Earth’s earliest non-marine eukaryotes more

LETTER Earth’s earliest non-marine eukaryotes Paul K. Strother1, Leila Battison2, Martin D. Brasier2 & Charles H. Wellman3 doi:10.1038/nature09943 The existence of a terrestrial Precambrian (more than 542 Myr ago) biota has been largely inferred from indirect chemical and geological evidence associated with palaeosols1,2, the weathering of clay minerals3 and microbially induced sedimentary structures in siliciclastic sediments4. Direct evidence of fossils within rocks of nonmarine origin in the Precambrian is exceedingly rare5,6. The most widely cited example comprises a single report of morphologically simple mineralized tubes and spheres interpreted as cyanobacteria, obtained from 1,200-Myr-old palaeokarst in Arizona5. Organicwalled microfossils were first described from the non-marine Torridonian (1.2–1.0 Gyr ago) sequence of northwest Scotland in 19077. Subsequent studies8–10 found few distinctive taxa—a century later, the Torridonian microflora is still being characterized as primarily nondescript ‘‘leiospheres’’11. We have comprehensively sampled grey shales and phosphatic nodules throughout the Torridonian sequence. Here we report the recovery of large populations of diverse organic-walled microfossils extracted by acid maceration, complemented by studies using thin sections of phosphatic nodules that yield exceptionally detailed three-dimensional preservation. These assemblages contain multicellular structures, complex-walled cysts, asymmetric organic structures, and dorsiventral, compressed organic thalli, some approaching one millimetre in diameter. They offer direct evidence of eukaryotes living in freshwater aquatic and subaerially exposed habitats during the Proterozoic era. The apparent dominance of eukaryotes in non-marine settings by 1 Gyr ago indicates that eukaryotic evolution on land may have commenced far earlier than previously thought. The Torridonian is a thick (up to 12 km) sequence of immature siliciclastic rocks deposited in three unconformable Groups: Stoer, Sleat and Torridon (Supplementary Figs 1, 2). The Stoer Group (Pb– Pb age, 1,199 6 70 Myr (ref. 12); 40Ar–39Ar age, 1,178.6 6 9 Myr (ref. 13)) is unconformably overlain by the Torridon Group, which has been dated as old as 994 6 48 Myr on the basis of Rb–Sr isochrons in the lowermost Diabaig Formation12. The Sleat Group has not been dated, but it is conformably overlain with strata correlated with the Torridon Group: the Applecross Formation is present, and parts of the Kinlock Formation have been correlated with the Diabaig Formation. The Torridonian rocks consist largely of compositionally immature, coarse-grained, siliciclastic redbeds with lesser red and grey shales. Numerous lines of lithological evidence point towards a non-marine depositional setting for the entire Torridonian sequence. These include evidence of valley-confined alluvial fans, rivers and unconfined bajadas in the Stoer Group14; braided rivers15 and fan-delta/lake deposits in the Sleat Group14–16; and, in addition to these fluvial and alluvial deposits, valley-confined lakes in the Torridon Group14. The interpretation of the grey shales of the Diabaig Formation (the basal unit of the Torridon Group) as lacustrine deposits is reinforced by a low boron content17, small wave ripples (Supplementary Fig. 3) and pervasive desiccation cracks4,14 (Supplementary Fig. 4), in combination with a lack of marine features such as tidal bundles and evaporites accompanying desiccation. Raindrop impressions found at Upper Diabaig and at Point Stoer provide additional evidence of subaerial exposure of mudrock 1 units (Supplementary Fig. 5). It has been concluded4 that sedimentary structures in the Diabaig Formation preserve non-marine microbial mats. Recent regional studies of the Torridonian, incorporating zircon provenance, continue to support a non-marine depositional setting for the entire sequence11. Samples of grey shale were collected from 17 different localities (Supplementary Figs 1, 2, Supplementary Table 1), of which 11 sections were reasonably productive (Supplementary Table 2). All of our samples, with the exception of TOR08-9, an isolated sample from Tarskavaig on Sleat, are from previously published stratigraphic sections where an inferred depositional environment based on geological grounds had been determined15. Dark grey shales, from which all palynomorphs were extracted, are considered to be lake bottom sediments, although at Cailleach Head, some of the yellowish grey mudstones are interpreted to be delta toe sediments15. These sediments retain the allochthonous character of normal sedimentation—they formed when rivers and streams scoured