The rise of algae in Cryogenian oceans and the emergence of animals

Abstract

The transition from dominant bacterial to eukaryotic marine primary productivity was one of the most profound ecological revolutions in the Earth's history, reorganizing the distribution of carbon and nutrients in the water column and increasing energy flow to higher trophic levels. But the causes and geological timing of this transition, as well as possible links with rising atmospheric oxygen levels and the evolution of animals, remain obscure. Here we present a molecular fossil record of eukaryotic steroids demonstrating that bacteria were the only notable primary producers in the oceans before the Cryogenian period (720-635 million years ago). Increasing steroid diversity and abundance marks the rapid rise of marine planktonic algae (Archaeplastida) in the narrow time interval between the Sturtian and Marinoan 'snowball Earth' glaciations, 659-645 million years ago. We propose that the incumbency of cyanobacteria was broken by a surge of nutrients supplied by the Sturtian deglaciation. The 'Rise of Algae' created food webs with more efficient nutrient and energy transfers, driving ecosystems towards larger and increasingly complex organisms. This effect is recorded by the concomitant appearance of biomarkers for sponges and predatory rhizarians, and the subsequent radiation of eumetazoans in the Ediacaran period.

Animal origins and the Tonian Earth system

“…A recent survey of the organic biomarker record in the Neoproterozoic Era reveals that the oldest steranesderived from eukaryotic sterols -appear in the late Tonian Period, 820-720 Ma ( Figure 3D) [55]. The ratio of steranes to hopanes (interpreted to derive from bacterial bacteriohopanepolyols) during the Tonian was three orders of magnitude lower than values typical of the Phanerozoic Eon (541-0 Ma), suggesting a comparatively low abundance of eukaryotes relative to bacteria.…”

“…The ratio of steranes to hopanes (interpreted to derive from bacterial bacteriohopanepolyols) during the Tonian was three orders of magnitude lower than values typical of the Phanerozoic Eon (541-0 Ma), suggesting a comparatively low abundance of eukaryotes relative to bacteria. These late Tonian steranes are exclusively represented by cholestane (C 27 ), with the absence of ergostane (C 28 ) and stigmastane (C 29 ), and are thought to have been primarily sourced from heterotrophic eukaryotes, with a potential contribution from red algae [55]. These biomarker patterns are therefore consistent with a mid-to-late Tonian appearance (or at least the presence) of animals and florideophytes, as well as related red algal lineages [56] (Figure 3).…”

“…[45]; (C) chromium isotope record aggregated from multiple studies [51,52,54,[77][78][79]; (D) Sterane/hopane ratios from ref. [55] and (E) relative fractions of cholestane, ergostane, and stigmastane (C27, C28, and C29, respectively) from ref. [55].…”

“…[55] and (E) relative fractions of cholestane, ergostane, and stigmastane (C27, C28, and C29, respectively) from ref. [55]. and the ca.…”

“…Cryostane (26-methylocholestane), which is restricted to the late Tonian, is another potential demosponge biomarker, as demosponges represent the only known extant organisms capable of methylating sterols in the 26-position [55,59]. These two biomarkers, if indeed sourced from demosponges, are each consistent with a mid-Tonian origin of crown-group animals, suggesting that animals, including bilaterians, emerged when eukaryotes were relatively less abundant in marine ecosystems, before the shift to more modern sterane/hopane ratios and sterane diversity levels 659-645 Ma (Figure 3).…”