Review Article

The slow rise of complex life as revealed through biomarker genetics
David A. Gold
Emerging Topics in Life Sciences Jun 29, 2018, ETLS20170150; DOI: 10.1042/ETLS20170150

Abstract

Organic molecules preserved in ancient rocks can function as ‘biomarkers’, providing a unique window into the evolution of life. While biomarkers demonstrate intriguing patterns through the Neoproterozoic, it can be difficult to constrain particular biomarkers to specific organisms. The goal of the present paper is to demonstrate the utility of biomarkers when we focus less on which organisms produce them, and more on how their underlying genetic pathways evolved. Using this approach, it becomes clear that there are discrepancies between the biomarker, fossil, and molecular records. However, these discrepancies probably represent long time periods between the diversification of eukaryotic groups through the Neoproterozoic and their eventual rise to ecological significance. This ‘long fuse’ hypothesis contrasts with the adaptive radiations often associated with the development of complex life.

  • biomarkers
  • eukaryotes
  • evolutionary biology
  • sterols

Introduction

Genetics offers an exciting vantage to study evolution, but geology takes primacy as a direct window into the past [1]. By its nature, the fossil record will always be woefully incomplete, but new technologies continually push the boundaries of what can be recovered; clumped isotopes reveal the metabolic rates of extinct organisms [2,3], fossilized melanosomes demonstrate the colors of preserved skin and feathers [4,5], and proteins are being recovered from increasingly old specimens [6,7]. One important contribution to this paleontological renaissance comes from geochemistry, where the molecular compounds produced by long-extinct organisms can be extracted from rocks and analyzed using mass spectrometry. These organic compounds — collectively referred to as ‘molecular fossils’ or ‘biomarkers’ — provide insights into the organisms that existed in the deep past, even when traditional fossils fail to preserve [8].

In this review, I will focus on a particular class of biomarkers called steranes. There are many other interesting biomarkers; 2-methylhopanes, for example, are produced by cyanobacteria and have been used to infer microbial community dynamics across major Earth history events [9,10]. However, steranes are particularly relevant to the Neoproterozoic, as they show dynamic fluctuations during this period that are thought to chart the evolution of complex life. It has been suggested that steranes offer a single character for evolutionary analysis and are therefore insufficient to identify specific lifeforms in the past [11,12]; I strongly disagree with this logic. Many scientists have spent decades elucidating the genetic underpinnings of biomarker biosynthesis [13]. Thanks to this effort, a biomarker is not merely a single chemical compound, it also speaks to the many genes required to make it. By combining genetic and geochemical data, we have an opportunity to fully leverage the information inherent in biomarkers.

Understanding sterane biomarkers

Interpreting sterane biomarkers requires an understanding of their molecular structure. Steranes are the degraded (in geological terms, diagenetic) products of sterols, which are a class of lipid molecules. All sterols share a basic carbon skeleton structure, which includes a cyclopentic ring nucleus and a side chain (Figure 1). The sterol shown in Figure 1A is cholesterol — the sterol that is probably most familiar to readers — but various organisms modify the side chain and/or nucleus to make hundreds of different variants. Over deep time, preserved sterols tend to lose the alcohol (OH) functional group attached to the third carbon. When this occurs, the sterol is now referred to as a sterane. Other than the loss of this functional group and most double bonds, steranes are highly resistant to diagenesis when incorporated into macromolecular structures such as petroleums and bitumens [8]. In addition to cholestane (the sterane derivative of cholesterol), common steranes preserved in the geologic record include ergostane (a derivative of the 28-carbon ergosterol) and stigmastane (a derivative of the 29-carbon stigmasterol/sitosterol). A variety of common and rare steranes are shown in Figure 1B.

Figure 1.
Figure 1. Sterol structure and diversity through time.

(A) Carbon skeleton structure of cholesterol. (B) The structure of six geologically important steranes. The number of carbons in each sterane is indicated to the right. (C) The relative abundance of these six steranes through geological time. Note that the Neoproterozoic and Phanerozoic are not shown to scale. Data for (C) adapted from ref. [20].

Many sterols are produced by specific lineages of life; in biological terms, such sterols are phylogenetically informative. Complex sterols, such as ergosterol and stigmasterol, are restricted to eukaryotic lifeforms [14,15]. Thus, the presence of steranes in the fossil record indicates the evolution of eukaryotic life. Additionally, certain sterols are more common in some eukaryotic groups than others. In sweeping generalities (that will be nuanced later in the present paper), ergostanes are often considered a biomarker for fungi and algae, 29-carbon steranes like stigmastane indicate plants and green algae, and 24-isoproylcholestane is a biomarker for prehistoric sea sponges. These patterns help scientists ‘read’ the biomarker record and determine which organisms were dominant at different points in the past.

The trajectory of steranes through the Neoproterozoic

The biomarker record in the Neoproterozoic demonstrates dramatic fluctuations and is summarized in Figure 1C. The oldest steranes were once thought to come from ∼2.7 billion-year-old rocks from the Pilbara Craton in Australia, but these have since been rejected as contamination [16,17]. Most of the published pre-Ediacaran biomarker record might also be compromised by younger contaminants, and resolving this is an important area of active research [18,19]. Today, the oldest accepted steranes occur ∼820 million years ago (Mya) [20]. For ∼100 million years, sterane concentrations remain low relative to bacterial hopanes [21]. Cholestanes are the dominant steranes found in these rocks, although trace amounts of an unusual sterane called cryostane have also been recovered [20,22]. The Cryogenian period (720–635 Mya) represents a time of increasing sterane diversity and abundance. Between the Sturtian and Marinoan glaciation events, steranes increase two to three orders of magnitude relative to hopanes [20]. Ergostane and stigmastane reach approximately modern levels, and rare steranes, such as 24-isopropylcholestane and 24-n-propylcholestane, first appear [20,23].

