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Lipid biomarkers: molecular tools for illuminating the history of microbial life

Nature Reviews Microbiology volume 20, pages 174–185 (2022)Cite this article

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Abstract

Fossilized lipids preserved in sedimentary rocks offer singular insights into the Earth’s palaeobiology. These ‘biomarkers’ encode information pertaining to the oxygenation of the atmosphere and oceans, transitions in ocean plankton, the greening of continents, mass extinctions and climate change. Historically, biomarker interpretations relied on inventories of lipids present in extant microorganisms and counterparts in natural environments. However, progress has been impeded because only a small fraction of the Earth’s microorganisms can be cultured, many environmentally significant microorganisms from the past no longer exist and there are gaping holes in knowledge concerning lipid biosynthesis. The revolution in genomics and bioinformatics has provided new tools to expand our understanding of lipid biomarkers, their biosynthetic pathways and distributions in nature. In this Review, we explore how preserved organic molecules provide a unique perspective on the history of the Earth’s microbial life. We discuss how advances in molecular biology have helped elucidate biomarker origins and afforded more robust interpretations of fossil lipids and how the rock record provides vital calibration points for molecular clocks. Such studies are open to further exploitation with the expansion of sequenced microbial genomes in accessible databases.

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Fig. 1: Geological timescale of the Earth’s fossil record in the context of planetary oxygenation.
Fig. 2: Commonly referenced lipid biomarkers and their known sources.
Fig. 3: Phylogeny of the proteins essential for biosynthesis of aromatic carotenoids.
Fig. 4: Structural differences between archaeal and bacterial membrane phospholipids.
Fig. 5: Identification of GDGT ring synthase proteins in Sulfolobus acidocaldarius.

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References

  1. Berner, E. K. & Berner, R. A. Global Environment: Water, Air, and Geochemical Cycles (Princeton Univ. Press, 2012).

  2. Cavosie, A. J., Valley, J. W. & Wilde, S. A. The oldest terrestrial mineral record: a review of 4400 to 4000 Ma detrital zircons from Jack Hills, Western Australia. Dev. Precambrian Geol. 15, 91–111 (2007).

    Article  Google Scholar 

  3. Betts, H. C. et al. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nat. Ecol. Evol. 2, 1556–1562 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  4. McNaughton, N. J., Compston, W. & Barley, M. E. Constraints on the age of the Warrawoona Group, eastern Pilbara Block, Western Australia. Precambrian Res. 60, 69–98 (1993).

    Article  CAS  Google Scholar 

  5. Sugitani, K., Mimura, K., Nagaoka, T., Lepot, K. & Takeuchi, M. Microfossil assemblage from the 3400 Ma strelley pool formation in the Pilbara Craton, Western Australia: results form a new locality. Precambrian Res. 226, 59–74 (2013).

    Article  CAS  Google Scholar 

  6. Sugitani, K. et al. Early evolution of large micro-organisms with cytological complexity revealed by microanalyses of 3.4 Ga organic-walled microfossils. Geobiology 13, 507–521 (2015).

    Article  CAS  PubMed  Google Scholar 

  7. Alleon, J. et al. Chemical nature of the 3.4 Ga Strelley Pool microfossils. Geochem. Perspect. Lett. 7, 37–42 (2018).

    Article  Google Scholar 

  8. Allwood, A. C. et al. Controls on development and diversity of Early Archean stromatolites. Proc. Natl Acad. Sci. USA 106, 9548–9555 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Allwood, A. C., Walter, M. R., Kamber, B. S., Marshall, C. P. & Burch, I. W. Stromatolite reef from the Early Archaean era of Australia. Nature 441, 714–718 (2006). This paper details connections between the morphology of some of the oldest stromatolites and features of their coastal marine setting. It is key to illustrating how complex microbial communities must have existed on the Earth at least 3.45 billion years ago.

    Article  CAS  PubMed  Google Scholar 

  10. Hofmann, H., Grey, K., Hickman, A. & Thorpe, R. Origin of 3.45 Ga coniform stromatolites in Warrawoona Group, Western Australia. Geol. Soc. Am. Bull. 111, 1256–1262 (1999).

    Article  Google Scholar 

  11. Des Marais, D. J. Isotopic evolution of the biogeochemical carbon cycle during the Precambrian. Rev. Mineral. Geochem. 43, 555–578 (2001).

    Article  CAS  Google Scholar 

  12. Buick, R. et al. Record of emergent continental crust ∼3.5 billion years ago in the Pilbara Craton of Australia. Nature 375, 574–577 (1995).

    Article  CAS  Google Scholar 

  13. Ueno, Y., Ono, S., Rumble, D. & Maruyama, S. Quadruple sulfur isotope analysis of ca. 3.5 Ga dresser formation: new evidence for microbial sulfate reduction in the early Archean. Geochim. Cosmochim. Acta 72, 5675–5691 (2008).

