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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 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 is poorly resolved taxonomically and chronologically. The red alga pania and Valeria (Javaux et al., 2001; Lamb et Bangiomorpha pubescens is the only recognized crown-group 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 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 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 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 (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 © 2017 Geological | Volume Society 46 | ofNumber America. 2 For| www.gsapubs.org permission to copy, contact [email protected]. 135

Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/46/2/135/4033219/135.pdf by Timothy M. Gibson on 14 January 2021 (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 187Os/188Os 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 72°N G1431 CLOCK ANALYSES 500 m 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 Forma­tion; 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 is in the fossil ages required for calibra- tion (Yoon et al., 2004; Berney and Pawlowski, northeastern Canada and northwestern Green- that the Hunting and Angmaat Formations, and 2006). As the first definitive fossil member of the land (known as the Bylot basins), the initial thus B. pubescens, are closer in age to 1.27 Ga and photosynthetic eukaryote (Butter- development of which was linked to emplace- than 0.72 Ga. This interpretation has informed a field, 2000), B. pubescens is the oldest eukaryotic ment of the ca. 1.27 Ga Mackenzie large igne- critical constraint for studies of eukaryotic evo- fossil included in these analyses and provides ous province (LIP; LeCheminant and Heaman, lution (Berney and Pawlowski, 2006; Parfrey et minimum limits on the age of both primary plas- 1989). Basalt flows with similar paleomagnetic al., 2011; Shih and Matzke, 2013; Knoll, 2014; tid endosymbiosis and the divergence between poles to the Mackenzie LIP occur at the base of Shih et al., 2017). the red (rhodophytes) and green (viridiplantae) the Bylot Supergroup and provide a maximum algae. To reexamine models for early eukaryotic depositional age for the overlying strata (Fahrig Re-Os evolution in light of the refined age of B. pube- et al., 1981). Mafic dikes that intrude the suc- Black shale samples were collected for scens, we conducted cross-calibrated molecular cession provide a minimum depositional age of Re-Os geochronology from stratigraphic sec- clock analyses (BEAST2, https://www.beast2. ca. 0.72 Ga (Heaman et al., 1992; Pehrsson and tions of the middle Arctic Bay and lower Victor org/; updated from Shih and Matzke, 2013), test- Buchan, 1999). Bay Formations in the Milne Inlet graben of ing three different priors on the rhodophytes-viri- The Angmaat Formation records prograda- northern Baffin Island (Fig. 1). Regression of all diplantae divergence: (1) no constraint, (2) the tion and stabilization of a rimmed carbonate Arctic Bay Formation samples yields a model 3 previously reported age for B. pubescens of ca. platform over black shale and siltstone of the age of 1.051 ± 0.031 Ga (2σ, n = 6, mean square 1.2 Ga (Butterfield, 2000), and (3) the age from underlying Arctic Bay Formation (Fig. 1; Turner, of weighted deviates, MSWD = 4.5) with an this study of ca. 1.045 Ga (Table 1). 187 188 2009). A regional subaerial unconformity devel- initial Os/ Os (Osi) of 1.44 ± 0.27. Regres- oped above the Angmaat Formation and is over- sion of all Victor Bay Formation samples yields DISCUSSION lain by black shale of the lower Victor Bay For- a model 3 age of 1.047 ± 0.032 Ga (2σ, n = 8, Much diversity within the Eukarya derives

mation, deposited during a subsequent marine MSWD = 6.4, Osi = 1.24 ± 0.17; Fig. DR4; from various forms of plastid acquisition (Del- transgression (Sherman et al., 2001). Chemo­ Table DR1). Uncertainty in these ages owes wiche, 1999), but dating the original endosym- stratigraphic data (Kah et al., 1999) and the largely to variation in the 187Os/188Os of basin biosis of an ancient photosynthetic cyanobac- absence of any discernable depositional hiatus in waters throughout the depositional timespan terium has been elusive. Our molecular clock the lower Bylot Supergroup led to the inference recorded by the sampled stratigraphic intervals analysis using the refined B. pubescens age of