Taken at face value, this record could signify the evolution and expansion of marine eukaryotic life. The presence of cholestanes ∼820 Mya could represent the evolution of unicellular eukaryotes, and perhaps multicellular red algae (rhodophytes), which predominantly synthesize cholesterol today [21]. The expansion of stigmastanes would mark the development of green algae (chlorophytes), while ergostanes signify the presence of fungi and/or additional marine eukaryotes (stramenopiles/alveolates/rhizarians). 24-isopropylcholestane would mark the evolution of sea sponges and thus the earliest animals [24]. This offers a narrative of eukaryotic diversification starting in the interglacial period of the Cryogenian, which continued through the Neoproterozoic until the Cambrian explosion of modern animal groups [25,26].

As compelling as this story is, it is inconsistent with other lines of evidence. For example, eukaryotes appear to have evolved well before ∼820 Mya. Molecular clocks — which compare genetic differences between living organisms to infer the timing of their last common ancestor [27] — place the origin of living eukaryotes between 950 and 1870 Mya [28–30]. Fossils also suggest an older history; Bangiomorpha pubescens is a well-accepted red algae from ∼1047 Mya [31], while other, more controversial red algae could be closer to 1600 Mya [32]. Sponge biomarkers have the opposite problem; unequivocal sponge fossils do not appear until the Cambrian, almost ∼100 million years after the origin of sponge biomarkers. These discrepancies have led to some doubt about our interpretations of the biomarker record.

The above statements describing the sources of various biomarkers are based on studies of living organisms, but a more rigorous way to interpret biomarkers is by thinking about the evolution of the genes required for their biosynthesis. A recurring theme throughout the present paper is that genes have a distinct evolutionary history from species. I have illustrated this point in Figure 2. When one species splits into two, each carries a copy of an ancestral gene. In one lineage that gene might eventually be removed by natural selection, while in the other lineage a gene duplication event occurs, meaning it now has two copies. Additionally, horizontal gene transfer allows genes to be swapped between distantly related organisms (this process appears to have been critical for the early evolution of sterol biosynthesis [33]). The important takeaway is that evolutionary events at the genetic level can occur at different times than the events that lead to different species. These patterns of gene loss, gene duplication, and horizontal gene transfer dictate the types of sterols that different lineages can produce. For the rest of the present paper, I will provide two case studies that show how a gene-centered view of sterol evolution helps clarify the patterns seen in the sterol record.

Figure 2.
Figure 2. Examples of evolution from the gene's perspective.

The history of two genes is illustrated in this scenario; the first indicated with a solid line and the second with a dotted line. Images adapted from ref. [34].

Sponge biomarkers and the rise of animal life

A plethora of Neoproterozoic sponge fossils have been described, but all remain controversial. I am inclined to agree with several recent reviews that suggest there are no unambiguous sponge fossils prior to the Cambrian [35,36]. This is, however, in complete disagreement with the molecular data, which consistently support a Neoproterozoic origin for sponge diversification [37–42]. In this regard, the presence of putative sponge biomarkers ∼650 Mya is compelling, as it brings the geological and genetic records into general congruence. It is possible that the Precambrian sponge fossil record has been lost due to significant taphonomic bias caused by sparse biomineralization in early sponges and/or poor preservation conditions [43]. It is worth noting that anoxic deposits from the Late Permian are associated with a decrease in the size and abundance of siliceous sponge spicules [44], and that oxygen levels would have been even lower in the Neoproterozoic. However, I sympathize with paleontologists who express skepticism regarding the extensive missing fossil record that biomarkers imply, particularly given the effort scientists have made in trying to find Precambrian sponges. Is it possible that convincing sponge fossils have not been found in the Neoproterozoic because they do not exist? My goal is to walk readers through the sponge biomarker hypothesis and give my perspective on the idea's strengths and limitations.

The sponge biomarker hypothesis [24,45] is an attempt to explain the relative abundance of 24-isopropylcholestanes in certain Neoproterozoic rocks. The 30-carbon (C30) precursor sterol is exceedingly rare in nature, but is found in two relevant lineages, the demosponges (a subset of living sea sponges) and pelagophyte algae. Some sea sponges produce 24-isopropylcholesterol as the major component of their lipid biomass [46–48], while pelagophytes produce trace amounts of the sterol during the biosynthesis of a different compound, 24-n-propylcholesterol (Figure 1B) [49–54]. Based on these observations, the ratio in rocks of 24-isopropylcholestanes to 24-n-propylcholestanes (24ipc/24npc) should be indicative of their source: low 24ipc/24npc ratios provide a biomarker for algae, while high ratios indicate sponges. Of course, all of these ideas are based on the production of sterols in living organisms; how can we be confident that pelagophyte algae did not produce larger quantities of 24-isopropylcholestrol in the deep past [12]?

This question can be addressed at the genetic level. Scientists have determined that the gene sterol 24-C-methyltransferase (or smt) is required to add methyl groups (carbon) to the 24th carbon in the sterol skeleton (Figure 1) [55]. In most cases, the number of smt genes an organism has dictates the upper limit to the number of methyl groups that can be added to carbon 24 [56]. Pelagophyte alage and sponges both appear to produce C30 sterols through independent gene duplications of the smt gene. So, understanding when these gene duplication events occurred can elucidate when the two lineages evolved the ability to produce C30 sterols.

