113254&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adam ZR, Skidmore ML, Mogk DW, Butterfield NJ. 2017. A Laurentian record of the earliest fossil eukaryotes. Geology 45:387–90
    [Google Scholar]
  2. 2.
    Agić H. 2021. Origin and early evolution of the eukaryotes: perspectives from the fossil record. Prebiotic Chemistry and the Origin of Life A Neubeck, S McMahon 255–89. Cham, Switz.: Springer
    [Google Scholar]
  3. 3.
    Agić H, Cohen PA 2021. Non-pollen palynomorphs in deep time: unraveling the evolution of early eukaryotes. Applications of Non-Pollen Palynomorphs: From Palaeoenvironmental Reconstructions to Biostra-tigraphy F Marret, J O'Keefe, P Osterloff, M Pound, L Shumilovskikh 321–42. Spec. Publ. 511 London: Geol. Soc.
    [Google Scholar]
  4. 4.
    Agić H, Moczydłowska M, Yin L. 2015. Affinity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China. J. Paleontol. 89:28–50
    [Google Scholar]
  5. 5.
    Agić H, Moczydłowska M, Yin L. 2017. Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton—a window into the early eukaryote evolution. Precambrian Res. 297:101–30
    [Google Scholar]
  6. 6.
    Allison CW, Hilgert JW 1986. Scale microfossils from the early Cambrian of northwest Canada. J. Paleontol. 60:973–1015
    [Google Scholar]
  7. 7.
    Anbar AD. 2008. Elements and evolution. Science 322:1481–83
    [Google Scholar]
  8. 8.
    Anderson OR. 1988. Fine structure of silica deposition and the origin of shell components in a testate amoebae Netzelia tuberculata. J. Protozool. 35:204–11
    [Google Scholar]
  9. 9.
    Anderson OR. 1994. Cytoplasmic origin and surface deposition of siliceous structures in Sarcodina. Protoplasma 181:61–77
    [Google Scholar]
  10. 10.
    Bengtson S, Rasmussen B, Krapež B. 2007. The Paleoproterozoic megascopic Stirling biota. Paleobiology 33:351–81
    [Google Scholar]
  11. 11.
    Bengtson S, Sallstedt T, Belivanova V, Whitehouse M. 2017. Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLOS Biol. 15:3e2000735
    [Google Scholar]
  12. 12.
    Betts HC, Puttick MN, Clark JW, Williams TA, Donoghue PCJ, Pisani D. 2018. Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin. Nat. Ecol. Evol. 2:1556–62
    [Google Scholar]
  13. 13.
    Breuninger RH. 2019. Depositional environment of Horodyskia (‘string of beads’) from the early Mesoproterozoic Greyson and Spokane Formations of the Belt Supergroup, near Helena, Montana, USA. Northwest Geol. 48:41–54
    [Google Scholar]
  14. 14.
    Brocks JJ. 2018. The transition from a cyanobacterial to algal world and the emergence of animals. Emerg. Top. Life Sci. 2:181–90
    [Google Scholar]
  15. 15.
    Brugerolle G. 2004. Devescovinid features, a remarkable surface cytoskeleton, and epibiotic bacteria revisited in Mixotricha paradoxa, a parabasalid flagellate. Protoplasma 224:49–59
    [Google Scholar]
  16. 16.
    Budd GE, Jensen S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. Camb. Philos. Soc. 75:253–95
    [Google Scholar]
  17. 17.
    Budd GE, Mann RP. 2020. The dynamics of stem and crown groups. Sci. Adv. 6:eaaz1626
    [Google Scholar]
  18. 18.
    Butterfield NJ. 2000. Bangiomorpha pubescens n. gen., n. sp.: Implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404
    [Google Scholar]
  19. 19.
    Butterfield NJ. 2009. Modes of pre-Ediacaran multicellularity. Precambrian Res. 173:201–11
    [Google Scholar]
  20. 20.
    Butterfield NJ. 2015. Early evolution of the Eukaryota. Palaeontology 58:5–17
    [Google Scholar]
  21. 21.
    Butterfield NJ. 2020. Constructional and functional anatomy of Ediacaran rangeomorphs. Geolog. Mag. 159:1148–59
    [Google Scholar]
  22. 22.
