Identification of 24-n-propylidenecholesterol in a member of the Foraminifera

Grabenstatter, Jonathan Dean; Méhay, Sabine; McIntyre-Wressnig, Anna; Giner, José‐Luis; Edgcomb, Virginia P.; Beaudoin, David J.; Bernhard, Joan M.; Summons, Roger E.

doi:10.1016/j.orggeochem.2013.08.010

Cited by 21 publications

(9 citation statements)

References 44 publications

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“…27 and this study) calcisponges (refs 2,28 and this study) homoscleromorphs (this study) and unicellular animal outgroups 13 . Indeed, only steroids possessing conventional side chains (with methyl, ethyl or propyl groups or a hydrogen substituent at C-24) have been reported for other sponge classes, heterotrophic protists and these unicellular animal outgroups 13,14,27,28 , but not steroids with unconventional side chains of any variety. Thus, the finding of 26-mes, together with the 24-ipc steranes in Neoproterozoic rocks and oils, is most parsimoniously explained by an origin from demosponges living in marine settings.…”

Section: Resultsmentioning

confidence: 99%

Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals

et al. 2018

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he transition from unicellular protists to multicellular animals constitutes one of the most intriguing and enigmatic events in the evolutionary history of life, largely due to the absence of unambiguous physical fossils for the earliest fauna. The Neoproterozoic rise of eukaryotes 1 , including demosponges 2 , in marine environments can be discerned from lipid biomarker records preserved in ancient sedimentary rocks that have experienced a mild thermal history. Molecular phylogenies commonly show that sponges (Porifera) are the sister group of other animals 3 and molecular evidence for Neoproterozoic animal life was first proposed based on the occurrence of unusual C 30 demosponge-derived steranes informally known as 24-isopropylcholestane (24-ipc) steranes in sedimentary rocks and oils of that age 2,4. These steranes are the hydrocarbon remains of 24-isopropylcholesterols and structurally related sterols 5. The record of 24-ipc steranes commences in Cryogenian-aged sediments in South Oman (around 717-635 million years ago (Ma) 2,6) and then occurs continuously through the Ediacaran-Cambrian formations of the Huqf Supergroup of the South Oman Salt Basin. Notably, these steroids also occur as covalently bound constituents fixed within the immobile kerogen phase of the same rocks, which is an important confirmation that these are not younger contaminant compounds that migrated into the rocks 2. Demosponges are the only known extant taxon that can biosynthesize 24-ipc precursors as their major sterols. High relative absolute abundances of 24-ipc steranes have now been reported in many other late Neoproterozoic-early Cambrian rocks and oils 2,4,7-9. These 24-ipc occurrences-if interpreted correctly-reflect an early presence of Porifera and provide a conservative minimum time estimate for the origin of animal multicellularity and the sponge body plan. Others have hypothesized that the 24-ipc steranes could be derived from unicellular animal ancestors or have an algal origin 10 since the parent sterols have been reported in trace amounts in some extant pelagophyte algae 2. The claim that poribacterial sponge symbionts from the candidate phylum Poribacteria can make 24-ipc steroids 11 has since been shown to be erroneous due to a genome assembly error 12,13. Currently, two chromatographically resolvable series of ancient C 30 steranes are known: 24-n-propylcholestane (24-npc) and 24-ipc. Demosponges are the most plausible Neoproterozoic-Cambrian source of 24-npc as well as 24-ipc because both are produced by extant demosponges 2. Foraminifera are another possible source of 24-npc 14. Pelagophyte algae probably account for the 24-npc steranes that are found in Devonian and younger marine sediments and their derived oils 13. Various recent findings support a pre-Ediacaran origin of animals and sponges, and arguably reinforce the validity of the 24-ipc biomarker record, including: (1) steroid assays and genomic analyses of extant taxa 13 , which suggest that sponges were the most likely Neoproterozoic source biota for 24-...

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Section: Resultsmentioning

confidence: 99%

Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals

et al. 2018

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“…Five-fraction column chromatography on SiO 2 was used to separate the sterols from other cellular lipids, which were derivatized to form trimethylysilyl ethers. GC-MS analyses were carried out on an Agilent GC-MSD 5975C equipped with a programmable temperature vaporizing injector (36). For comparative genomic analyses, proteomes were queried using candidate sequences (provided in Dataset S1) using BLASTp, with a P value cutoff of 10e-5.…”