Figure 3 shows a molecular clock of the smt gene (adapted from ref. [56]). In other words, this analysis tracks the pattern of speciation events and gene duplication events that led to the diversity of smt genes that exist across eukaryotes today. Every star in this figure marks a gene duplication event; the stars relevant to sponge and algal duplications are highlighted in yellow. The bars around each star represent 95% confidence windows. As the bars demonstrate, there is significant uncertainty regarding the timing of these gene duplication events. But, the results strongly reject one hypothesis for the sterane's source; the gene duplication event in the algal lineage did not occur until hundreds of millions of years after the Neoproterozoic. This work provides compelling evidence that neither pelagophyte algae nor their direct ancestors had the genes necessary to produce C30 sterols in the Neoproterozoic.

Figure 3.
Figure 3. A molecular clock of the smt gene, illustrating the origins of 24-isopropylcholesterol.

These results refute the hypothesis that pelagophyte algae could be responsible for Neoproterozoic biomarkers, but several additional arguments against the sponge biomarker hypothesis have been proposed. One claim is that this biomarker disappears in the Cambrian which, in seeming contradiction, is precisely when diverse sponge fossils finally show up. This argument is not entirely correct. It is not true that 24-isopropylcholestanes disappear in the Cambrian; instead, the 24ipc/24npc ratio becomes heavily biased toward 24-n-propylcholestanes [45]. This is consistent with increased algal outputs relative to sponges in the Cambrian. Secondly, most sponges do not produce 24-isopropylcholestrol, and while the sterol is present in all major classes of demosponges, only a handful of species produce it as a significant component of their sterol repertoire [24]. It is therefore quite possible that the drop in 24-isopropylcholestanes after the Cambrian represents the replacement of a dominant, primitive sponge lineage by various diverse forms found in the Cambrian, many of which traded 24-isopropylcholestrol for other sterols.

A second argument is how do we know that another group of organisms (either unsampled or extinct) did not converge on the ability to synthesize 24-isopropylcholesterol? This is a more serious problem, and given the nature of science will never be fully refutable. However, I do not think this problem is intractable. Sterol pathways have not changed much in eukaryotes over evolutionary time. Key enzymes in the sterol biosynthesis pathway are deeply conserved [13,57], and major clades of eukaryotes tend to produce similar sets of sterols [58]. No demonstrably extinct sterols have been identified in the fossil record [59]. Sponges are unique among living organisms in the diversity of unusual sterols they produce. From a genetic level, they appear to do this through a two-step process. Firstly, modification of the sponge smt gene allows for the promiscuous methylation of sterols, meaning a single SMT enzyme can generate both C28 and C29 sterols [56,60]. One or more gene duplication events resulted in additional sponge smt genes, which allow for the production of rare C30 sterols [56]. This hypothesis has only been proposed over the last few years and needs to be further tested with additional genetic and functional experiments. Most importantly, more genetic data need to be collected from sponge species that produce C30 sterols as their primary lipids. However, the more we come to understand about the genetic history of sponge smt genes, the more complex their evolution appears to be, and the less likely convergence appears.

As a final point for those interested in molecular clocks, the inability to fully rule out alternative sterane sources — combined with uncertainty about when precisely demosponges evolved the ability to produce this compound [61] — is why sponge biomarkers should not be used for the calibration of molecular clocks. Fortunately, the inclusion of sponge biomarkers as a molecular clock calibration is not necessary to get a Neoproterozoic origin for sponges, and the two should be treated as independent lines of evidence for sponge-grade animals existing in the Cryogenian. I find this convergence of data compelling evidence for a Neoproterozoic origin of animal life, and enigmatic fossils from this period should be considered in light of these data.

Algal biomarkers: a Cryogenian diversification?

For this second case study, I would like to turn back to the major pattern of Neoproterozoic steranes — the diversification of ergosteranes and stigmastanes following the Sturtian glaciation. Hoshino et al. [23] emphasize that this pattern is consistent with the genetic record as described in ref. [56]. They note that molecular clock data suggest that green algal smt genes diverged in the Late Cryogenian, and that ‘stigmasteroid biosynthesis emerged in an ancestral green algae and subsequently led to the rise of this group to ecological dominance’. I have reproduced the relevant image in Figure 4. To be clear, I think Hoshino et al. provide important new data on the biomarker record, and present an intriguing hypothesis about the rise of complex life. However, interpreting their particular claim in the light of the gene/species evolution dichotomy reveals that the genetic data are more problematic than Hoshino et al. suggest.

Figure 4.
Figure 4. A molecular clock of the smt gene, illustrating the origins of C29 sterols.

The same molecular clock from Figure 3, with annotations made by Hoshino et al. [23]. I note the origin of the relevant gene duplication event using a yellow star.

What Hoshino et al. focus on is a speciation event, specifically when the green algae Ostreococcus tauri separated from higher plants. But, stigmastanes are far more ubiquitous than 24-isopropylcholestanes. Many other eukaryotes, besides green algae and plants, synthesize C29 sterols, including certain fungi, ichthyosporeans, amoebas, sea sponges, eustigmatophytes, and kinetoplastids [56,57,60,62,63]. In most of these organisms, the ability to synthesize C29 sterols is associated with a second copy of the smt gene [56]. So, from a genetics perspective, the question is not when did green algae like Ostreococcus evolve, but when did eukaryotes evolve a second smt gene?

Figure 4 suggests that the ‘algal’ gene duplication event is actually quite old and extends all the way back to the origin of the Bikonta (i.e. the last common ancestor of stramenopile algae and green algae). The molecular data therefore suggest that the ability to make C29 sterols predates stigmastanes in the rock record by hundreds of millions of years. It also shows that C29 biosynthesis is an ancient trait in eukaryotes. It is therefore unlikely that the evolution of stigmasteroid biosynthesis played a causal role in the success of green algae in the Neoproterozoic, as this ability already existed in its ancestors for hundreds of millions of years. The basic premise of Hoshino et al. — that the rise of stigmastanes in the Neoproterozoic coincides with the rise of green algae — is still consistent with the molecular data, but a gene-centered understanding of biomarkers reveals as many questions as answers.