    Calver CR, Grey K, Laan M. 2010. The ‘string of beads’ fossil (Horodyskia) in the mid-Proterozoic of Tasmania. Precambrian Res. 180:18–25
    [Google Scholar]
  23. 23.
    Carlisle EM, Jobbins M, Pankhania V, Cunningham JA, Donoghue PCJ. 2021. Experimental taphonomy of organelles and the fossil record of early eukaryote evolution. Sci. Adv. 7:eabe9487
    [Google Scholar]
  24. 24.
    Cavalier-Smith T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int. J. Syst. Evol. Microbiol. 52:297–354
    [Google Scholar]
  25. 25.
    Chernikova D, Motamedi S, Csürös M, Koonin EV, Rogozin IB. 2011. A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes. Biol. Direct 6:26
    [Google Scholar]
  26. 26.
    Cleveland LR, Grimstone AV. 1964. The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Proc. R. Soc. Lond. B 159:668–86
    [Google Scholar]
  27. 27.
    Cohen PA, Knoll AH. 2012. Scale microfossils from the mid-Neoproterozoic Fifteenmile Group, Yukon Territory. J. Paleontol. 86:775–800
    [Google Scholar]
  28. 28.
    Cohen PA, Kodner RB. 2021. The earliest history of eukaryotic life: uncovering an evolutionary story through the integration of biological and geological data. Trends Ecol. Evol. 37:246–56
    [Google Scholar]
  29. 29.
    Cohen PA, Riedman LA. 2018. It's a protist-eat-protist world: recalcitrance, predation, and evolution in the Tonian–Crypgenian ocean. Emerging Top. Life Sci. 2:173–80
    [Google Scholar]
  30. 30.
    Cohen PA, Schopf JW, Butterfield NJ, Kudryavstev AB, Macdonald FA. 2011. Phosphate biomineralization in mid-Neoproterozoic protists. Geology 39:539–42
    [Google Scholar]
  31. 31.
    Cohen PA, Strauss JV, Rooney AD, Sharma M, Tosca N. 2017. Controlled hydroxyapatite biomineralization in a ∼810 million-year-old unicellular eukaryote. Sci. Adv. 3:e1700095
    [Google Scholar]
  32. 32.
    Crockford PW, Hayles JA, Bao H, Planavsky NJ, Bekker A et al. 2018. Triple oxygen isotope evidence for limited mid-Proterozoic primary productivity. Nature 559:613–16
    [Google Scholar]
  33. 33.
    Cuthill JFH, Conway Morris S. 2014. Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic body plan. Proc. R. Soc. Lond. B 111:13122–26
    [Google Scholar]
  34. 34.
    Desmond E, Gribaldo S. 2009. Phylogenomics of sterol synthesis: insights into the origin, evolution and diversity of a key eukaryotic feature. Genome Biol. Evol. 2009:364–81
    [Google Scholar]
  35. 35.
    Dong L, Xiao S, Shen B, Zhou C. 2008. Silicified Horodyskia and Palaeopascichnus from upper Ediacaran cherts in South China: tentative phylogenetic interpretation and implications for evolutionary stasis. J. Geol. Soc. Lond. 165:367–78
    [Google Scholar]
  36. 36.
    Donoghue PCJ. 2005. Saving the stem group—a contradiction in terms?. Paleobiology 31:553–58
    [Google Scholar]
  37. 37.
    Donoghue PCJ, Antcliffe JB. 2010. Origins of multicellularity. Nature 466:41–42
    [Google Scholar]
  38. 38.
    Dunn FS, Liu AG, Grazhdankin DV, Vixseboxse P, Flannery-Sutherland J et al. 2021. The developmental biology of Charnia and the eumetazoan affinity of the Ediacaran rangeomorphs. Sci. Adv. 7:eabe0291
    [Google Scholar]
  39. 39.
    Dykstra MJ, Porter D. 1984. Diplophrys marina, a new scale-forming marine protist with labyrinthulid affinities. Mycologia 76:626–32
    [Google Scholar]
  40. 40.
    Eckford-Soper LK, Anderson KH, Frisbæk Hansen T, Canfield DE 2022. A case for an active eukaryotic marine biosphere during the Proterozoic era. PNAS 119:e2122042119
    [Google Scholar]
  41. 41.