    Article  CAS  Google Scholar 

  14. Bontognali, T. R. R. et al. Sulfur isotopes of organic matter preserved in 3.45-billion-year-old stromatolites reveal microbial metabolism. Proc. Natl Acad. Sci. USA 109, 15146–15151 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Beaumont, V. & Robert, F. Nitrogen isotope ratios of kerogens in Precambrian cherts: a record of the evolution of atmosphere chemistry? Precambrian Res. 96, 63–82 (1999).

    Article  CAS  Google Scholar 

  16. Morgan, G. J. Emile Zuckerkandl, Linus Pauling, and the molecular evolutionary clock, 1959–1965. J. Hist. Biol. 31, 155–178 (1998).

    Article  CAS  PubMed  Google Scholar 

  17. Zuckerkandl, E. & Pauling, L. Molecules as documents of evolutionary history. J. Theor. Biol. 8, 357–366 (1965). This classic paper informs us how the sequences of present-day macromolecules encode a history of their origin and evolution.

    Article  CAS  PubMed  Google Scholar 

  18. Zuckerkandl, E. & Pauling, L. in Evolving Genes and Proteins 97–166 (Elsevier, 1965).

  19. Peterson, K. J., Summons, R. E. & Donoghue, P. C. J. Molecular palaeobiology. Palaeontology 50, 775–809 (2007).

    Article  Google Scholar 

  20. Gaucher, E. A. Ancestral sequence reconstruction as a tool to understand natural history and guide synthetic biology: realizing and extending the vision of Zuckerkandl and Pauling. Liberles [83] 31, 20–33 (2007).

    Google Scholar 

  21. Kacar, B., Hanson-Smith, V., Adam, Z. R. & Boekelheide, N. Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree. Geobiology 15, 628–640 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Brocks, J. J. et al. Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea. Nature 437, 866–870 (2005).

    Article  CAS  PubMed  Google Scholar 

  23. McKenna, E. J. & Kallio, R. E. Microbial metabolism of the isoprenoid alkane pristane. Proc. Natl Acad. Sci. USA 68, 1552 (1971).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Waples, D. W., Haug, P. & Welte, D. H. Occurrence of a regular C25 isoprenoid hydrocarbon in Tertiary sediments representing a lagoonal-type, saline environment. Geochim. Cosmochim. Acta 38, 381–387 (1974).

    Article  CAS  Google Scholar 

  25. Knoll, A. H., Summons, R. E., Waldbauer, J. R. & Zumberge, J. in The Evolution of Primary Producers in the Sea (eds Falkwoski, P. & Knoll, A.H.) 133–163 (Elsevier, 2007).

  26. Brocks, J. J. The transition from a cyanobacterial to algal world and the emergence of animals. Emerg. Top. Life Sci. 2, 181–190 (2018).

    Article  CAS  PubMed  Google Scholar 

  27. Sinninghe Damsté, J. S. & Köster, J. A euxinic southern North Atlantic Ocean during the Cenomanian/Turonian oceanic anoxic event. Earth Planet. Sci. Lett. 158, 165–173 (1998).

    Article  Google Scholar 

  28. Kuypers, M. M. M. et al. Massive expansion of marine archaea during a mid-cretaceous oceanic anoxic event. Science 293, 92–95 (2001).

    Article  CAS  PubMed  Google Scholar 

  29. Brassell, S. C., Eglinton, G., Marlowe, I. T., Pflaumann, U. & Sarnthein, M. Molecular stratigraphy: a new tool for climatic assessment. Nature 320, 129–133 (1986). This study is the first detailing how fossilized organic molecules can serve as SST proxies.

    Article  CAS  Google Scholar 

  30. Schouten, S. et al. Extremely high sea-surface temperatures at low latitudes during the Middle Cretaceous as revealed by archaeal membrane lipids. Geology 31, 1069–1072 (2003).

    Article  CAS  Google Scholar 

  31. Bobrovskiy, I., Hope, J. M., Krasnova, A., Ivantsov, A. & Brocks, J. J. Molecular fossils from organically preserved Ediacara biota reveal cyanobacterial origin for Beltanelliformis. Nat. Ecol. Evol. 2, 437 (2018).

    Article  PubMed  Google Scholar 

  32. Evitt, W. R. A discussion and proposals concerning fossil dinoflagellates, hystrichospheres, and acritarchs, II. Proc. Natl Acad. Sci. USA 49, 298 (1963).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Treibs, A. Chlorophyll- und Häminderivate in organischen Mineralstoffen [German]. Angew. Chem. 49, 682–686 (1936).

