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Niche Expansion for Phototrophic Sulfur Bacteria at the Proterozoic–Phanerozoic Transition

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Niche Expansion for Phototrophic Sulfur Bacteria at the Proterozoic–Phanerozoic Transition Niche expansion for phototrophic sulfur bacteria at the Proterozoic–Phanerozoic transition Xingqian Cuia,b,1, Xiao-Lei Liuc, Gaozhong Shend, Jian Maa, Fatima Husaina, Donald Rochere, John E. Zumbergee, Donald A. Bryantd,f, and Roger E. Summonsa,1 aDepartment of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139; bSchool of Oceanography, Shanghai Jiao Tong University, 200030 Shanghai, China; cSchool of Geosciences, University of Oklahoma, Norman, OK 73019; dDepartment of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802; eGeoMark Research, Ltd., Houston, TX 77095; and fDepartment of Chemistry and Biochemistry, Montana State University, Bozeman, MT 59717 Edited by Donald E. Canfield, Institute of Biology and Nordic Center for Earth Evolution, University of Southern Denmark, Odense M., Denmark, and approved June 9, 2020 (received for review April 5, 2020) Fossilized carotenoid hydrocarbons provide a window into the green sulfur bacteria (GSB; Chlorobiaceae) and purple sulfur physiology and biochemistry of ancient microbial phototrophic bacteria (PSB; Chromatiaceae), these microbes serve as impor- communities for which only a sparse and incomplete fossil record tant sources of primary carbon fixation in environments with exists. However, accurate interpretation of carotenoid-derived restricted water circulation, such as fjords, stratified seas, and biomarkers requires detailed knowledge of the carotenoid inven- saline lakes (5). They can also be productive constituents of tories of contemporary phototrophs and their physiologies. Here microbial mats (6). Their presence in ancient environments is we report two distinct patterns of fossilized C40 diaromatic carot- commonly recorded by distinct pigment-derived hydrocarbons enoids. Phanerozoic marine settings show distributions of diaro- preserved in sedimentary rocks and oils, typically where sedi- matic hydrocarbons dominated by isorenieratane, a biomarker ments were laid down in hypersaline lagoons, in narrow re- derived from low-light-adapted phototrophic green sulfur bacte- stricted seaways, and more widely during oceanic anoxic events ria. In contrast, isorenieratane is only a minor constituent within (7–10). The oldest reported fossil carotenoids attributed to the Neoproterozoic marine sediments and Phanerozoic lacustrine pale- GSB are from the Paleoproterozoic (1.65 Ga) Barney Creek oenvironments, for which the major compounds detected are Formation (BCF) of northern Australia (11). renierapurpurane and renieratane, together with some novel C39 Besides light, the other significant control on the ubiquity and EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES and C38 carotenoid degradation products. This latter pattern can productivity of GSB and PSB is sulfide availability, which, in be traced to cyanobacteria as shown by analyses of cultured taxa turn, has fluctuated with the inventories of sulfur species on and laboratory simulations of sedimentary diagenesis. The cyano- Earth’s surface over time. Marine sulfate reservoirs apparently bacterial carotenoid synechoxanthin, and its immediate biosyn- remained low through the Archean Eon and for most of the thetic precursors, contain thermally labile, aromatic carboxylic-acid functional groups, which upon hydrogenation and mild heating Proterozoic Eon (12). However, it is generally agreed that a yield mixtures of products that closely resemble those found in substantial increase in marine sulfate concentrations occurred the Proterozoic fossil record. The Neoproterozoic–Phanerozoic late in the Neoproterozoic coeval with a spurt in ocean transition in fossil carotenoid patterns likely reflects a step change in the surface sulfur inventory that afforded opportunities for the Significance expansion of phototropic sulfur bacteria in marine ecosystems. Furthermore, this expansion might have also coincided with a major Carotenoid pigments afford valuable clues about the chemistry change in physiology. One possibility is that the green sulfur bacteria and biology of both modern and ancient aquatic environments. developed the capacity to oxidize sulfide fully to sulfate, an in- This study reveals that fossil aromatic carotenoids—long con- novation which would have significantly increased their capacity sidered biomarkers for anoxygenic, phototrophic sulfur bacte- for photosynthetic carbon fixation. ria and their physiological requirement for hydrogen sulfide and illumination—can also be biosynthesized by oxygen-producing carotenoids | Neoproterozoic Era | phototrophic sulfur bacteria | cyanobacteria. Cyanobacterial aromatic carotenoids, which