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1.1-Billion-Year-Old Porphyrins Establish a Marine Ecosystem Dominated by Bacterial Primary Producers

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1.1-Billion-Year-Old Porphyrins Establish a Marine Ecosystem Dominated by Bacterial Primary Producers 1.1-billion-year-old porphyrins establish a marine ecosystem dominated by bacterial primary producers N. Guenelia,1, A. M. McKennab, N. Ohkouchic, C. J. Borehamd, J. Beghine, E. J. Javauxe, and J. J. Brocksa,1 aResearch School of Earth Sciences, Australian National University, Canberra, ACT 2601, Australia; bNational High Magnetic Field Laboratory, Florida State University, Tallahassee, FL 32310-4005; cDepartment of Biogeochemistry, Japan Agency for Marine–Earth Science and Technology, 237-0061 Kanagawa Prefecture, Yokosuka, Natsushimacho, Japan; dGeoscience Australia, Symonston, ACT 2609, Australia; and eDepartment of Geology, Unité de Recherche Geology, University of Liège, 4000 Liege, Belgium Edited by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved June 8, 2018 (received for review March 6, 2018) The average cell size of marine phytoplankton is critical for the the molecular fossils of biological lipids, can provide comple- flow of energy and nutrients from the base of the food web to mentary information about primary producers. For example, higher trophic levels. Thus, the evolutionary succession of primary hydrocarbon fossils of carotenoid pigments extracted from sed- producers through Earth’s history is important for our understand- imentary rocks have been used to detect phototrophic green ing of the radiation of modern protists ∼800 million years ago and (Chlorobiaceae) and purple sulfur bacteria (PSB) (Chromatia- ∼ the emergence of eumetazoan animals 200 million years later. ceae) in 1,640-My-old marine ecosystems (4, 5), while the con- Currently, it is difficult to establish connections between primary centration of eukaryotic steranes, relative to bacterial hopanes, production and the proliferation of large and complex organisms may provide basic information about the ecological relevance of because the mid-Proterozoic (∼1,800–800 million years ago) rock Precambrian algae (6). The relative abundance as well as di- record is nearly devoid of recognizable phytoplankton fossils. We report the discovery of intact porphyrins, the molecular fossils of versity of steranes dramatically increased in the brief interlude chlorophylls, from 1,100-million-year-old marine black shales of between the Sturtian and Marinoan snowball Earth glaciations of – the Taoudeni Basin (Mauritania), 600 million years older than pre- 659 645 Ma, heralding the rise of planktonic algae as important 15 primary producers in the oceans (Fig. 1A). Steranes in the time vious findings. The porphyrin nitrogen isotopes (δ Npor = 5.6– 10.2‰) are heavier than in younger sedimentary sequences, and interval 645 to ∼500 Ma have a strong predominance of stigmastane the isotopic offset between sedimentary bulk nitrogen and por- (a structure with 29 carbon atoms, C29), revealing Chlorophyta, a EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES phyrins (epor = −5.1 to −0.5‰) points to cyanobacteria as domi- division of green algae, as dominant primary producers from the nant primary producers. Based on fossil carotenoids, anoxygenic late Cryogenian to early Paleozoic (Fig. 1) (7, 8). green (Chlorobiacea) and purple sulfur bacteria (Chromatiaceae) Preceding the Cryogenian rise of planktonic algae, the oldest e also contributed to photosynthate. The low por values, in combi- clearly indigenous eukaryotic steranes appear in the geological nation with a lack of diagnostic eukaryotic steranes in the time record ∼900–800 Ma, albeit in low concentrations relative to interval of 1,600–1,000 million years ago, demonstrate that algae bacterial biomarkers (7, 8). These Tonian (1,000–720 Ma) ster- EVOLUTION played an insignificant role in mid-Proterozoic oceans. The paucity anes display a primordial distribution with a nearly 100% pre- of algae and the small cell size of bacterial phytoplankton may dominance of cholestane (C27, red circles in Fig. 1A), which may have curtailed the flow of energy to higher trophic levels, poten- be related to the activity of rhodophytes (9) or heterotrophic tially contributing to a diminished evolutionary pace toward com- eukaryotes (8). plex eukaryotic ecosystems and large and active organisms. chlorophyll | Taoudeni Basin | Mesoproterozoic | compound-specific Significance nitrogen isotopes | primary producers The oceans of Earth’s middle age, 1.8–0.8 billion years ago, were devoid of animal-like life. According to one hypothesis, he succession of primary producers in the oceans shaped the emergence of large, active organisms was restrained by the marine ecology through Earth’s history (1). Primary pro- T limited supply of large food particles such as algae. Through ducers