    Article  CAS  Google Scholar 

  34. Hills, I. R. & Whitehead, E. V. Triterpanes in optically active petroleum distillates. Nature 209, 977–979 (1966).

    Article  CAS  Google Scholar 

  35. Blumer, M. Pigments of a fossil echinoderm. Nature 188, 1100–1101 (1960).

    Article  CAS  Google Scholar 

  36. Ourisson, G., Albrecht, P. & Rohmer, M. The hopanoids. Palaeochemistry and biochemistry of a group of natural products. Pure Appl. Chem. 51, 709–729 (1979). This review details how a particular group of bacterial membrane lipids gave rise to a ubiquitous and abundant class of chemical fossils.

    Article  CAS  Google Scholar 

  37. Rohmer, M. & Ourisson, G. Dérivés du bactériohopane: variations structurales et répartition [French]. Tetrahedron Lett. 17, 3637–3640 (1976).

    Article  Google Scholar 

  38. Yon, D. A., Maxwell, J. R. & Ryback, G. 2,6,10-Trimethyl-7-(3-methylbutyl)-dodecane, a novel sedimentary biological marker compound. Tetrahedron Lett. 23, 2143–2146 (1982).

    Article  CAS  Google Scholar 

  39. Barrick, R. C., Hedges, J. I. & Peterson, M. L. Hydrocarbon geochemistry of the Puget Sound region — I. Sedimentary acyclic hydrocarbons. Geochim. Cosmochim. Acta 44, 1349–1362 (1980).

    Article  CAS  Google Scholar 

  40. Requejo, A. G. & Quinn, J. G. Geochemistry of C25 and C30 biogenic alkenes in sediments of the Narragansett Bay estuary. Geochim. Cosmochim. Acta 47, 1075–1090 (1983).

    Article  CAS  Google Scholar 

  41. Dunlop, R. W. & Jefferies, P. R. Hydrocarbons of the hypersaline basins of Shark Bay, Western Australia. Org. Geochem. 8, 313–320 (1985).

    Article  CAS  Google Scholar 

  42. Volkman, J. K., Barrett, S. M. & Dunstan, G. A. C25 and C30 highly branched isoprenoid alkenes in laboratory cultures of two marine diatoms.Org. Geochem. 21, 407–414 (1994).

    Article  CAS  Google Scholar 

  43. Sinninghe Damste, J. S. et al. The rise of the rhizosolenid diatoms. Science 304, 584–587 (2004).

    Article  CAS  Google Scholar 

  44. Rowland, S. J. et al. Factors influencing the distributions of polyunsaturated terpenoids in the diatom, Rhizosolenia setigera. Phytochemistry 58, 717–728 (2001).

    Article  CAS  PubMed  Google Scholar 

  45. Blumer, M., Guillard, R. R. L. & Chase, T. Hydrocarbons of marine phytoplankton. Mar. Biol. 8, 183–189 (1971).

    Article  CAS  Google Scholar 

  46. Eglinton, G. & Hamilton, R. J. Leaf epicuticular waxes. Science 156, 1322–1335 (1967).

    Article  CAS  PubMed  Google Scholar 

  47. Rohmer, M., Bouvier-Nave, P. & Ourisson, G. Distribution of hopanoid triterpanes in prokaryotes. J. Gen. Microbiol. 130, 1137–1150 (1984).

    CAS  Google Scholar 

  48. Volkman, J. K. et al. Microalgal biomarkers: a review of recent research developments. Org. Geochem. 29, 1163–1179 (1998). This paper reviews the laborious but essential work of surveying biomarkers across living organisms. The distribution of biomarkers in modern algae provides a solid foundation on which molecular fossils have historically been interpreted.

    Article  CAS  Google Scholar 

  49. Sturt, H. F., Summons, R. E., Smith, K., Elvert, M. & Hinrichs, K.-U. Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry — new biomarkers for biogeochemistry and microbial ecology. Rapid Commun. Mass. Spectrom. 18, 617–628 (2004).

    Article  CAS  PubMed  Google Scholar 

  50. White, D. C. & Ringelberg, D. B. in Techniques in Microbial Ecology. (eds Burlage, R. S. et al.) 255–272 (Oxford Univ. Press, 1998).

  51. Vestal, J. R. & White, D. C. Lipid analysis in microbial ecology. Bioscience 39, 535–541 (1989).

    Article  CAS  PubMed  Google Scholar 

  52. Lipp, J. S. & Hinrichs, K.-U. Structural diversity and fate of intact polar lipids in marine sediments. Geochim. Cosmochim. Acta 73, 6816–6833 (2009).

    Article  CAS  Google Scholar 

  53. Rossel, P. E. et al. Intact polar lipids of anaerobic methanotrophic archaea and associated bacteria. Org. Geochem. 39, 992–999 (2008).

    Article  CAS  Google Scholar 

  54. Taylor, J. & Parkes, R. J. The cellular fatty acids of the sulphate-reducing bacteria, Desulfobacter sp., Desulfobulbus sp. and Desulfovibrio desulfuricans. J. Gen. Microbiol. 129, 3303–3309 (1983).

