Cryogenian evolution of stigmasteroid biosynthesis

Abstract

Sedimentary hydrocarbon remnants of eukaryotic C₂₆-C₃₀ sterols can be used to reconstruct early algal evolution. Enhanced C₂₉ sterol abundances provide algal cell membranes a density advantage in large temperature fluctuations. Here, we combined a literature review with new analyses to generate a comprehensive inventory of unambiguously syngenetic steranes in Neoproterozoic rocks. Our results show that the capacity for C₂₉ 24-ethyl-sterol biosynthesis emerged in the Cryogenian, that is, between 720 and 635 million years ago during the Neoproterozoic Snowball Earth glaciations, which were an evolutionary stimulant, not a bottleneck. This biochemical innovation heralded the rise of green algae to global dominance of marine ecosystems and highlights the environmental drivers for the evolution of sterol biosynthesis. The Cryogenian emergence of C₂₉ sterol biosynthesis places a benchmark for verifying older sterane signatures and sets a new framework for our understanding of early algal evolution.

Fig. 1. Evolutionary radiation of stigmasteroid (24) biosynthesis.

(A) Tonian rocks are nearly exclusively characterized by C₂₇ steranes [cholestane; see (F): Green symbols denote C₂₇ dominance and complete absence of C₂₉ steranes, with only sporadic traces of C₂₈ 4-desmethylsteranes]. (B) The oldest noncontaminated C₂₉ 24-ethylsteranes [stigmastane; see (F): yellow symbols stand for C₂₇ > C₂₉, whereas red symbols indicate C₂₇ < C₂₉ and often C₂₇ ≪ C₂₉] only appear during the latest Cryogenian (Marinoan deglaciation) and earliest Ediacaran in Oman, whereas contemporaneous rocks from three other localities are still strongly or exclusively dominated by C₂₇ steranes, indicating a 720- to 635-Ma Snowball Earth glacial origin of the stigmasteroid biosynthetic pathway—in agreement with the physiological membrane density advantage yielded by cellular phytosterols (19, 20) and molecular clocks (30). (C and D) Global dominance of C₂₉ steroid biosynthesis by 600 Ma (table S1) highlights the evolutionary advantage of the likely chlorophyte host organism and a rapid rise to ecological dominance. (E) Schematic representation of Neoproterozoic time showing steroidal dominance (green, C₂₇ versus red, C₂₉) and the time brackets from (A) to (D). (F) Relevant molecular structures and schematic tandem-MS chromatograms of (bottom to top) C₂₇ [green, mass/charge ratio (m/z) 372 to 217], C₂₈ (yellow, m/z 386 to 217), and C₂₉ (red, m/z 400 to 217) steranes, emphasizing the color code used in (A) to (D). Ages on the top right of the maps comply with the palaeogeographic snapshots after (31).