Conclusion

At first glance, a gene-centered interpretation of the biomarker record suggests significant discrepancies between the geochemical, paleontological, and molecular datasets. In truth, I think they are telling us a consistent story. I suspect the likeliest explanation for these discrepancies is a ‘long fuse’ hypothesis, meaning there is often a lag time between when organisms first evolve, and when they achieve sufficient ecological presence to leave a fossil record. Molecular clocks suggest red and green algae evolved in the Paleo/Mesoproterozoic [64,65], consistent with the presence of Bangiomorpha in the fossil record. Presumably, the sulfidic oceans and global glaciation events that dominated the Meso- and Neoproterozoic kept algal populations small, as indicated by undetectable-to-low sterane levels [20,25,66]. Only after the Sturtian glaciation event and the increased oxygenation of ocean waters did algae come to dominate the ocean's photic zone and subsequently leave a biomarker record. Similarly, molecular clocks consistently demonstrate that animals evolved in the Cryogenian [38,39,67]. 24-Isopropylcholestanes suggest that sponge-grade animals were present at this time, but it is unclear how common they were, or whether they produced the structural spicules that are diagnostic of sponge fossils [37]. Putative animals’ fossils through the Neoproterozoic suggest that most forms were uncommon, small, unmineralized, and generally unlikely to leave a fossil record [68–71]. It was only after the Cambrian that biomineralization evolved and animal diversity radiated. If this ‘long fuse’ hypothesis is correct, then I predict that the earliest members of eukaryote groups will also be some of the hardest to find. These point to the importance of combining genetic, fossil, and geochemical tools to explore this critical phase of Earth's history.

Summary

  • Organic compounds preserved in rocks can provide biomarkers for prehistoric organisms.

  • Sterane biomarkers show a complicated pattern through the Neoproterozoic that could represent the evolution of complex life.

  • Steranes are difficult to interpret on their own, but studying the genes responsible for their biosynthesis reveals what organism(s) could have produced them.

  • Combining biomarker, fossil, and genetic data suggests a lag time between the origin of several major groups (such as algae and animals) and when they become ecologically important enough to leave fossil records.

Competing Interests

The Authors declare that there are no competing interests associated with the manuscript.

Abbreviations: 24ipc/24npc, 24-isopropylcholestanes/24-n-propylcholestanes; C30, 30-carbon; Mya, million years ago; smt, sterol 24-C-methyltransferase

  • Received February 6, 2018.
  • Revision received April 30, 2018.
  • Accepted May 23, 2018.