    CAS  Google Scholar 

  55. Brocks, J. J. & Pearson, A. Building the biomarker tree of life. Rev. Mineral. Geochem. 59, 233–258 (2005).

    Article  CAS  Google Scholar 

  56. Volkman, J. K. Sterols and other triterpenoids: source specificity and evolution of biosynthetic pathways. Org. Geochem. 36, 139–159 (2005).

    Article  CAS  Google Scholar 

  57. Schouten, S., Hopmans, E. C. & Sinninghe Damsté, J. S. The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: a review. Org. Geochem. 54, 19–61 (2013).

    Article  CAS  Google Scholar 

  58. Peters, K. E., Walters, C. C. & Moldowan, J. M. The Biomarker Guide 2nd edn (Cambridge Univ. Press, 2005).

  59. Pearson, A. 12.11 Lipidomics for geochemistry. Treatise Geochem. 12, 291–336 (2014).

    Article  Google Scholar 

  60. Newman, D. K., Neubauer, C., Ricci, J. N., Wu, C.-H. & Pearson, A. Cellular and molecular biological approaches to interpreting ancient biomarkers. Annu. Rev. Earth Planet. Sci. 44, 493–522 (2016). This paper details our changing understanding on the role of 2-methylhopanoids in bacteria, and how this change impacts our interpretation of the related molecular fossil. It provides a case study on the importance of knowing what a biomarker biologically does in a microbe, not just its presence or absence.

    Article  CAS  Google Scholar 

  61. Ochs, D., Kaletta, C., Entian, K. D., Beck-Sickinger, A. & Poralla, K. Cloning, expression, and sequencing of squalene-hopene cyclase, a key enzyme in triterpenoid metabolism. J. Bacteriol. 174, 298–302 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Schmerk, C. L. et al. Elucidation of the Burkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid-producing bacteria. Environ. Microbiol. 17, 735–750 (2015).

    Article  CAS  PubMed  Google Scholar 

  63. Welander, P. V. et al. Identification and characterization of Rhodopseudomonas palustris TIE-1 hopanoid biosynthesis mutants. Geobiology 10, 163–177 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Pearson, A., Flood Page, S. R., Jorgenson, T. L., Fischer, W. W. & Higgins, M. B. Novel hopanoid cyclases from the environment. Environ. Microbiol. 9, 2175–2188 (2007). This paper is the first example of using a biomarker biosynthesis gene, the squalene–hopene cyclase gene necessary for hopanoid production, to demonstrate the potential diversity of biomarker producers in environmental metagenomic data sets.

    Article  CAS  PubMed  Google Scholar 

  65. Villanueva, L., Rijpstra, W. I. C., Schouten, S. & Damsté, J. S. S. Genetic biomarkers of the sterol–biosynthetic pathway in microalgae. Environ. Microbiol. Rep. 6, 35–44 (2014).

    Article  CAS  PubMed  Google Scholar 

  66. Villanueva, L., Schouten, S. & Sinninghe Damsté, J. S. Depth-related distribution of a key gene of the tetraether lipid biosynthetic pathway in marine Thaumarchaeota. Environ. Microbiol. 17, 3527–3539 (2015).

    Article  CAS  PubMed  Google Scholar 

  67. Banta, A. B., Wei, J. H. & Welander, P. V. A distinct pathway for tetrahymanol synthesis in bacteria. Proc. Natl Acad. Sci. USA 112, 13478–13483 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Benson, D. A. et al. GenBank. Nucleic Acids Res. 41, D36–D42 (2013).

    Article  CAS  PubMed  Google Scholar 

  69. Eglinton, G. & Calvin, M. Chemical fossils. Sci. Am. 216, 32–43 (1967).

    Article  CAS  Google Scholar 

  70. Jensen, S. V. L. Bacterial carotenoids. Acta Chem. Scand. 19, 1025–30 (1965).

    Article  CAS  PubMed  Google Scholar 

  71. Jensen, S. V. L. Bacterial carotenoids XXII. Acta Chem. Scand. 21, 2578–80 (1967).

    PubMed  Google Scholar 

  72. Summons, R. E. & Powell, T. G. Chlorobiaceae in Paleozoic seas revealed by biological markers, isotopes and geology. Nature 319, 763–765 (1986).

    Article  CAS  Google Scholar 

  73. Abella, C., Montesinos, E. & Guerrero, R. in Shallow Lakes Contributions to Their Limnology 173–181 (Springer, 1980).

  74. French, K. L., Rocher, D., Zumberge, J. E. & Summons, R. E. Assessing the distribution of sedimentary C40 carotenoids through time. Geobiology 13, 139–151 (2015).