    El Albani A, Bengtson S, Canfield DE, Bekker A, Macchiarelli R et al. 2010. Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 466:100–4
    [Google Scholar]
  42. 42.
    El Albani A, Bengtson S, Canfield DE, Riboulleau A, Bard CR et al. 2014. The 2.1 Ga Francevillian biota: biogenicity, taphonomy and biodiversity. PLOS ONE 9:6e99438
    [Google Scholar]
  43. 43.
    El Albani A, Mangano MG, Buatois LA, Bengtson S, Riboulleau A et al. 2019. Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago. PNAS 116:3431–36
    [Google Scholar]
  44. 44.
    Eme L, Sharpe SC, Brown MW, Roger AJ. 2014. On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb. Perspect. Biol. 6:a016139
    [Google Scholar]
  45. 45.
    Eme L, Spang A, Lombard J, Stairs C, Ettema TJG. 2017. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15:711–23
    [Google Scholar]
  46. 46.
    Fedonkin MA, Yochelson EL. 2002. Middle Proterozoic (1.5 Ga) Horodyskia moniliformis Yochelson and Fedonkin, the oldest known tissue-grade colonial eucaryote. Smithsonian Contr. Paleobiol. 94: https://doi.org/10.5479/si.00810266.94.1
    [Crossref] [Google Scholar]
  47. 47.
    Gast RJ, Sanders RW, Caron DA. 2009. Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends Microbiol. 17:563–69
    [Google Scholar]
  48. 48.
    Gibson TM, Shih PM, Cumming VM, Fischer WW, Crockford PW et al. 2018. Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology 46:135–38
    [Google Scholar]
  49. 49.
    Greenman JW, Rainbird RH, Turner EC. 2020. High-resolution correlation between contrasting early Tonian carbonate succession in NW Canada highlights pronounced global carbon isotope variations. Precambrian Res. 346:105816
    [Google Scholar]
  50. 50.
    Grey K, Williams IR. 1990. Problematic bedding-plane marking from the middle Proterozoic Manganese Subgroup, Bangemall Basin, Western Australia. Precambrian Res. 46:307–27
    [Google Scholar]
  51. 51.
    Grey K, Williams IR, Martin DMcB, Fedonkin MA. 2002. New occurrences of ‘strings of beads’ in the Bangemall Supergroup: a potential biostratigraphic marker horizon. Geolog. Surv. W. Aust. Annu. Rev. 2000–2001:69–73
    [Google Scholar]
  52. 52.
    Grey K, Yochelson EL, Fedonkin MA, Martin DMcB. 2010. Horodyskia williamsii new species, a Mesoproterozoic macrofossil from Western Australia. Precambrian Res. 180:1–17
    [Google Scholar]
  53. 53.
    Hammarlund EU. 2018. Valuable snapshots of deep time. Nat. Geosci. 11:298–99
    [Google Scholar]
  54. 54.
    Han T-M, Runnegar B. 1992. Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee Iron-Formation, Michigan. Science 257:232–35
    [Google Scholar]
  55. 55.
    Hodgkiss MSW, Crockford PW, Peng Y, Wing B, Horner TJ. 2019. A productivity collapse to end Earth's Great Oxidation. Proc. R. Soc. 116:17207–12
    [Google Scholar]
  56. 56.
    Hofmann HJ. 1999. Global distribution of the Proterozoic sphaeromorph acritarch Valeria lophostriata (Jankauskas). Acta Micropaleontol. Sinica 16:215–24
    [Google Scholar]
  57. 57.
    Horodyski RJ. 1982. Problematic bedding-plane markings from the middle Proterozoic Appekunny Argillite, Belt Supergroup, northwestern Montana. J. Paleontol. 56:882–89
    [Google Scholar]
  58. 58.
    Husnik F, Tashyreva D, Boscaro V, George EE, Lukeš J et al. 2021. Bacterial and archaeal symbioses with protists. Curr. Biol. 31:R862–77
    [Google Scholar]
  59. 59.
    Imachi H, Nobu MK, Nakahara N, Morono Y, Ogawara M et al. 2019. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577:519–25
    [Google Scholar]
  60. 60.
    Jankauskas TV. 1979. Нижнерифейские микробиоты Южного Урала [Lower Riphean microbiota of the Southern Urals. ]. Доклады Академии Наук СССР [Rep. Acad. Sci. USSR] 247:1465–68
    [Google Scholar]
  61. 61.