References

  1. ↵
    1. Pisani, D. and
    2. Liu, A.G.
    (2015) Animal evolution: only rocks can set the clock. Curr. Biol. 25, R1079–R1081 doi:10.1016/j.cub.2015.10.015
    OpenUrlCrossRef
  2. ↵
    1. Eagle, R.A.,
    2. Schauble, E.A.,
    3. Tripati, A.K.,
    4. Tütken, T.,
    5. Hulbert, R.C. and
    6. Eiler, J.M.
    (2010) Body temperatures of modern and extinct vertebrates from 13C-18O bond abundances in bioapatite. Proc. Natl Acad. Sci. U.S.A. 107, 10377–10382 doi:10.1073/pnas.0911115107
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Eagle, R.A.,
    2. Tütken, T.,
    3. Martin, T.S.,
    4. Tripati, A.K.,
    5. Fricke, H.C.,
    6. Connely, M.
    (2011) Dinosaur body temperatures determined from isotopic (13C-18O) ordering in fossil biominerals. Science 333, 443–445 doi:10.1126/science.1206196
    OpenUrlAbstract/FREE Full Text
  4. ↵
    1. Zhang, F.,
    2. Kearns, S.L.,
    3. Orr, P.J.,
    4. Benton, M.J.,
    5. Zhou, Z.,
    6. Johnson, D.
    (2010) Fossilized melanosomes and the colour of Cretaceous dinosaurs and birds. Nature 463, 1075–1078 doi:10.1038/nature08740
    OpenUrlCrossRefGeoRefPubMedWeb of Science
  5. ↵
    1. Brown, C.M.,
    2. Henderson, D.M.,
    3. Vinther, J.,
    4. Fletcher, I.,
    5. Sistiaga, A.,
    6. Herrera, J.
    (2017) An exceptionally preserved three-dimensional armored dinosaur reveals insights into coloration and Cretaceous predator-prey dynamics. Curr. Biol. 27, 2514–2521.e3 doi:10.1016/j.cub.2017.06.071
    OpenUrlCrossRef
  6. ↵
    1. Lee, Y.-C.,
    2. Chiang, C.-C.,
    3. Huang, P.-Y.,
    4. Chung, C.-Y.,
    5. Huang, T.D.,
    6. Wang, C.-C.
    (2017) Evidence of preserved collagen in an Early Jurassic sauropodomorph dinosaur revealed by synchrotron FTIR microspectroscopy. Nat. Commun. 8, 14220 doi:10.1038/ncomms14220
    OpenUrlCrossRef
  7. ↵
    1. Greenwalt, D.E.,
    2. Goreva, Y.S.,
    3. Siljeström, S.M.,
    4. Rose, T. and
    5. Harbach, R.E.
    (2013) Hemoglobin-derived porphyrins preserved in a Middle Eocene blood-engorged mosquito. Proc. Natl Acad. Sci. U.S.A. 110, 18496–18500 doi:10.1073/pnas.1310885110
    OpenUrlAbstract/FREE Full Text
  8. ↵
    1. Briggs, D.E.G. and
    2. Summons, R.E.
    (2014) Ancient biomolecules: their origins, fossilization, and role in revealing the history of life. BioEssays 36, 482–490 doi:10.1002/bies.201400010
    OpenUrlCrossRefPubMed
  9. ↵
    1. Xie, S.,
    2. Pancost, R.D.,
    3. Yin, H.,
    4. Wang, H. and
    5. Evershed, R.P.
    (2005) Two episodes of microbial change coupled with Permo/Triassic faunal mass extinction. Nature 434, 494–497 doi:10.1038/nature03396
    OpenUrlCrossRefPubMedWeb of Science
  10. ↵
    1. Kuypers, M.M.M.,
    2. van Breugel, Y.,
    3. Schouten, S.,
    4. Erba, E. and
    5. Damsté, J.S.S.
    (2004) N2-fixing cyanobacteria supplied nutrient N for Cretaceous oceanic anoxic events. Geology 32, 853–856 doi:10.1130/G20458.1
    OpenUrlAbstract/FREE Full Text
  11. ↵
    1. Cunningham, J.A.,
    2. Liu, A.G.,
    3. Bengtson, S. and
    4. Donoghue, P.C.J.
    (2017) The origin of animals: can molecular clocks and the fossil record be reconciled? BioEssays 39, 1–12 doi:10.1002/bies.201600120
    OpenUrlCrossRef
  12. ↵
    1. Antcliffe, J.B.
    (2013) Questioning the evidence of organic compounds called sponge biomarkers. Palaeontology 56, 917–925 doi:10.1111/pala.12030
    OpenUrlCrossRefGeoRefWeb of Science
  13. ↵
    1. Summons, R.E.,
    2. Bradley, A.S.,
    3. Jahnke, L.L. and
    4. Waldbauer, J.R.
    (2006) Steroids, triterpenoids and molecular oxygen. Philos. Trans. R. Soc. B: Biol. Sci. 361, 951–968 doi:10.1098/rstb.2006.1837
    OpenUrlAbstract/FREE Full Text
  14. ↵
    1. Pearson, A.,
    2. Budin, M. and
    3. Brocks, J.J.
    (2003) Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc. Natl Acad. Sci. U.S.A. 100, 15352–15357 doi:10.1073/pnas.2536559100
    OpenUrlAbstract/FREE Full Text
  15. ↵
    1. Wei, J.H.,
    2. Yin, X. and
    3. Welander, P.V.
    (2016) Sterol synthesis in diverse bacteria. Front. Microbiol. 7, 990 doi:10.3389/fmicb.2016.00990
    OpenUrlCrossRef
  16. ↵
    1. Brocks, J.J.,
    2. Logan, G.A.,
    3. Buick, R. and
    4. Summons, R.E.
    (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036 doi:10.1126/science.285.5430.1033
    OpenUrlCrossRefGeoRefPubMedWeb of Science
  17. ↵
    1. French, K.L.,
    2. Hallmann, C.,
    3. Hope, J.M.,
    4. Schoon, P.L.,
    5. Zumberge, J.A.,
    6. Hoshino, Y.
    (2015) Reappraisal of hydrocarbon biomarkers in Archean rocks. Proc. Natl Acad. Sci. U.S.A. 112, 5915–5920 doi:10.1073/pnas.1419563112
    OpenUrlAbstract/FREE Full Text
  18. ↵
    1. Brocks, J.J.
    (2011) Millimeter-scale concentration gradients of hydrocarbons in Archean shales: live-oil escape or fingerprint of contamination? Geochim. Cosmochim. Acta 75, 3196–3213 doi:10.1016/j.gca.2011.03.014