    Article  CAS  PubMed  Google Scholar 

  75. Sinninghe Damsté, J. S. & Koopmans, M. P. The fate of carotenoids in sediments: an overview. Pure Appl. Chem. 69, 2067–2074 (1997).

    Article  Google Scholar 

  76. Frigaard, N.-U., Maresca, J. A., Yunker, C. E., Jones, A. D. & Bryant, D. A. Genetic manipulation of carotenoid biosynthesis in the green sulfur bacterium Chlorobium tepidum. J. Bacteriol. 186, 5210–5220 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Maresca, J., Graham, J. & Bryant, D. The biochemical basis for structural diversity in the carotenoids of chlorophototrophic bacteria. Photosynthesis Res. 97, 121–140 (2008).

    Article  CAS  Google Scholar 

  78. Maresca, J. A., Romberger, S. P. & Bryant, D. A. Isorenieratene biosynthesis in green sulfur bacteria requires the cooperative actions of two carotenoid cyclases. J. Bacteriol. 190, 6384–6391 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Vogl, K. & Bryant, D. A. Biosynthesis of the biomarker okenone: χ-ring formation. Geobiology 10, 205–215 (2012).

    Article  CAS  PubMed  Google Scholar 

  80. Krügel, H., Krubasik, P., Weber, K., Saluz, H. P. & Sandmann, G. Functional analysis of genes from Streptomyces griseus involved in the synthesis of isorenieratene, a carotenoid with aromatic end groups, revealed a novel type of carotenoid desaturase. Biochim. Biophys. Acta 1439, 57–64 (1999).

    Article  PubMed  Google Scholar 

  81. Krubasik, P. & Sandmann, G. A carotenogenic gene cluster from Brevibacterium linens with novel lycopene cyclase genes involved in the synthesis of aromatic carotenoids. Mol. Gen. Genet. 263, 423–432 (2000).

    Article  CAS  PubMed  Google Scholar 

  82. Graham, J. E., Lecomte, J. T. J. & Bryant, D. A. Synechoxanthin, an aromatic C40 xanthophyll that is a major carotenoid in the cyanobacterium Synechococcus sp. PCC 7002. J. Nat. Products 71, 1647–1650 (2008).

    Article  CAS  Google Scholar 

  83. Graham, J. E. & Bryant, D. A. The biosynthetic pathway for synechoxanthin, an aromatic carotenoid synthesized by the euryhaline, unicellular cyanobacterium Synechococcus sp. strain PCC 7002. J. Bacteriol. 190, 7966–7974 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Koopmans, M. P., Schouten, S., Kohnen, M. E. L. & Damsté, J. S. S. Restricted utility of aryl isoprenoids as indicators for photic zone anoxia. Geochim. Cosmochim. Acta 60, 4873–4876 (1996).

    Article  CAS  Google Scholar 

  85. Brocks, J. J. & Schaeffer, P. Okenane, a biomarker for purple sulfur bacteria (Chromatiaceae), and other new carotenoid derivatives from the 1640 Ma Barney Creek formation. Geochim. Cosmochim. Acta 72, 1396–1414 (2008).

    Article  CAS  Google Scholar 

  86. Yamaguchi, M. On carotenoids of a sponge “Reniera japonica”. Bull. Chem. Soc. Jpn. 30, 111–114 (1957).

    Article  CAS  Google Scholar 

  87. Yamaguchi, M. Renieratene, a new carotenoid containing benzene rings, isolated from a sea sponge. Bull. Chem. Soc. Jpn. 31, 739–742 (1958).

    Article  CAS  Google Scholar 

  88. Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 10, 641–654 (2012).

    Article  CAS  PubMed  Google Scholar 

  89. French, K. L., Birdwell, J. E. & Berg, V. Biomarker similarities between the saline lacustrine eocene green river and the paleoproterozoic Barney Creek formations. Geochim. Cosmochim. Acta 274, 228–245 (2020).

    Article  CAS  Google Scholar 

  90. Cui, X. et al. Niche expansion for phototrophic sulfur bacteria at the Proterozoic–Phanerozoic transition. Proc. Natl Acad. Sci. USA 117, 17599–17606 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Koopmans, M. P., De Leeuw, J. W. & Sinninghe Damsté, J. S. Novel cyclised and aromatised diagenetic products of β-carotene in the Green River Shale. Org. Geochem. 26, 451–466 (1997).

    Article  CAS  Google Scholar 

  92. Behrens, A., Schaeffer, P., Bernasconi, S. & Albrecht, P. Mono- and bicyclic squalene derivatives as potential proxies for anaerobic photosynthesis in lacustrine sulfur-rich sediments. Geochim. Cosmochim. Acta 64, 3327–3336 (2000).

