1.1-billion-year-old porphyrins establish a marine ecosystem dominated by bacterial primary producers

Abstract

The average cell size of marine phytoplankton is critical for the flow of energy and nutrients from the base of the food web to higher trophic levels. Thus, the evolutionary succession of primary producers through Earth's history is important for our understanding of the radiation of modern protists ∼800 million years ago and the emergence of eumetazoan animals ∼200 million years later. Currently, it is difficult to establish connections between primary production and the proliferation of large and complex organisms because the mid-Proterozoic (∼1,800-800 million years ago) rock record is nearly devoid of recognizable phytoplankton fossils. We report the discovery of intact porphyrins, the molecular fossils of chlorophylls, from 1,100-million-year-old marine black shales of the Taoudeni Basin (Mauritania), 600 million years older than previous findings. The porphyrin nitrogen isotopes (δ¹⁵N_por = 5.6-10.2‰) are heavier than in younger sedimentary sequences, and the isotopic offset between sedimentary bulk nitrogen and porphyrins (ε_por = -5.1 to -0.5‰) points to cyanobacteria as dominant primary producers. Based on fossil carotenoids, anoxygenic green (Chlorobiacea) and purple sulfur bacteria (Chromatiaceae) also contributed to photosynthate. The low ε_por values, in combination with a lack of diagnostic eukaryotic steranes in the time interval of 1,600-1,000 million years ago, demonstrate that algae played an insignificant role in mid-Proterozoic oceans. The paucity of algae and the small cell size of bacterial phytoplankton may have curtailed the flow of energy to higher trophic levels, potentially contributing to a diminished evolutionary pace toward complex eukaryotic ecosystems and large and active organisms.

Keywords: Mesoproterozoic; Taoudeni Basin; chlorophyll; compound-specific nitrogen isotopes; primary producers.

Fig. 1.

Temporal history of biomarker and fossil data. (A) Ratio of eukaryotic steranes over bacterial hopanes through time (details and references see text). Green circles, late Cryogenian to present data, including C₂₇ to C₂₉ steranes (cholestanes, ergostanes, and stigmastanes); red circles, Tonian to early Cryogenian steranes with a ∼100% cholestane predominance; and unfilled black circles, mid-Proterozoic biomarker assemblages, where hopanes are present but steranes are below detection limits. (B) First occurrences or radiations of organism groups and biomarkers (for data sources, see text). C, Cenozoic; Cr, Cryogenian; Ed, Ediacaran; M, Mesozoic; Neoprot., Neoproterozoic; P, Paleozoic; Tn, Tonian.

Fig. 2.

Selected biomarker classes identified in black shales (sample 08, drill core S2, 140.25 m) of the El Mreïti Group. (A) Summed GC-MS metastable reaction monitoring (MRM) chromatograms of M+ → 191 transitions of the saturated fraction. A complete homologous series of 17α(H),21β(H)-hopanes with 27–35 carbon atoms (black triangles) were identified. T_s = 18α(H)-22,29,30 trisnorneohopane, T_m = 17α(H)-22,29,30-trisnorhopane, and γ = gammacerane. (B) m/z 134 selected ion recording chromatogram of the aromatic fraction. Filled circles, 2,3,6-AI; open circles, 2,3,4-AI.

Fig. 3.

Structures of nickel and vanadyl-oxide porphyrins discussed in the text. M, Ni, or VO. DBE, double bond equivalents (i.e., number of rings plus double bonds).

Fig. 4.

Identification of Ni- and VO-porphyrins by FT-ICR MS. (A) Isoabundance-contoured plots of double-bond equivalents (DBEs) versus carbon number for the N₄⁵⁸Ni class (08-EOM and 13-Ni) and the N₄O₁V₁ class (13-VO). (B) DBE distributions for Ni- and VO-porphyrins in samples 08-EOM, 13-VO, and 13-Ni. Normalized abundances are reported for each sample. Note that M^+o and [M + H]⁺ ions can be distinguished by their integer versus half-integer calculated DBE values.

Fig. 5.

δ¹⁵N values of chlorophylls and porphyrin derivatives from Touirist Formation sample 13-Ni (pink stars), the water column and sediments of various modern water bodies, and Phanerozoic sediments. Lakes, freshwater lakes (compiled from refs. , , , and 75). BPhe, bacteriopheophytin; Phe, pheophytin; PPhe, pyropheophytin.

Fig. 6.

Whisker plot of a wide range of ε_por data (, , , –53). “This study” is Touirist Formation sample 13-Ni.