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Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/46/2/135/4033219/135.pdf by Timothy M. Gibson on 14 January 2021 17 the most conservative (i.e., oldest) placement of the age assignment for these fossils is correct A Arctic Bay Fm. the B. pubescens constraint. Various morpho- (see the Data Repository), they may represent Age = 1.048 ± 0.012 Ga logical features of B. pubescens suggest that it eukaryotes that diverged long before the origins 15 Osi = 1.45 ± 0.10 MSWD = 0.69 T1413-181.1 might belong to the Bangiales within the of red and green algae. In this case, convergent n = 5 Rhodophyta (Butterfield, 2000), and thus our evolution may account for their similarities to 13 Os analyses provide a conservative minimum age extant algae. Considering that plastids have been 188 limit on primary plastid endosymbiosis. acquired at least twice within the Eukarya (i.e., 11 Os / Although the algorithms employed in molec- algae and Paulinella; Marin et al., 2005), these 187 T1413-182.6 T1413-181.8a ular clock studies differ, the age constraints they fossils could represent an early failed experi- T1413-182.0 implement exert by far the greatest control on mentation in photosynthesis. In addition, it is 9 T1413-184.0 their results. Accordingly, results from this study difficult to distinguish the primary morphology 187Re/188Os are calibrated with and improved by the revised of these fossils from secondary taphonomic fea- 7 350 450 550 650 750 850 first appearance age of B. pubescens. However, tures from phosphatization that obscure their we note that these analyses differ from previ- taxonomic assignment. However, if the inter- B Victor Bay Fm. ous studies in other ways. Due to the paucity of pretations of the taxonomic identity and age of 9 Age = 1.046 ± 0.016 Ga MB1501-51.6a available calibration points in deep , Pre- these fossils are correct, then they are discordant Osi = 1.28 ± 0.10 MSWD = 1.15 MB1501-51.6b cambrian molecular clock studies often employ with the results of this study. n = 6 MB1501-51.7 indirect or ambiguous constraints on the origins Os 7 of key lineages (e.g., Archean lipid biomark- CONCLUSIONS 188 ers and/or microfossils of uncertain taxonomic Given the remarkable preservation of B. Os / affinity) that affect their age estimates for evo- pubescens and its morphological similarities 18 7 G1431-26.0d G1431-28.1 5 lutionary events. For example, Sánchez-Bar- to modern Bangia red algae (Butterfield et al., acaldo et al. (2017) calculated, using contro- 1990; Butterfield, 2000), a precise first appear- G1431-26.0b versial cyanobacterial microfossil calibrations ance age of 1.047 Ga cements its role as currently 187Re/188Os (Butterfield, 2015), that both primary plastid the most robust geological datum for reconstruct- 3 100200 300400 500 endosymbiosis and the split between the red ing early eukaryotic evolution. This revised age and green algae occurred ca. 1.9 Ga. Because narrows the window for when photosynthesis in Figure 2. Re-Os isochron diagrams. A: The Arctic Bay Formation. MSWD—mean square divergence calculations from molecular data are crown eukaryotes first evolved and introduces of weighted deviates. B: The Victor Bay For- only as valuable as their geological tie points, a chronological framework for investigating mation. Data-point error ellipses represent 2σ this study employs less controversial constraints the role this fundamental biological innovation uncertainty. Elemental abundances and isoto- from the fossil record of algae and plants; and played in shaping global biogeochemical cycles. pic compositions are presented in Table DR1 by using a cross-calibration approach (Shih and (see footnote 1). Matzke, 2013), the value of these constraints is ACKNOWLEDGMENTS effectively doubled. This research was supported by the Agouron Institute, as well as funding from the Geo-mapping for Energy Various other Proterozoic fossils have been and Minerals (GEM), GEM-2, Natural Sciences and ca. 1.045 Ga (run T09) suggests that primary suggested to represent ca. 1.8–1.6 Ga primi- Engineering Research Council of Canada, and Polar plastid endosymbiosis occurred by ca. 1.25 Ga tive eukaryotic algae (Han and Runnegar, Continental Shelf Program. Gibson acknowledges (Table 1). This analysis yields a decrease in the 1992; Moczydłowska et al., 2011; Bengtson et funding from the Eric Mountjoy Legacy Fund (McGill 95% confidence interval width for this event al., 2017). The Vindhyan Supergroup of cen- University), Mountjoy Exchange Award (Geologi- cal Association of Canada), and a Graduate Student compared to the analysis using the previously tral India was interpreted to host ca. 1.6 Ga Research Grant (Geological Society of America). We accepted age of B. pubescens (run T08). The crown-group rhodophyte fossils (Bengtson et thank E.J. Javaux, A.D. Rooney, and an anonymous analysis with no age constraint for B. pubescens al., 2017). Whereas Rafatazmia chitrakootensis reviewer for constructive comments. places the divergence between rhodophytes and and Ramathallus lobatus may have eukaryotic viridiplantae at 1.166 Ga, which is younger than affinities, they are hundreds of millions of years REFERENCES CITED the fossil’s previously inferred age, but consis- older than most phylogenetic estimates (includ- Adam, Z.R., Skidmore, M.L., Mogk, D.W., and Butter- field, N.J., 2017, A Laurentian record of the earli- tent with this study and many previous molec- ing those that exclude the age of B. pubescens as est fossil eukaryotes: Geology, v. 45, p. 387–390, ular clock estimates (Berney and Pawlowski, a constraint) for the rhodophytes-viridiplantae https://​doi​.org​/10​.1130​/G38749.1. 2006; Cavalier-Smith et al., 2006; Parfrey et al., divergence, more than 500 m.y. older than B. 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TABLE 1. EFFECTS OF THE NEW AGE FOR BANGIOMORPHA PUBESCENS ON MOLECULAR CLOCK ANALYSES Run Bangiomorpha age prior for red-green divergence Red-Green Divergence ± 2σ 95% CI width Primary plastid endosymbiosis ± 2σ 95% CI width (Ga) (Ga) (Ga) T07 omitted1.166 (1.450–0.883) 0.5671.325 (1.1647–1.029)0.618 T08 1. 198 ± 0.024 (previous) 1. 194 (1.242–1.150)0.092 1. 422 (1.568–1.291)0.277 T09 1.045 ± 0.015 (this study) 1.046 (1.046–1.016)0.058 1. 246 (1.368–1.142) 0.226 Note: Multiple analyses using a lognormal relaxed clock in BEAST2 (https://www.beast2.org/) utilized either no constraint for the age of B. pubescens (run T07), its previously accepted age (run T08), or its new reported age from this study (run T09). The various analyses were compared based on 95% confidence interval (CI) widths (in billions of years) of key nodes of interest, specifically the red-green divergence and plastid endosymbiosis. BEAST2 run outputs are presented in Figures DR1–DR3 (see text footnote 1).

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