are cyanobacteria | photic zone euxinia distinct in their chemical structures and occurrence patterns, are the most commonly encountered compounds in Proterozoic ma- he transition from the Proterozoic to the Phanerozoic Eon rine settings as well as in lakes from more recent eras. In contrast, Twas a pivotal time in Earth’s history: The explosion in bi- carotenoids diagnostic for green sulfur bacteria of the family ological diversity is recorded in sedimentary rocks by a stunning Chlorobiaceae became both prevalent and abundant in marine array of microscopic and macroscopic fossils. During this up- paleoenvironments beginning in the Phanerozoic Eon. This ex- heaval, the biogeochemical cycles of carbon, sulfur, nitrogen, and pansion occurs as marine sulfate inventories increased toward the phosphorous underwent significant reorganizations as recorded end of the Proterozoic Eon. by mineral assemblages, redox-sensitive element abundances, and stable isotopic proxies that point to progressive oxygenation Author contributions: X.C. and R.E.S. designed research; X.C., X.-L.L., G.S., J.M., F.H., and – ’ R.E.S. performed research; D.R. and J.E.Z. contributed new reagents/analytic tools; X.C., of the ocean atmosphere system (1, 2). However, much of life s X.-L.L., D.A.B., and R.E.S. analyzed data; and X.C., X.-L.L., G.S., F.H., D.A.B., and R.E.S. biological diversity is only recorded molecularly, that is, in the wrote the paper. nucleic acids of extant organisms and in fossil molecules pre- The authors declare no competing interest. served in sediments and petroleum (3). Phototrophic bacteria, This article is a PNAS Direct Submission. including cyanobacteria, as drivers of planetary oxygenation are This open access article is distributed under Creative Commons Attribution-NonCommercial- particularly important as biogeochemical agents and yet their NoDerivatives License 4.0 (CC BY-NC-ND). fossil record is notably obscure. 1To whom correspondence may be addressed. Email: [email protected] or The phototrophic sulfur bacteria, ubiquitous microbes that [email protected]. populate illuminated aquatic environments where oxygen is ab- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ sent or in trace concentrations (4), are noted for having partic- doi:10.1073/pnas.2006379117/-/DCSupplemental. ularly distinctive and long-lasting molecular fossils. Comprised of First published July 9, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2006379117 PNAS | July 28, 2020 | vol. 117 | no. 30 | 17599–17606 Downloaded by guest on September 26, 2021 oxygenation (12–14). Isotopic studies suggest that the Phanero- primary producers. These biomarkers, although representative of zoic oceans also experienced substantial fluctuations in sulfate a much smaller pool of chemical diversity after diagenetic and levels (15–18), with estimates of concentrations that vary be- catagenetic alteration, still preserve a highly detailed picture of tween ∼5 and ∼30 mM, while the modern ocean concentration precursor carotenoids and chlorophylls. The simultaneous re- stands at 28 mM. As a consequence, the spatial and secular quirement for sulfide as an electron donor and light to power distributions, as well as the primary productivity of phototrophic anoxygenic photosynthesis (4, 24) has resulted in the aromatic sulfur bacteria, must have been restricted in sulfide-limited carotenoids and their aryl isoprenoid derivatives being viewed as Neoproterozoic seas (19). The occurrence of photic zone euxi- not only biomarkers for the PSB and GSB but also for situations nia (PZE) during the Mesoproterozoic has so far only been where anoxic and sulfidic waters permanently or episodically reported in the BCF based on the detection of pigment-derived chemical fossils that were ascribed to phototrophic sulfur bac- protruded into the photic zone, that is, PZE (10, 20, 25). Aro- teria (20). While abundant evidence suggests the redox stratifi- matic carotenoids comprise 1-alkyl-2,3,4- trimethyl substituted χ – cation of Proterozoic sea water columns (21), direct pigment -rings, as typified by okenone (V) from the PSB (26 28), and evidence for PZE is confined to just a few reports (11, 22, 23). 1-alkyl-2,3,6-trimethyl-subsituted ϕ-rings as found in chlor- Chemical fossils derived from pigments, exemplified by ca- obactene (III) and isorenieratene (XIII) from GSB (29, 30). rotenoids and porphyrins, record the history of Earth’s aquatic Besides GSB and PSB, aromatic carotenoids, and the genes A B C D E F Fig. 1. Variation of diaromatic carotenoid-based proxies from Neoproterozoic to Cenozoic presented in geologic time and as histograms. (A) The ratio of (ren+rnp)/(paleo+iso) calculated based on analyses by GC-MS with dMRM acquisition of the diagnostic transition of 546→134 Da. (B) The sum of three C39 diaromatic carotenoid isomers (MRM
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