Section: Methodsmentioning

confidence: 99%

Sterol and genomic analyses validate the sponge biomarker hypothesis

Gold

Grabenstatter

Mendoza

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Molecular fossils (or biomarkers) are key to unraveling the deep history of eukaryotes, especially in the absence of traditional fossils. In this regard, the sterane 24-isopropylcholestane has been proposed as a molecular fossil for sponges, and could represent the oldest evidence for animal life. The sterane is found in rocks ∼650-540 million y old, and its sterol precursor (24-isopropylcholesterol, or 24-ipc) is synthesized today by certain sea sponges. However, 24-ipc is also produced in trace amounts by distantly related pelagophyte algae, whereas only a few close relatives of sponges have been assayed for sterols. In this study, we analyzed the sterol and gene repertoires of four taxa (Salpingoeca rosetta, Capsaspora owczarzaki, Sphaeroforma arctica, and Creolimax fragrantissima), which collectively represent the major living animal outgroups. We discovered that all four taxa lack C 30 sterols, including 24-ipc. By building phylogenetic trees for key enzymes in 24-ipc biosynthesis, we identified a candidate gene (carbon-24/28 sterol methyltransferase, or SMT) responsible for 24-ipc production. Our results suggest that pelagophytes and sponges independently evolved C 30 sterol biosynthesis through clade-specific SMT duplications. Using a molecular clock approach, we demonstrate that the relevant sponge SMT duplication event overlapped with the appearance of 24-isopropylcholestanes in the Neoproterozoic, but that the algal SMT duplication event occurred later in the Phanerozoic. Subsequently, pelagophyte algae and their relatives are an unlikely alternative to sponges as a source of Neoproterozoic 24-isopropylcholestanes, consistent with growing evidence that sponges evolved long before the Cambrian explosion ∼542 million y ago.sponges | Porifera | sterols | steranes | Amorphea

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“…C 28 steroids (preserved as 24-methylcholestanes) are important in higher order endosymbiotic red algal lineages that were not dominant or diverse until late Mesozoic time and younger (Grantham and Wakefield, 1988), including haptophytes and diatoms, but also in some prasinophytes from the green lineage (Kodner et al, 2008;Volkman, 2003). The C 30 steranes, 24-n-propylcholestanes are mainly derived from sterol precursors produced by the exclusively marine algal class Pelagophyceae, although these have also been reported as minor constituents of foraminifera (Giner et al, 2009;Grabenstatter et al, 2013).…”

Section: Organic Geochemistrymentioning

confidence: 99%

Empirical links between trace metal cycling and marine microbial ecology during a large perturbation to Earth's carbon cycle

Owens

Reinhard

Rohrssen

et al. 2016

Earth and Planetary Science Letters

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Available online xxxx Editor: D. Vance Keywords: oceanic anoxic event (OAE2) trace metal drawdown geochemistry anoxia euxinia biomarkersUnderstanding the global redox state of the oceans and its cause-and-effect relationship with periods of widespread organic-carbon deposition is vital to interpretations of Earth's climatic and biotic feedbacks during periods of expanded oceanic oxygen deficiency. Here, we present a compilation of new and published data from an organic-rich locality within the proto-North Atlantic Ocean during the Cenomanian-Turonian boundary event that shows a dramatic drawdown of redox-sensitive trace elements. Iron geochemistry independently suggests euxinic deposition (i.e., anoxic and sulfidic bottom waters) for the entire section, thus confirming its potential as an archive of global marine metal inventories. In particular, depleted molybdenum (Mo) and vanadium (V) concentrations effectively record the global expansion of euxinic and oxygen-deficient but non-sulfidic waters, respectively. The V drawdown precedes the OAE, fingerprinting an expansion of oxygen deficiency prior to an expansion of euxinia. Molybdenum drawdown, in contrast, is delayed with respect to V and coincides with the onset of OAE2. Parallel lipid biomarker analyses provide evidence for significant and progressive reorganization of marine microbial ecology during the OAE in this region of the proto-North Atlantic, with the smallest relative eukaryotic contributions to total primary production occurring during metal-depleted intervals. This relationship may be related to decreasing supplies of enzymatically important trace elements. Similarly, box modeling suggests that oceanic drawdown of Mo may have approached levels capable of affecting marine nitrogen fixation. Predictions of possible nitrogen stress on eukaryotic production, locally and globally, are consistent with the low observed levels of Mo and a rise in 2-methylhopane index values during the peak of the OAE. At the same time, the environmental challenge presented by low dissolved oxygen and euxinia coincides with increased turnover rates of radiolarian clades, calcareous nanofossils, and foraminifera, suggesting that the temporal patterns of anoxia/euxinia and associated nutrient limitation may have contributed to the fabric of OAE2-related turnover.

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Identification of 24-n-propylidenecholesterol in a member of the Foraminifera

Cited by 21 publications

References 44 publications

Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals

Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals

Sterol and genomic analyses validate the sponge biomarker hypothesis

Empirical links between trace metal cycling and marine microbial ecology during a large perturbation to Earth's carbon cycle

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