    Article  CAS  Google Scholar 

  93. Schaeffer, P., Adam, P., Wehrung, P. & Albrecht, P. Novel aromatic carotenoid derivatives from sulfur photosynthetic bacteria in sediments. Tetrahedron Lett. 38, 8413–8416 (1997).

    Article  CAS  Google Scholar 

  94. Brocks, J. J. et al. The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578 (2017). This study highlights how specific chemical modifications in lipid structures, in this case methylation of sterol molecules, can be informative and can be used to track the emergence of specific microbial groups in the geologic record.

    Article  CAS  PubMed  Google Scholar 

  95. 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 

  96. Knoll, A. H. The early evolution of eukaryotes: a geological perspective. Science 256, 622–627 (1992).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  98. Hoshino, Y. & Gaucher, E. A. Evolution of bacterial steroid biosynthesis and its impact on eukaryogenesis. Proc. Natl Acad. Sci. USA 118, e2101276118 (2021). This recent study uses a phylogenetic approach to assess the evolutionary history of sterol biosynthesis and the potential impact of bacterial sterol biosynthesis on the rise of eukaryotes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  100. Luo, G. et al. Rapid oxidation of Earth’s atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. 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  CAS  PubMed  Google Scholar 

  102. Barker, H. A. Studies upon the methane-producing bacteria. Arch. für Mikrobiologie 7, 420–438 (1936).

    Article  CAS  Google Scholar 

  103. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977). This classic study shows how ribosomal RNA sequences reveal that all life follows one of three lines of descent from a common ancestor.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Spang, A., Caceres, E. F. & Ettema, T. J. G. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357, eaaf3883 (2017).

    Article  PubMed  CAS  Google Scholar 

  105. Blank, C. E. Not so old archaea — the antiquity of biogeochemical processes in the archaeal domain of life. Geobiology 7, 495–514 (2009).

    Article  CAS  PubMed  Google Scholar 

  106. Salvador-Castell, M., Tourte, M. & Oger, P. M. In search for the membrane regulators of archaea. Int. J. Mol. Sci. 20, 4434 (2019).

    Article  CAS  PubMed Central  Google Scholar 

  107. Koga, Y. & Morii, H. Recent advances in structural research on ether lipids from archaea including comparative and physiological aspects. Biosci. Biotechnol. Biochem. 69, 2019–2034 (2005).

    Article  CAS  PubMed  Google Scholar 

  108. Moldowan, J. M. & Seifert, W. K. Head-to-head linked isoprenoid hydrocarbons in petroleum. Science 204, 169–171 (1979).

    Article  CAS  PubMed  Google Scholar 

  109. Baumann, L. M. F. et al. Intact polar lipid and core lipid inventory of the hydrothermal vent methanogens Methanocaldococcus villosus and Methanothermococcus okinawensis. Org. Geochem. 126, 33–42 (2018).

    Article  CAS  Google Scholar 

  110. Summons, R. E., Powell, T. G. & Boreham, C. J. Petroleum geology and geochemistry of the Middle Proterozoic McArthur Basin, northern Australia: III. Composition of extractable hydrocarbons. Geochim. Cosmochim. Acta 52, 1747–1763 (1988).

    Article  CAS  Google Scholar 

  111. Tierney, J. E. in Treatise on Geochemistry Vol. 12 (eds Holland, H.D. & Turekian, K.K.) 379–393 (Elsevier, 2014).

  112. Weijers, J. W. H., Schouten, S., van den Donker, J. C., Hopmans, E. C. & Sinninghe Damsté, J. S. Environmental controls on bacterial tetraether membrane lipid distribution in soils. Geochim. Cosmochim. Acta 71, 703–713 (2007).

    Article  CAS  Google Scholar 

  113. Schouten, S., Forster, A., Panoto, F. E. & Sinninghe Damsté, J. S. Towards calibration of the TEX86 palaeothermometer for tropical sea surface temperatures in ancient greenhouse worlds. Org. Geochem. 38, 1537–1546 (2007).

    Article  CAS  Google Scholar 

  114. Schouten, S., Hopmans, E. C., Schefuß, E. & Sinninghe Damsté, J. S. Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Earth Planet. Sci. Lett. 204, 265–274 (2002). This study establishes the basis for the TEX86 palaeotemperature proxy as a SST based on the distribution of archaeal GDGT membrane lipids in marine sediments.

    Article  CAS  Google Scholar 

  115. Schouten, S., Hopmans, E. C. & Damsté, J. S. S. The effect of maturity and depositional redox conditions on archaeal tetraether lipid palaeothermometry. Org. Geochem. 35, 567–571 (2004).

    Article  CAS  Google Scholar 

  116. Tierney, J. E. GDGT thermometry: lipid tools for reconstructing paleotemperatures. Paleontol. Soc. Pap. 18, 115–132 (2012).

    Article  Google Scholar 

  117. Zhang, Y. G., Pagani, M. & Wang, Z. Ring Index: a new strategy to evaluate the integrity of TEX86 paleothermometry. Paleoceanography 31, 220–232 (2016).