    Javaux EJ. 2007. The early eukaryotic fossil record. Eukaryotic Membranes and Cytoskeleton: Origins and Evolution, ed. G Jékely 1–15. Austin, TX: Landes Biosci.; New York: Springer
    [Google Scholar]
  62. 62.
    Javaux EJ 2011. Early eukaryotes in Precambrian oceans. Origins and Evolution of Life: An Astrobiological Perspective M Gargaud, P López-García, H Martin 414–49. Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  63. 63.
    Javaux EJ, Knoll AH. 2017. Micropaleontology of the lower Mesoproterozoic Roper Group, Australia, and implications for early eukaryotic evolution. J. Paleontol. 91:199–229
    [Google Scholar]
  64. 64.
    Javaux EJ, Knoll AH, Walter MR. 2001. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412:66–69
    [Google Scholar]
  65. 65.
    Javaux EJ, Knoll AH, Walter MR. 2003. Recognizing and interpreting the fossils of early eukaryotes. Origins Life Evol. Biosphere 33:75–94
    [Google Scholar]
  66. 66.
    Javaux EJ, Knoll AH, Walter MR. 2004. TEM evidence for eukaryotic diversity in mid-Proterozoic oceans. Geobiology 2:121–32
    [Google Scholar]
  67. 67.
    Javaux EJ, Lepot K. 2018. The Paleoproterozoic fossil record: implications for the evolution of the biosphere during Earth's middle-age. Earth Sci. Rev. 176:68–86
    [Google Scholar]
  68. 68.
    Javaux EJ, Marshall CP, Bekker A. 2010. Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463:934–38
    [Google Scholar]
  69. 69.
    Jeffries RPS. 1979. The origin of chordates—a methodological essay. The Origin of the Major Invertebrate Groups MR House 443–77. London: Academic
    [Google Scholar]
  70. 70.
    Keeling PJ. 2010. The endosymbiotic origin, diversification and fate of plastids. Philos. Trans. R. Soc. B 365:729–48
    [Google Scholar]
  71. 71.
    Knoll AH. 2003. Biomineralization and evolutionary history. Rev. Mineral. Geochem. 54:329–56
    [Google Scholar]
  72. 72.
    Knoll AH. 2011. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 39:217–39
    [Google Scholar]
  73. 73.
    Knoll AH. 2014. Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6:a016121
    [Google Scholar]
  74. 74.
    Knoll AH, Barghoorn ES. 1975. Precambrian eukaryotic organisms: a reassessment of the evidence. Science 190:52–54
    [Google Scholar]
  75. 75.
    Knoll AH, Javaux EJ, Hewitt D, Cohen PA. 2006. Eukaryotic organisms in Proterozoic oceans. Philos. Trans. R. Soc. B 361:1023–38
    [Google Scholar]
  76. 76.
    Knoll AH, Lahr DJG 2016. Fossils, feeding and the evolution of complex multicellularity. Multicellularity, Origins and Evolution KJ Niklas, SA Newman 1–16. Cambridge, MA: MIT Press
    [Google Scholar]
  77. 77.
    Koumandou VL, Wickstead B, Ginger ML, Van der Giezen M, Dacks JB et al. 2013. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit. Rev. Biochem. Mol. Biol. 48:373–96
    [Google Scholar]
  78. 78.
    Lamb DM, Awramik SM, Chapman DJ, Zhu S. 2009. Evidence for eukaryotic diversification in the ∼1800 million-year-old Changzhougou Formation, North China. Precambrian Res. 173:93–104
    [Google Scholar]
  79. 79.
    Lamża L. 2021. Superorganisms of the protist kingdom: a new level of biological organization. Found. Sci. 26:281–300
    [Google Scholar]
  80. 80.
    Lane N, Martin W. 2010. The energetics of genome complexity. Nature 467:929–34
    [Google Scholar]
  81. 80a.
    Loron CC, François C, Rainbird RH, Turner EC, Borensztajn , Javaux EJ 2019. Early fungi from the Proterozoic era in Arctic Canada. Nature 570:232–35
    [Google Scholar]
  82. 81.
