Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis Timothy M. Gibson1, Patrick M. Shih2,3, Vivien M. Cumming1, Woodward W. Fischer4, Peter W. Crockford1, Malcolm S.W. Hodgskiss1*, Sarah Wörndle1, Robert A. Creaser5, Robert H. Rainbird6, Thomas M. Skulski6, and Galen P. Halverson1 1Department of Earth and Planetary Sciences/GEOTOP, McGill University, Montréal, Quebec H3A 0E8, Canada 2Joint BioEnergy Institute, Emeryville, California 94608, USA 3Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA 4Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125, USA 5Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada 6Geological Survey of Canada, Ottawa, Ontario K1A 0E8, Canada ABSTRACT ornamentation characteristic of eukaryotes are Although the geological record indicates that eukaryotes evolved by 1.9–1.4 Ga, their 1.65–1.4 Ga sphaeromorphic acritarchs; i.e., Tap- early evolution is poorly resolved taxonomically and chronologically. The fossil red alga pania and Valeria (Javaux et al., 2001; Lamb et Bangiomorpha pubescens is the only recognized crown-group eukaryote older than ca. 0.8 al., 2009; Knoll, 2014; Adam et al., 2017). Ga and marks the earliest known expression of extant forms of multicellularity and eukary- Aside from B. pubescens, eukaryotic fos- otic photosynthesis. Because it postdates the divergence between the red and green algae sils remain taxonomically unresolvable until and the prior endosymbiotic event that gave rise to the chloroplast, B. pubescens is uniquely ca. 0.8 Ga (Knoll, 2014; Cohen and Macdon- important for calibrating eukaryotic evolution. However, molecular clock estimates for the ald, 2015). Accepting that the last eukaryotic divergence between the red and green algae are highly variable, and some analyses estimate common ancestor had evolved by 1.65 Ga, the this split to be younger than the widely inferred but poorly constrained first appearance age protracted early evolutionary history of stem of 1.2 Ga for B. pubescens. As a result, many molecular clock studies reject this fossil ex post group eukaryotes is poorly documented. While facto. Here we present new Re-Os isotopic ages from sedimentary rocks that stratigraphically B. pubescens was long presumed to arise 1.2 Ga bracket the occurrence of B. pubescens in the Bylot Supergroup of Baffin Island and revise (see the GSA Data Repository1), its true age its first appearance to 1.047 +0.013/–0.017 Ga. This date is 150 m.y. younger than commonly was only loosely constrained by conventional held interpretations and permits more precise estimates of early eukaryotic evolution. Using radiometric ages to a >500 m.y. interval. Here cross-calibrated molecular clock analyses with the new fossil age, we calculate that photosyn- we present two new Re-Os isochron ages that thesis within the Eukarya emerged ca. 1.25 Ga. This date for primary plastid endosymbiosis precisely date the first appearance ofB. pube- serves as a benchmark for interpreting the fossil record of early eukaryotes and evaluating scens in the Bylot Supergroup of Baffin Island. their role in the Proterozoic biosphere. This revised fossil age helps resolve inconsis- tencies between molecular clocks and fossil evi- INTRODUCTION al., 1990; Butterfield, 2000). Therefore, this fos- dence for early eukaryotic diversification (e.g., Photosynthetic eukaryotes (i.e., plants and sil is widely recognized as critical to calibrating Berney and Pawlowski, 2006; Cavalier-Smith et algae) are responsible for most global primary the tempo of early eukaryotic diversification and al., 2006; Parfrey et al., 2011; Eme et al., 2014) production, and their evolution and diversi- constraining the acquisition of photosynthesis and permits more precise calibration of primary fication set the stage for today’s thriving bio- within the domain. Because concrete evidence plastid endosymbiosis and the split between the sphere. However, the timing and tempo of early for such evolutionary milestones is scarce, the red and green algae. eukaryotic evolution are unclear (Berney and appearance of B. pubescens in the fossil record Pawlowski, 2006; Parfrey et al., 2011; Shih and presents a rare opportunity to anchor interpreta- GEOLOGICAL BACKGROUND Matzke, 2013). While the origins of the Eukarya tions regarding early eukaryotic evolution. B. pubescens was first described in chert are debated, it is clear they became photosyn- The timing for the origin of the Eukarya from peritidal carbonate facies of the Hunting thetic by engulfing a cyanobacterium in the pri- is unresolved, with estimates spanning >1 b.y. Formation on Somerset Island (Butterfield et al., mary endosymbiotic event that gave rise to the (Roger and Hug, 