    Article  Google Scholar 

  118. Kim, J.-H., Schouten, S., Hopmans, E. C., Donner, B. & Sinninghe Damsté, J. S. Global sediment core-top calibration of the TEX86 paleothermometer in the ocean. Geochim. Cosmochim. Acta 72, 1154–1173 (2008).

    Article  CAS  Google Scholar 

  119. Kim, J.-H. et al. New indices and calibrations derived from the distribution of crenarchaeal isoprenoid tetraether lipids: implications for past sea surface temperature reconstructions. Geochim. Cosmochim. Acta 74, 4639–4654 (2010).

    Article  CAS  Google Scholar 

  120. Trommer, G. et al. Distribution of Crenarchaeota tetraether membrane lipids in surface sediments from the Red Sea. Org. Geochem. 40, 724–731 (2009).

    Article  CAS  Google Scholar 

  121. Tierney, J. E. & Tingley, M. P. A Bayesian, spatially-varying calibration model for the TEX86 proxy. Geochim. Cosmochim. Acta 127, 83–106 (2014).

    Article  CAS  Google Scholar 

  122. Tierney, J. E. & Tingley, M. P. A TEX86 surface sediment database and extended Bayesian calibration. Sci. Data 2, 150029 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Zhou, A. et al. Energy flux controls tetraether lipid cyclization in Sulfolobus acidocaldarius. Environ. Microbiol. 22, 343–353 (2020).

    Article  CAS  PubMed  Google Scholar 

  124. Qin, W. et al. Confounding effects of oxygen and temperature on the TEX86 signature of marine Thaumarchaeota. Proc. Natl Acad. Sci. USA 112, 10979–10984 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Hurley, S. J. et al. Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX86 temperature proxy. Proc. Natl Acad. Sci. USA 113, 7762–7767 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. DeLong, E. F. Archaea in coastal marine environments. Proc. Natl Acad. Sci. USA 89, 5685–5689 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Lincoln, S. A. et al. Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean. Proc. Natl Acad. Sci. USA 111, 9858–9863 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Zeng, Z. et al. GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean. Proc. Natl Acad. Sci. USA 116, 22505–22511 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Besseling, M. A. et al. The absence of intact polar lipid-derived GDGTs in marine waters dominated by Marine Group II: implications for lipid biosynthesis in archaea. Sci. Rep. 10, 1–10 (2020).

    Article  CAS  Google Scholar 

  130. Pearson, A. Resolving a piece of the archaeal lipid puzzle. Proc. Natl Acad. Sci. USA 116, 22423–22425 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Gold, D. A., O’Reilly, S. S., Luo, G., Briggs, D. E. G. & Summons, R. E. Prospects for sterane preservation in sponge fossils from museum collections and the utility of sponge biomarkers for molecular clocks. Bull. Peabody Mus. Nat. History 57, 181–189 (2016).

    Article  Google Scholar 

  132. French, K. L. et al. Reappraisal of hydrocarbon biomarkers in Archean rocks. Proc. Natl Acad. Sci. USA 112, 5915–5920 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Lee, A. K. et al. C-4 sterol demethylation enzymes distinguish bacterial and eukaryotic sterol synthesis. Proc. Natl Acad. Sci. USA 115, 5884–5889 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Pollier, J. et al. A widespread alternative squalene epoxidase participates in eukaryote steroid biosynthesis. Nat. Microbiol. 4, 226–233 (2019).

    Article  CAS  PubMed  Google Scholar 

  135. Cronin, J. R., Pizzarello, S., Epstein, S. & Krishnamurthy, R. V. Molecular and isotopic analyses of the hydroxy acids, dicarboxylic acids, and hydroxydicarboxylic acids of the Murchison meteorite. Geochim. Cosmochim. Acta 57, 4745–4752 (1993).

    Article  CAS  PubMed  Google Scholar 

  136. Summons, R. E., Albrecht, P., McDonald, G. & Moldowan, J. M. Molecular biosignatures. Strateg. Life Detection 25, 133–159 (2008).

    Article  Google Scholar 

  137. Davila, A. F. & McKay, C. P. Chance and necessity in biochemistry: implications for the search for extraterrestrial biomarkers in Earth-like environments. Astrobiology 14, 534–540 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  138. Summons, R. E. et al. Preservation of martian organic and environmental records: final report of the Mars Biosignature Working Group. Astrobiology 11, 157–181 (2011).

    Article  PubMed  Google Scholar 

  139. McKay, C. P. What is life — and how do we search for it in other worlds? PLoS Biol. 2, e302 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  140. 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  CAS  PubMed  Google Scholar 

  141. Martin, A. P., Condon, D. J., Prave, A. R. & Lepland, A. A review of temporal constraints for the Palaeoproterozoic large, positive carbonate carbon isotope excursion (the Lomagundi–Jatuli Event). Earth Sci. Rev. 127, 242–261 (2013).