    OpenUrlCrossRefGeoRefWeb of Science
  19. ↵
    1. Rasmussen, B.,
    2. Fletcher, I.R.,
    3. Brocks, J.J. and
    4. Kilburn, M.R.
    (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1104 doi:10.1038/nature07381
    OpenUrlCrossRefGeoRefPubMedWeb of Science
  20. ↵
    1. Brocks, J.J.,
    2. Jarrett, A.J.M.,
    3. Sirantoine, E.,
    4. Hallmann, C.,
    5. Hoshino, Y. and
    6. Liyanage, T.
    (2017) The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578–581 doi:10.1038/nature23457
    OpenUrlCrossRef
  21. ↵
    1. Summons, R.E.,
    2. Brassell, S.C.,
    3. Eglinton, G.,
    4. Evans, E.,
    5. Horodyski, R.J.,
    6. Robinson, N.
    (1988) Distinctive hydrocarbon biomarkers from fossiliferous sediment of the Late Proterozoic Walcott Member, Chuar Group, Grand Canyon, Arizona. Geochim. Cosmochim. Acta 52, 2625–2637 doi:10.1016/0016-7037(88)90031-2
    OpenUrlCrossRefGeoRefWeb of Science
  22. ↵
    1. Brocks, J.J.,
    2. Jarrett, A.J.M.,
    3. Sirantoine, E.,
    4. Kenig, F.,
    5. Moczydłowska, M.,
    6. Porter, S.
    (2016) Early sponges and toxic protists: possible sources of cryostane, an age diagnostic biomarker antedating Sturtian Snowball Earth. Geobiology 14, 129–149 doi:10.1111/gbi.12165
    OpenUrlCrossRefPubMed
  23. ↵
    1. Hoshino, Y.,
    2. Poshibaeva, A.,
    3. Meredith, W.,
    4. Snape, C.,
    5. Poshibaev, V.,
    6. Versteegh, G.J.M.
    (2017) Cryogenian evolution of stigmasteroid biosynthesis. Sci. Adv. 3, e1700887 doi:10.1126/sciadv.1700887
    OpenUrlFREE Full Text
  24. ↵
    1. Love, G.D.,
    2. Grosjean, E.,
    3. Stalvies, C.,
    4. Fike, D.A.,
    5. Grotzinger, J.P.,
    6. Bradley, A.S.
    (2009) Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 doi:10.1038/nature07673
    OpenUrlCrossRefGeoRefPubMedWeb of Science
  25. ↵
    1. Canfield, D.E.,
    2. Poulton, S.W. and
    3. Narbonne, G.M.
    (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 92–95 doi:10.1126/science.1135013
    OpenUrlAbstract/FREE Full Text
  26. ↵
    1. Chen, X.,
    2. Ling, H.-F.,
    3. Vance, D.,
    4. Shields-Zhou, G.A.,
    5. Zhu, M.,
    6. Poulton, S.W.
    (2015) Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nat. Commun. 6, 7142 doi:10.1038/ncomms8142
    OpenUrlCrossRefPubMed
  27. ↵
    1. Lee, M.S.Y. and
    2. Ho, S.Y.W.
    (2016) Molecular clocks. Curr. Biol. 26, R399–R402 doi:10.1016/j.cub.2016.03.071
    OpenUrlCrossRef
  28. ↵
    1. Douzery, E.J.P.,
    2. Snell, E.A.,
    3. Bapteste, E.,
    4. Delsuc, F. and
    5. Philippe, H.
    (2004) The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc. Natl Acad. Sci. U.S.A. 101, 15386–15391 doi:10.1073/pnas.0403984101
    OpenUrlAbstract/FREE Full Text
    1. Berney, C. and
    2. Pawlowski, J.
    (2006) A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc. R. Soc. Lond. B Biol. Sci. 273, 1867–1872 doi:10.1098/rspb.2006.3537
    OpenUrlAbstract/FREE Full Text
  30. ↵
    1. Parfrey, L.W.,
    2. Lahr, D.J.G.,
    3. Knoll, A.H. and
    4. Katz, L.A.
    (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. U.S.A. 108, 13624–13629 doi:10.1073/pnas.1110633108
    OpenUrlAbstract/FREE Full Text
  31. ↵
    1. Gibson, T.M.,
    2. Shih, P.M.,
    3. Cumming, V.M.,
    4. Fischer, W.W.,
    5. Crockford, P.W.,
    6. Hodgskiss, M.S.
    (2017) Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology 46, 135–138 doi:10.1130/G39829.1
    OpenUrlCrossRef
  32. ↵
    1. Bengtson, S.,
    2. Sallstedt, T.,
    3. Belivanova, V. and
    4. Whitehouse, M.
    (2017) Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLoS Biol. 15, e2000735 doi:10.1371/journal.pbio.2000735
    OpenUrlCrossRef
  33. ↵
    1. Gold, D.A.,
    2. Caron, A.,
    3. Fournier, G.P. and
    4. Summons, R.E.
    (2017) Paleoproterozoic sterol biosynthesis and the rise of oxygen. Nature 543, 420–423 doi:10.1038/nature21412
    OpenUrlCrossRef
  34. ↵
    1. Knight, C
    . (1843) Pictorial Museum of Animated Nature, Charles Knight and Company, London.
  35. ↵
    1. Botting, J.P. and
    2. Muir, L.A.
    (2017) Early sponge evolution: a review and phylogenetic framework. Palaeoworld 27, 1–29 doi:10.1016/j.palwor.2017.07.001
    OpenUrlCrossRef
  36. ↵
    1. Antcliffe, J.B.,
    2. Callow, R.H.T. and
    3. Brasier, M.D.
    (2014) Giving the early fossil record of sponges a squeeze. Biol. Rev. 89, 972–1004 doi:10.1111/brv.12090
    OpenUrlCrossRefGeoRef
  37. ↵
    1. Sperling, E.A.,
    2. Robinson, J.M.,
    3. Pisani, D. and
    4. Peterson, K.J.
    (2010) Where's the glass? Biomarkers, molecular clocks, and microRNAs suggest a 200-Myr missing Precambrian fossil record of siliceous sponge spicules. Geobiology 8, 24–36 doi:10.1111/j.1472-4669.2009.00225.x
    OpenUrlCrossRefPubMedWeb of Science
  38. ↵
    1. Erwin, D.H.,
    2. Laflamme, M.,
    3. Tweedt, S.M.,