    Loron CC, Halverson GP, Rainbird RH, Skulski T, Turner EC et al. 2021. Shale-hosted biota from the Dismal Lakes Group in the Arctic Canada supports an early Mesoproterozoic diversification of eukaryotes. J. Paleontol. 95:1113–37
    [Google Scholar]
  83. 82.
    Loron CC, Rainbird RH, Turner EC, Greenman JW, Javaux EJ. 2018. Implications of selective predation on the macroevolution of eukaryotes: evidence from Arctic Canada. Emerg. Top. Life Sci. 2:247–55
    [Google Scholar]
  84. 83.
    Loron CC, Rainbird RH, Turner EC, Greenman JW, Javaux EJ. 2019. Organic-walled microfossils from the late Mesoproterozoic to early Neoproterozoic lower Shaler Supergroup (Arctic Canada): diversity and biostratigraphic significance. Precambrian Res. 321:349–74
    [Google Scholar]
  85. 84.
    Lyons TW, Diamond CW, Planavsky NJ, Reinhard CT, Li C. 2021. Oxygenation, life, and the planetary system during Earth's middle history: an overview. Astrobiology 21:906–23
    [Google Scholar]
  86. 85.
    Lyons TW, Reinhard CT, Planavsky NJ. 2014. The rise of oxygen in Earth's early ocean and atmosphere. Nature 506:307–15
    [Google Scholar]
  87. 86.
    Maloney KM, Halverson GP, Schiffbauer JD, Xiao S, Gibson TM et al. 2021. New multicellular marine macroalgae form the early Tonian of northwestern Canada. Geology 49:743–47
    [Google Scholar]
  88. 87.
    Marshall CR. 2017. Five palaeobiological laws needed to understand the evolution of the living biota. Nat. Ecol. Evol. 1:6165
    [Google Scholar]
  89. 88.
    Matz MV, Frank TM, Marshall NJ, Widder EA, Johnsen S. 2008. Giant deep-sea protist produces bilaterian-like traces. Curr. Biol. 18:1849–54
    [Google Scholar]
  90. 89.
    Melkonian M, Becker B, Becker D. 1991. Scale formation in algae. J. Electron Microsc. Tech. 17:165–78
    [Google Scholar]
  91. 90.
    Miao L, Moczydłowska M, Zhu S, Zhu M. 2019. New record of organic-walled, morphologically distinct microfossils from the late Paleoproterozoic Changcheng Group in the Yanshan Range, North China. Precambrian Res. 321:172–98
    [Google Scholar]
  92. 91.
    Mills DB. 2020. The origin of phagocytosis in Earth history. Interface Focus 10:20200019
    [Google Scholar]
  93. 92.
    Mills DB, Boyle RA, Daines SJ, Sperling EA, Pisani D et al. 2022. Eukaryogenesis and oxygen in Earth history. Nat. Ecol. Evol. 6:520–32
    [Google Scholar]
  94. 93.
    Morais L, Fairchild TR, Lahr DJG, Rudnitzki ID, Schopf JW et al. 2017. Carbonaceous and siliceous Neoproterozoic vase-shaped microfossils (Urucum Formation, Brazil) and the question of early protistan biomineralization. J. Paleontol. 91:393–406
    [Google Scholar]
  95. 94.
    Nguyen K, Love GD, Zumberge JA, Kelly AE, Owens JD et al. 2019. Absence of biomarker evidence for early eukaryotic life from the Mesoproterozoic Roper Group: searching across a marine redox gradient in mid-Proterozoic habitability. Geobiology 17:247–60
    [Google Scholar]
  96. 95.
    Pang K, Tang Q, Schiffbauer JD, Yao J, Yuan X et al. 2013. The nature and origin of nucleus-like intracellular inclusions in Paleoproterozoic eukaryote microfossils. Geobiology 11:499–510
    [Google Scholar]
  97. 96.
    Pang K, Tang Q, Yuan X-L, Wan B, Xiao S 2015. A biomechanical analysis of the early eukaryotic fossil Valeria and new occurrence of organic-walled microfossils from the Paleo-Mesoproterozoic Ruyang Group. Palaeoworld 24:251–62
    [Google Scholar]
  98. 97.
    Parfrey LW, Lahr DJG, Knoll AH, Katz LA. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. PNAS 108:13624–29
    [Google Scholar]
  99. 98.