    Article  CAS  Google Scholar 

  142. Welander, P. V., Coleman, M., Sessions, A. L., Summons, R. E. & Newman, D. K. Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes. Proc. Natl Acad. Sci. USA 107, 8537–8542 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Zundel, M. & Rohmer, M. Prokaryotic triterpenoids. 3. The biosynthesis of 2β-methylhopanoids and 3β-methylhopanoids of Methylobacterium organophilum and Acetobacter pasteurianus ssp. pasteurianus. Eur. J. Biochem. 150, 35–39 (1985).

    Article  CAS  PubMed  Google Scholar 

  144. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Article  CAS  PubMed  Google Scholar 

  145. Eddy, S. R. Profile hidden Markov models. Bioinformatics 14, 755–763 (1998).

    Article  CAS  PubMed  Google Scholar 

  146. Finn, R. D. et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, D279–D285 (2016).

    Article  CAS  PubMed  Google Scholar 

  147. Schmerk, C. L., Bernards, M. A. & Valvano, M. A. Hopanoid production is required for low-pH tolerance, antimicrobial resistance, and motility in Burkholderia cenocepacia. J. Bacteriol. 193, 6712–6723 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Ricci, J. N., Morton, R., Kulkarni, G., Summers, M. L. & Newman, D. K. Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme. Geobiology 15, 173–183 (2017).

    Article  CAS  PubMed  Google Scholar 

  149. Garby, T. J. et al. Lack of methylated hopanoids renders the cyanobacterium Nostoc punctiforme sensitive to osmotic and pH stress. Appl. Environ. Microbiol. 83, e00777–00717 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Bradley, A. S. et al. Hopanoid-free Methylobacterium extorquens DM4 overproduces carotenoids and has widespread growth impairment. PLoS ONE 12, e0173323 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  151. Bergsten, J. A review of long-branch attraction. Cladistics 21, 163–193 (2005).

    Article  PubMed  Google Scholar 

  152. Chen, K., Durand, D. & Farach-Colton, M. NOTUNG: a program for dating gene duplications and optimizing gene family trees. J. Comput. Biol. 7, 429–447 (2000).

    Article  CAS  PubMed  Google Scholar 

  153. Wu, Y.-C., Rasmussen, M. D., Bansal, M. S. & Kellis, M. TreeFix: statistically informed gene tree error correction using species trees. Syst. Biol. 62, 110–120 (2013).

    Article  PubMed  Google Scholar 

  154. Magnabosco, C., Moore, K. R., Wolfe, J. M. & Fournier, G. P. Dating phototrophic microbial lineages with reticulate gene histories. Geobiology 16, 179–189 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Brasier, M. D. et al. Questioning the evidence for Earth’s oldest fossils. Nature 416, 76–81 (2002).

    Article  PubMed  Google Scholar 

  156. Knoll, A. H., Bergmann, K. D. & Strauss, J. V. Life: the first two billion years. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150493 (2016).

    Article  Google Scholar 

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Acknowledgements

This work was supported by a grant from the Simons Collaboration on the Origin of Life through an award (290361FY18) to R.E.S. and by National Science Foundation awards (1752564) to P.V.W and (2044871) to D.A.G.

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Authors and Affiliations

  1. Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

    Roger E. Summons

  2. Department of Earth System Science, Stanford University, Stanford, CA, USA

    Paula V. Welander

  3. Department of Earth & Planetary Sciences, University of California Davis, Davis, CA, USA

    David A. Gold

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  1. Roger E. Summons
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  2. Paula V. Welander
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  3. David A. Gold
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The authors contributed equally to all aspects of the article.

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Glossary

Warrawoona Group

A geological unit in Western Australia that includes the remains of microorganisms as old as 3.46 billion years.

Pilbara Craton

An ancient fragment of continental crust in Western Australia that includes rocks as old as 3.6 billion years.

Stromatolites

Layered sedimentary structures that form when a microbial community traps and binds sediment grains.

Hopanoids

A class of molecules comprising six C5 isoprene units folded into a pentacyclic ring system.

Accessory pigment

A coloured molecule that absorbs light and works in concert with the primary pigment, typically chlorophyll a.

Sedimentary diagenesis

The processes by which sedimentary rocks and their components became modified over time during burial.

Carbonaceous chondrites

Carbon-rich meteorites composed of small mineral grains and representing some of the post-primitive material in the solar system.

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Summons, R.E., Welander, P.V. & Gold, D.A. Lipid biomarkers: molecular tools for illuminating the history of microbial life. Nat Rev Microbiol 20, 174–185 (2022). https://doi.org/10.1038/s41579-021-00636-2

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