    4. Sperling, E.A.,
    5. Pisani, D. and
    6. Peterson, K.J.
    (2011) The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 doi:10.1126/science.1206375
    OpenUrlAbstract/FREE Full Text
  39. ↵
    1. Dohrmann, M. and
    2. Wörheide, G
    . (2017) Dating early animal evolution using phylogenomic data. Sci. Res. 7, 3599 doi:10.1038/s41598-017-03791-w
    OpenUrlCrossRef
    1. Sharpe, S.C.,
    2. Eme, L.,
    3. Brown, M.W. and
    4. Roger, A.J.
    (2015) Timing the origins of multicellular eukaryotes through phylogenomics and relaxed molecular clock analyses. In Evolutionary Transitions to Multicellular Life (Ruiz-Trillo, I. and Nedelcu, A.M., eds), pp. 3–29, Springer, Dordrecht
    1. Ma, J.-Y. and
    2. Yang, Q.
    (2016) Early divergence dates of demosponges based on mitogenomics and evaluated fossil calibrations. Palaeoworld 25, 292–302 doi:10.1016/j.palwor.2015.03.004
    OpenUrlCrossRef
  42. ↵
    1. Schuster, A.,
    2. Vargas, S.,
    3. Knapp, I.,
    4. Pomponi, S.A.,
    5. Toonen, R.J.,
    6. Erpenbeck, D.
    (2017) Divergence times in demosponges (Porifera): first insights from new mitogenomes and the inclusion of fossils in a birth-death clock model. bioRxiv 159806 doi:10.1101/159806
    OpenUrlAbstract/FREE Full Text
  43. ↵
    1. Muscente, A.D.,
    2. Michel, F.M.,
    3. Dale, J.G. and
    4. Xiao, S.
    (2015) Assessing the veracity of Precambrian ‘sponge’ fossils using in situ nanoscale analytical techniques. Precambrian Res. 263, 142–156 doi:10.1016/j.precamres.2015.03.010
    OpenUrlCrossRefGeoRef
  44. ↵
    1. Liu, G.,
    2. Feng, Q.,
    3. Shen, J.,
    4. Yu, J.,
    5. He, W. and
    6. Algeo, T.J.
    (2013) Decline of siliceous sponges and spicule miniaturization induced by marine productivity collapse and expanding anoxia during the Permian-Triassic crisis in South China. Palaios 28, 664–679 doi:10.2110/palo.2013.p13-035r
    OpenUrlAbstract/FREE Full Text
  45. ↵
    1. McCaffrey, M.A.,
    2. Moldowan, J.M.,
    3. Lipton, P.A.,
    4. Summons, R.E.,
    5. Peters, K.E.,
    6. Jeganathan, A.
    (1994) Paleoenvironmental implications of novel C30 steranes in Precambrian to Cenozoic age petroleum and bitumen. Geochim. Cosmochim. Acta 58, 529–532 doi:10.1016/0016-7037(94)90481-2
    OpenUrlCrossRefGeoRefWeb of Science
  46. ↵
    1. Hofheinz, W. and
    2. Oesterhelt, G.
    (1979) 24-Isopropylcholesterol and 22-Dehydro-24-isopropylcholesterol, Novel Sterols from a Sponge. Helv. Chim. Acta 62, 1307–1309 doi:10.1002/hlca.19790620443
    OpenUrlCrossRef
    1. Umeyama, A.,
    2. Adachi, K.,
    3. Ito, S. and
    4. Arihara, S.
    (2000) New 24-isopropylcholesterol and 24-isopropenylcholesterol sulfate from the marine sponge Epipolasis species. J. Nat. Prod. 63, 1175–1177 doi:10.1021/np000024j
    OpenUrlCrossRefPubMed
  48. ↵
    1. Dai, J.,
    2. Sorribas, A.,
    3. Yoshida, W.Y.,
    4. Kelly, M. and
    5. Williams, P.G.
    (2010) Topsentinols, 24-isopropyl steroids from the marine sponge Topsentia sp. J. Nat. Prod. 73, 1597–1600 doi:10.1021/np100374b
    OpenUrlCrossRefPubMed
  49. ↵
    1. Kokke, W.,
    2. Shoolery, J.N.,
    3. Fenical, W. and
    4. Djerassi, C.
    (1984) Biosynthetic studies of marine lipids. 4. Mechanism of side chain alkylation in E-24-propylidenecholesterol by a Chrysophyte alga. J. Org. Chem. 49, 3742–3752 doi:10.1021/jo00194a014
    OpenUrlCrossRefWeb of Science
    1. Giner, J.-L.,
    2. Li, X. and
    3. Boyer, G.L.
    (2001) Sterol composition of Aureoumbra lagunensis, the Texas brown tide alga. Phytochemistry 57, 787–789 doi:10.1016/S0031-9422(01)00135-2
    OpenUrlCrossRefPubMedWeb of Science
    1. Rohmer, M.,
    2. Kokke, W.,
    3. Fenical, W. and
    4. Djerassi, C.
    (1980) Isolation of two new C30 sterols, (24E)-24-N-propylidenecholesterol and 24ξ-N-propylcholesterol, from a cultured marine chrysophyte. Steroids 35, 219–231 doi:10.1016/0039-128X(80)90104-X
    OpenUrlCrossRefPubMedWeb of Science
    1. Raederstorff, D. and
    2. Rohmer, M.
    (1984) Sterols of the unicellular algae Nematochrysopsis roscoffensis and Chrysotila lamellosa: isolation of (24E)-24-n-propylidenecholesterol and 24-n-propylcholesterol. Phytochemistry 23, 2835–2838 doi:10.1016/0031-9422(84)83024-1
    OpenUrlCrossRefWeb of Science
    1. Giner, J.-L. and
    2. Boyer, G.L.
    (1998) Sterols of the brown tide alga Aureococcus anophagefferens. Phytochemistry 48, 475–477 doi:10.1016/S0031-9422(97)00860-1
    OpenUrlCrossRef
  54. ↵
    1. Giner, J.-L.,
    2. Zhao, H.,
    3. Boyer, G.L.,
    4. Satchwell, M.F. and
    5. Andersen, R.A.
    (2009) Sterol chemotaxonomy of marine pelagophyte algae. Chem. Biodivers. 6, 1111–1130 doi:10.1002/cbdv.200800316
    OpenUrlCrossRefPubMed
  55. ↵
    1. Bouvier-Navé, P.,
    2. Husselstein, T. and
    3. Benveniste, P.