    Patterson DJ, Dürrschmidt M. 1988. The formation of siliceous scales by Raphidiophrys ambigua (Protisa, Centroheliozoa). J. Cell Sci. 91:33–39
    [Google Scholar]
  100. 99.
    Payne JL, Boyer AG, Brown JH, Finnegan S, Kowalewski M et al. 2009. Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. PNAS 106:24–27
    [Google Scholar]
  101. 100.
    Perasso L, Ludwig M, Wetherbee R. 1997. The surface periplast component of the protist Komma caudate (Cryptophyceae) self-assembles from a secreted high-molecular-mass polypeptide. Protoplasma 200:186–97
    [Google Scholar]
  102. 101.
    Pickett-Heaps JD. 1998. Cell division and morphogenesis of the centric diatom Chaetoceros decipiens (Bacillariophyceae) II. Electron microscopy and a new paradigm for tip growth. J. Phycol. 34:995–1004
    [Google Scholar]
  103. 102.
    Porter SM. 2011. The rise of predators. Geology 39:607–8
    [Google Scholar]
  104. 103.
    Porter SM. 2016. Tiny vampires in ancient seas: evidence for predation via perforation in fossils from the 780–40 million-year-old Chuar Group, Grand Canyon, USA. Proc. R. Soc. Lond. Ser. B 283:20160221
    [Google Scholar]
  105. 104.
    Porter SM. 2020. Insights into eukaryogenesis from the fossil record. Interface Focus 10:20190105
    [Google Scholar]
  106. 105.
    Porter SM, Knoll AH. 2000. Testate amoebae in the Neoproterozoic Era: evidence from vase-shaped microfossils in the Chuar Group, Grand Canyon. Paleobiology 26:360–85
    [Google Scholar]
  107. 106.
    Porter SM, Meisterfeld R, Knoll AH. 2003. Vase-shaped microfossils from the Neoproterozoic Chuar Group, Grand Canyon: a classification guided by modern testate amoebae. J. Paleontol. 77:409–29
    [Google Scholar]
  108. 107.
    Porter SM, Riedman LA. 2016. Systematics of organic-walled microfossils from the ca. 780–740 Ma Chuar Group, Grand Canyon, Arizona. J. Paleontol. 90:815–53
    [Google Scholar]
  109. 108.
    Porter SM, Riedman LA. 2019. Evolution: Ancient fossilized amoebae find their home in the tree. Curr. Biol. 29:R200–23
    [Google Scholar]
  110. 109.
    Prasad B, Asher R. 2001. Acritarch biostratigraphy and lithostratigraphic classification of Proterozoic and lower Paleozoic sediments (Pre-Unconformity Sequence) of Ganga Basin, India. Palaeontographica Indica. No. 5 Dehra Dun, India: Geosci. Res. Group
    [Google Scholar]
  111. 110.
    Preisig HR. 1994. Siliceous structures and silicification in flagellated protists. Protoplasma 181:29–42
    [Google Scholar]
  112. 111.
    Radek R 2010. Adhesion of bacteria to protists. Prokaryotic Cell Wall Compounds: Structure and Biochemistry H König, H Claus, A Varma 429–56. Berlin: Springer
    [Google Scholar]
  113. 112.
    Riedman LA, Porter SM. 2016. Organic-walled microfossils of the mid-Neoproterozoic Alinya Formation, Officer Basin, Australia. J. Paleontol. 90:854–87
    [Google Scholar]
  114. 113.
    Riedman LA, Porter SM, Calver CR 2018. Vase-shaped microfossil biostratigraphy with new data from Tasmania, Svalbard, Greenland, Sweden and the Yukon. Precambrian Res. 319:19–36
    [Google Scholar]
  115. 114.
    Roger AJ, Muñoz-Gómez SA, Kamikawa R. 2017. The origin and diversification of mitochondria. Curr. Biol. 27:R1177–92
    [Google Scholar]
  116. 115.
    Samuelsson J, Butterfield NJ. 2001. Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications. Precambrian Res. 107:235–51
    [Google Scholar]
  117. 116.
    Sansom RS, Wills MA. 2013. Fossilization causes organisms to appear erroneously primitive by distorting evolutionary trees. Sci. Rep. 3:2545
    [Google Scholar]
  118. 117.