form the base of the food web. Their cell size, elemental the discovery of molecular fossils of the photopigment chlo- stoichiometry, and cell density influence the flow of energy and rophyll in 1.1-billion-year-old marine sedimentary rocks, we nutrients to higher trophic levels (2), presumably setting limits were able to quantify the abundance of different phototrophs. for ecosystem complexity. The composition of phytoplankton The nitrogen isotopic values of the fossil pigments showed communities in Earth’s early oceans, including anoxygenic and that the oceans were dominated by cyanobacteria, while larger oxygenic phototrophic bacteria and eukaryotic algae, may thus planktonic algae were scarce. This supports the hypothesis that have set the pace for the emergence and radiation of different small cells at the base of the food chain limited the flow groups of filter feeders, grazers, and predators, including the of energy to higher trophic levels, potentially retarding the proliferation of modern protists ∼800 Ma and the appearance of emergence of large and complex life. eumetazoan animals some 200 My later (1) (Fig. 1B). Based on the fossil record, chlorophyll c (Chl c) algae, in- Author contributions: N.G. and J.J.B. designed research; N.G., A.M.M., N.O., C.J.B., and cluding dinoflagellates, coccolithophorids, and diatoms, were the J.J.B. performed research; A.M.M., N.O., and C.J.B. contributed new reagents/analytic major energy and carbon source in the oceans of the past ∼250 tools; N.G., A.M.M., N.O., C.J.B., and J.J.B. analyzed data; and N.G., A.M.M., N.O., J.B., My (Fig. 1B). By contrast, Paleozoic (541–251 Ma) and Edia- E.J.J., and J.J.B. wrote the paper. caran (635–541 Ma) oceans were presumably dominated by The authors declare no conflict of interest. primary endosymbiotic algae (Archaeplastida), encompassing This article is a PNAS Direct Submission. the red (Rhodophyta) and green algae (Chlorophyta) (1). Published under the PNAS license. Deeper yet in time, reconstructing the succession of primary 1To whom correspondence may be addressed. Email: [email protected] or jochen. producers becomes challenging. Phytoplankton without a pre- [email protected]. servable cuticle or skeleton are rarely preserved in the body fossil This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. record, and there are no uncontentious fossils of planktonic 1073/pnas.1803866115/-/DCSupplemental. bacteria or algae in the pre-Ediacaran (3). However, biomarkers, www.pnas.org/cgi/doi/10.1073/pnas.1803866115 PNAS Latest Articles | 1of9 Downloaded by guest on September 24, 2021 A Sterane/hopane ratio B First occurrences (FT-ICR MS), we identify geoporphyrins in 1,100-My-old black 0 2 4 shales. Porphyrins are the molecular fossils of (bacterio)chloro- 0.00 C phylls. Their nitrogen isotopic composition can provide quanti- tative information about dominant phototrophs in past ecosystems (15). Some groups of phototrophs possess a characteristic offset M (epor) between the nitrogen isotopic composition of the whole cell and chlorophylls, independent of the nitrogen source (15), and c Radiation of Chl algae under suitable conditions this isotopic offset is largely unaffected by degradation processes in the water column and bottom sediments P (16). Therefore, the nitrogen isotopic composition of porphyrins in sediments and sedimentary rocks may preserve information about Phanerozoic primary producers present in an ancient environment, largely in- Cambrian Explosion 0.54 Ediacara biota, filter feeders, dependent of physical and chemical conditions such as food source Ed motile animals and diagenesis. 0.63 Radiation of macroalgae Cr Rise of planktonic algae Depositional Environment 0.72 Sturtian glaciation Amoebozoans, rhizarians, Eleven black shales studied for their molecular content (Table 1 predation marks and SI Appendix, Table S1) come from the En Nesoar and Tn first steranes Touirist formations of the 1,100 Ma El Mreïti Group (17) de- Neoprot. posited on an epicratonic platform of the Taoudeni Basin on the cholestane West African Craton (18). The black shales, with a carbon 1.00 no steranes content of up to 32%, accumulated beneath anoxic ferruginous Benthic rhodophytes and occasionally sulfidic waters (19) during maximal flooding of the craton in a quiet subwave base environment possibly pro- tected by offshore stromatolite reefs (18). The black shales contain micrometer-thin laminae of organic matter and pyritized filamentous sheaths that are interpreted as benthic microbial Cyanobacterial porphyrins communities, presumably of heterotrophic and/or chemosyn- Meso- thetic microorganisms thriving beneath anoxic waters (19), and irregularly shaped, discrete or bedding-parallel accumulations of organic particles typical of planktonic debris (SI Appendix, SI Geology and Samples). Oldest eukaryotic fossils 1.60 Results Chromatiaceae Chlorobiacea
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