2006). Isolated stem group 1990) and later in similar facies in the correlative plastid, an organelle that houses photosynthetic eukaryotes may date as far back as ca. 3.2 Ga Angmaat Formation of the Bylot Supergroup machinery known as a chloroplast (Keeling, (Javaux et al., 2010), whereas more widely occur- on Baffin Island, both in northeastern Canada 2010). The fossil red alga Bangiomorpha pubes- ring fossils with possible eukaryotic affinities, (Knoll et al., 2013; Fig. 1). The Hunting and cens provides the earliest unambiguous record of such as Grypania, occur in 1.9–1.8 Ga rocks Angmaat Formations occur within comparable photosynthetic eukaryotic life and exhibits dis- (Han and Runnegar, 1992). Fossils from the Vind- stratigraphic sequences hypothesized to be tinct morphological features of complex multi- hyan Supergroup in India are suggested to repre- remnants of previously interconnected basins in cellularity and sexual reproduction (Butterfield et sent ca. 1.6 Ga algae (Bengtson et al., 2017), but their age (Ray, 2006) and taxonomic assignment 1 GSA Data Repository item 2017030, supplemen- tal methods, text, Figures DR1–DR4, Tables DR1– *Current address: Department of Geological & are uncertain. The first fossils with robust age DR3, is available online at http://www.geosociety.org Environmental Sciences, Stanford University, 450 control that conclusively display both the large /datarepository /2017/ or on request from editing@ Serra Mall, Stanford, California 94305, USA. cell size and complex ultrastructure or surface geosociety.org. GEOLOGY, February 2018; v. 46; no. 2; p. 135–138 | GSA Data Repository item 2018030 | https://doi.org/10.1130/G39829.1 | Published online 8 December 2017 ©GEOLOGY 2017 Geological | Volume Society 46 | ofNumber America. 2 For| www.gsapubs.org permission to copy, contact [email protected]. 135 (Cohen et al., 1999; Creaser et al., 2002; Cohen, A Conglomerate B 2004) rather than open-system behavior of the Sinasiuvik ~0.72 Ga Sandstone Greenland Re-Os isotope system. This conclusion is based Fm. on (1) linear correlation between 187Re/188Os and . Siltstone 187 188 . Os/ Os within each sample set; (2) general Shale agreement both between these ages and with Elwin sg Carbonate existing age constraints; (3) lack of correlation Aqigilik between 187Os/188Os and 1/188Os (Kendall et al., Fm. Basalt 2009; Rooney et al., 2010); and (4) Re and Os Nunatsiaq Gp Unconformity Somerset Island Bylot Island Borden Basin abundances and Osi values similar to reported Strathcona Bangiomorpha Sound Fm. values for black shale (Dubin and Peucker- Athole Pt. pubescens Aston-Hunting Baffin Island Ehrenbrink, 2015). Regression of samples from Fm. n Re-Os samples Basi a narrow stratigraphic range yields statistically (this study) indistinguishable, but more precise (model 3) depositional ages than regressions using the Victor Bay Elwin sg. full stratigraphic sampling ranges. Arctic Bay Fm. C Strathcona Sound Fm. Formation samples from a 2.9 m stratigraphic G1431 & MB1501 Athole Point Fm. Victor Bay Fm. range yield an age of 1.048 ± 0.012 Ga (2σ, n luksan Gp. Angmaat / Nanisivik Fm. = 5), and Victor Bay Formation samples from a Nanisivik Angmaat Fm. 0.15 m stratigraphic range yield an age of 1.046 Fms. Ikpiarjuk Fm. Ikpiarjuk Fm. Iqqittuq Fm. ± 0.016 Ga (2σ, n = 6; Fig. 2). These deposi- Iqqittuq Fm. 73°N Fabricius Fiord Fm. tional ages significantly improve chronostrati- Fabricius Fiord Fm. Arctic Bay Fm. graphic constraints on the Bylot Supergroup and Arctic Bay T1413 MB1501 Adams Sound Fm. .U Fm. Nauyat Fm. bracket the Angmaat Formation. We propose T1413 Fault 20 km 1.047 +0.013/–0.017 Ga as the first appearance age of B. pubescens. Adams Milne Inlet Graben Eqalulik Gp Sound Fm. CROSS-CALIBRATED MOLECULAR m 72°N G1431 CLOCK ANALYSES 500 Nauyat Fm. ~1.27 Ga When combined with robust fossil data, 84°W 82°W 80°W 78°W molecular clocks offer an effective method to Figure 1. Location and geological context of the study area. A: Schematic lithostratigraphy of query the evolutionary history of eukaryotes the Bylot Supergroup in the Borden Basin (age constraints from LeCheminant and Heaman, (Hedges et al., 2004; Parfrey et al., 2011; Shih 1989; Heaman et al., 1992; Pehrsson and Buchan, 1999). Gp.—Group; sg.—subgroup; Fm.— and Matzke, 2013). Although several potential Forma tion; Pt.—Point. B: Locations (red boxes) where Bangiomorpha pubescens occurs. C: Map sources of error exist in molecular clock analy- of the Borden Basin (adapted from Turner, 2009) showing Re-Os sample localities (red stars) ses, one pivotal, geologically resolvable incon- and B. pubescens fossil locality (yellow star; Knoll et al., 2013). sistency