    Schavemaker PE, Muñoz-Gómez SA. 2022. The role of mitochondrial energetics in the origin and diversification of eukaryotes. Nat. Ecol. Evol. 6:1307–17
    [Google Scholar]
  119. 118.
    Schneider DA, Bickford ME, Cannon WF, Schulz KJ, Hamilton MA. 2002. Age of volcanic rocks and syndepositional iron formations, Marquette Range Supergroup: implications for the tectonic setting of Paleoproterozoic iron formations of the Lake Superior region. Can. J. Earth Sci. 39:999–1012
    [Google Scholar]
  120. 119.
    Schulz HW, Jørgensen BB. 2001. Big bacteria. Annu. Rev. Microbiol. 55:105–37
    [Google Scholar]
  121. 120.
    Sforna MC, Loron CC, Demoulin CF, François C, Cornet Y et al. 2022. Intracellular bound chlorophyll residues identify 1 Gyr-old fossil as eukaryotic algae. Nat. Commun. 13:146
    [Google Scholar]
  122. 121.
    Sharma M, Shukla Y. 2009. Taxonomy and affinity of early Mesoproterozoic megascopic helically coiled and related fossils from the Rohtas Formation, the Vindhyan Supergroup, India. Precambrian Res. 173:105–22
    [Google Scholar]
  123. 122.
    Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Matijn J et al. 2015. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–79
    [Google Scholar]
  124. 123.
    Stairs CW, Ettema TJG. 2020. The Archaeal roots of the eukaryotic dynamic actin cytoskeleton. Curr. Biol. 30:R521–26
    [Google Scholar]
  125. 124.
    Strassert JFH, Irisarri I, Williams TA, Burki F. 2021. A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids. Nat. Commun. 12:1879
    [Google Scholar]
  126. 125.
    Strother PK, Brasier MD, Wacey D, Timpe L, Saunders M et al. 2021. A possible billion-year-old holozoan with differentiated multicellularity. Curr. Biol. 31:122658–65.e2
    [Google Scholar]
  127. 126.
    Tang Q, Pang K, Li G, Chen L, Yuan X et al. 2021. One-billion year-old epibionts highlight symbiotic ecological interactions in early eukaryote evolution. Gondwana Res. 97:22–33
    [Google Scholar]
  128. 127.
    Tang Q, Pang K, Yuan X, Xiao S. 2020. A one-billion-year-old multicellular chlorophyte. Nat. Ecol. Evol. 4:543–49
    [Google Scholar]
  129. 128.
    Turner EC. 2021. Possible poriferan body fossils in early Neoproterozoic microbial reefs. Nature 596:87–91
    [Google Scholar]
  130. 129.
    Volland J-M, Gonzalez-Rizzo S, Gros O, Tyml T, Ivanova N et al. 2022. A centimeter-long bacterium with DNS contained in metabolically active, membrane-bound organelles. Science 376:1453–58
    [Google Scholar]
  131. 130.
    Xiao S 2022. Extinctions, morphological gaps, major transitions, stem groups, and the origin of major clades, with a focus on early animals. Acta Geol. Sin. 96:1821–29
    [Google Scholar]
  132. 131.
    Xiao S, Knoll AH, Kaufman AJ, Yin L, Zhang Y. 1997. Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China Platform. Precambrian Res. 84:197–220
    [Google Scholar]
  133. 132.
    Yin L, Yuan X, Meng F, Hu J. 2005. Protists of the Upper Mesoproterozoic Ruyang Group in Shanxi Province, China. Precambrian Res. 141:49–66
    [Google Scholar]
  134. 133.
    Yoshida M, Noël M-H, Nakayama T, Naganuma T, Inouye I. 2006. A haptophyte bearing siliceous scales: ultrastructure and phylogenetic position of Hyalithus neolepis gen. et sp. nov. (Prymnesiophyceae, Haptophyta). Protist 157:213–34
    [Google Scholar]
  135. 134.
    Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckstrom D, Juzokaite L et al. 2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–58
    [Google Scholar]
  136. 135.
    Zhu S, Zhu M, Knoll AH, Yin Z, Zhao F et al. 2016. Decimeter-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang Formation in North China. Nat. Commun. 7:11500
    [Google Scholar]
/content/journals/10.1146/annurev-micro-032421-113254
Loading
/content/journals/10.1146/annurev-micro-032421-113254
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error