    (1998) Two families of sterol methyltransferases are involved in the first and the second methylation steps of plant sterol biosynthesis. FEBS J. 256, 88–96 PMID:9746350
    OpenUrlPubMedWeb of Science
  56. ↵
    1. Gold, D.A.,
    2. Grabenstatter, J.,
    3. de Mendoza, A.,
    4. Riesgo, A.,
    5. Ruiz-Trillo, I. and
    6. Summons, R.E.
    (2016) Sterol and genomic analyses validate the sponge biomarker hypothesis. Proc. Natl Acad. Sci. U.S.A. 113, 2684–2689 doi:10.1073/pnas.1512614113
    OpenUrlAbstract/FREE Full Text
  57. ↵
    1. Desmond, E. and
    2. Gribaldo, S.
    (2009) Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature. Genome Biol. Evol. 1, 364–381 doi:10.1093/gbe/evp036
    OpenUrlCrossRefPubMedWeb of Science
  58. ↵
    1. Volkman, J.
    (2003) Sterols in microorganisms. Appl. Microbiol. Biotechnol. 60, 495–506 doi:10.1007/s00253-002-1172-8
    OpenUrlCrossRefPubMedWeb of Science
  59. ↵
    1. Knoll, A.H.,
    2. Summons, R.E.,
    3. Waldbauer, J.R. and
    4. Zumberge, J. E.
    (2007) The geological succession of primary producers in the oceans. In Evolution of Primary Producers in the Sea, pp. 133–163, Elsevier
  60. ↵
    1. Gold, D.A.,
    2. O'reilly, S.S.,
    3. Watson, J.,
    4. Degnan, B.M.,
    5. Degnan, S.M.,
    6. Krömer, J.O.
    (2017) Lipidomics of the sea sponge Amphimedon queenslandica and implication for biomarker geochemistry. Geobiology 15, 836–843 doi:10.1111/gbi.12253
    OpenUrlCrossRef
  61. ↵
    1. Gold, D.A.,
    2. O'Reilly, S.S.,
    3. Luo, G.,
    4. Briggs, D.E.G. and
    5. Summons, R.E.
    (2016) Prospects for sterane preservation in sponge fossils from museum collections and the utility of sponge biomarkers for molecular clocks. Bull. Peabody Mus. Nat. Hist. 57, 181–189 doi:10.3374/014.057.0208
    OpenUrlCrossRef
  62. ↵
    1. Weete, J.D.,
    2. Abril, M. and
    3. Blackwell, M.
    (2010) Phylogenetic distribution of fungal sterols. PLoS ONE 5, e10899 doi:10.1371/journal.pone.0010899
    OpenUrlCrossRefPubMed
  63. ↵
    1. Méjanelle, L.,
    2. Sanchez-Gargallo, A.,
    3. Bentaleb, I. and
    4. Grimalt, J.O.
    (2003) Long chain n-alkyl diols, hydroxy ketones and sterols in a marine eustigmatophyte, Nannochloropsis gaditana, and in Brachionus plicatilis feeding on the algae. Org. Geochem. 34, 527–538 doi:10.1016/S0146-6380(02)00246-2
    OpenUrlCrossRefGeoRef
  64. ↵
    1. Bhattacharya, D. and
    2. Medlin, L.K.
    (2004) Dating algal origin using molecular clock methods. Protist 155, 9–10.
    OpenUrl
  65. ↵
    1. Yang, E.C.,
    2. Boo, S.M.,
    3. Bhattacharya, D.,
    4. Saunders, G.W.,
    5. Knoll, A.H.,
    6. Fredericq, S.
    (2016) Divergence time estimates and the evolution of major lineages in the florideophyte red algae. Sci. Rep. 6, 21361 doi:10.1038/srep21361
    OpenUrlCrossRef
  66. ↵
    1. Johnston, D.T.,
    2. Poulton, S.W.,
    3. Dehler, C.,
    4. Porter, S.,
    5. Husson, J.,
    6. Canfield, D.E.
    (2010) An emerging picture of Neoproterozoic ocean chemistry: insights from the Chuar Group, Grand Canyon, USA. Earth Planet. Sci. Lett. 290, 64–73 doi:10.1016/j.epsl.2009.11.059
    OpenUrlCrossRefGeoRefWeb of Science
  67. ↵
    1. dos Reis, M.,
    2. Thawornwattana, Y.,
    3. Angelis, K.,
    4. Telford, M.J.,
    5. Donoghue, P.C.J. and
    6. Yang, Z.
    (2015) Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales. Curr. Biol. 25, 2939–2950 doi:10.1016/j.cub.2015.09.066
    OpenUrlCrossRefPubMed
  68. ↵
    1. Jensen, S.,
    2. Droser, M.L. and
    3. Gehling, J.G.
    (2006) A critical look at the Ediacaran trace fossil record. In Neoproterozoic Geobiology and Paleobiology, pp. 115–157, Springer
    1. Gold, D.A.,
    2. Runnegar, B.,
    3. Gehling, J.G. and
    4. Jacobs, D.K.
    (2015) Ancestral state reconstruction of ontogeny supports a bilaterian affinity for Dickinsonia. Evol. Dev. 17, 315–324 doi:10.1111/ede.12168
    OpenUrlCrossRef
    1. Fedonkin, M.A. and
    2. Waggoner, B.M.
    (1997) The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism. Nature 388, 868–871 doi:10.1038/42242
    OpenUrlCrossRefGeoRefWeb of Science
  71. ↵
    1. Droser, M.L.,
    2. Tarhan, L.G. and
    3. Gehling, J.G.
    (2017) The rise of animals in a changing environment: global ecological innovation in the late Ediacaran. Annu. Rev. Earth Planet. Sci. 45, 593–617 doi:10.1146/annurev-earth-063016-015645
    OpenUrlCrossRef
View Abstract
Back to top

 

Forthcoming Topics

Actions

Email
The slow rise of complex life as revealed through biomarker genetics
David A. Gold
Emerging Topics in Life Sciences Aug 2018, ETLS20170150; DOI: 10.1042/ETLS20170150
del.icio.us logo Digg logo Reddit logo Technorati logo Twitter logo CiteULike logo Facebook logo Mendeley logo
Citation Tools
Print
Alerts
Request Permissions
Save to my folders

View Full PDF

Jump To

Keywords

biomarkers
eukaryotes
evolutionary biology
sterols

Related Articles

Cited By...