the regional surface and transported those sediments into a basin. The palynological content of our samples represents a combination of this allochthonous input plus in situ microfossils. Palynological samples were supplemented by thin section studies of phosphatic nodules from Loch Diabaig and Cailleach Head, which support the largely allochthonous nature of these deposits because they do not retain evidence of in situ microbial biofabrics. Palynological assemblages (see Methods Summary) are dominated by simple spherical palynomorphs (sphaeromorph acritarchs) without distinctive surface ornament or sculpture, of the kind usually placed in the genus Leiosphaeridia (Fig. 1a). Surface ornament, when present, is limited to low verrucae (Fig. 1b) or scattered granae (Fig. 1c, d). Acanthomorph (with spines) acritarchs have not been observed. Excystment features include simple median splits (Fig. 1e) and circular pylomes (Fig. 1f). Such features, including pre-formed sutures in the cell wall, are associated with a eukaryotic level of cellular structure18. The appearance and texture of vesicle walls is remarkably varied, reflecting primary differences in thickness, construction and original composition. Some vesicle walls are structurally complex, as in Fig. 1g, h, and Supplementary Fig. 6. Here the vesicle wall is composed of roughly parallel, short cylindrical subunits, which impart a coarsely corrugate appearance in surface (Fig. 1g) view and a beaded appearance equatorially (Fig. 1h, Supplementary Fig. 6a, e). Overall, this multicellular fossil (Fig. 1h, Supplementary Fig. 6a, e) consists of a mass of cells tightly packed together and encased within a spherical vesicle. The bluntly ellipsoidal specimen in Fig. 1i has a distinctive wall, characterized by a highly-ordered arrangement of circular pits creating a reticulate pattern (Fig. 1j). This undescribed taxon superficially resembles Dictyosphaera, but lacks the plate-like wall structure of this Mesoproterozoic eukaryote19. Cell clusters are quite common, including Synsphaeridium spp. (Fig. 1k), Chlorogloeaopsis spp. (German) Hofmann and Torridoniphycus lepidus Zhang (in part). Many cell clusters show features such as mutually adpressed walls (Fig. 2a), indicating that these are not simply random associations of solitary cells. The preservation of internal bodies within vesicle walls is quite common; such a morphological feature is seen in numerous other Proterozoic Department of Earth and Environmental Sciences, Boston College, Weston, Massachusetts 02493, USA. 2Department of Earth Sciences, University of Oxford, Parks Road, Oxford OX1 3PR, UK. 3Department of Animal & Plant Sciences, The University of Sheffield, Sheffield S10 2TN, UK. 0 0 M O N T H 2 0 1 1 | VO L 0 0 0 | N AT U R E | 1 ©2011 Macmillan Publishers Limited. All rights reserved RESEARCH LETTER a c d b e f g h i j k Figure 1 | Sphaeromorph acritarchs and cell clusters from the Torridonian, NW Scotland. a, Leiosphaeridia crassa; TOR08-18/Glame Member, Applecross Formation. b, Acritarch similar to Trematoligotriletum emarginatum Tim. with irregular verrucate surface; TOR08-26/Allt na Beistre Member, Applecross Formation. c, Lophosphaeridium sp. enclosed in a thin membranous vesicle; TOR08-34/Diabaig Formation. d, Surface detail of inner cyst (Lophosphaeridium sp.) in c showing small, evenly distributed granae. e, Leiosphaeridia crassa exhibiting a median split; TOR08-45/Cailleach Head Formation. f, Ellipsoidal cyst with granular wall structure exhibiting a terminal circular pylome excystment feature (arrow); TOR08-34/Diabaig Formation. g, Coarsely corrugate vesicle with dense contents; TOR08-27/Diabaig Formation. h, Spherical ball of cells enclosed within a complex wall (thin section from phosphatic nodule, Diabaig Formation). i, Blunt ellipsoidal vesicle with a micro-reticulate wall; TOR08-46/Cailleach Head Formation. j, Detail of i (box), showing the reticulate wall texture. k, Cell cluster, similar to Synsphaeridium sp. Note included condensed organic ‘spots’ (arrows); TOR0826/Allt na Beistre Member, Applecross Formation. Scale bars: 10 mm (a– c, e–i, k), 1 mm (d, j). assemblages6,20. These dense organic ‘spots’ occur in both macerated specimens (Fig. 1k, arrows) and thin sections that retain threedimensional preservation (Fig. 2a, arrows). The Torridonian assemblages contain some striking examples of microfossils that show complexity that goes considerably beyond that of simple leiospheres. Figure 1h illustrates a multicellular sphere from a phosphatic nodule with a clearly differentiated outer wall that is similar to the dispersed corrugated forms in Fig. 1g and Supplementary Fig. 6e, f. A confocal laser scanning image of the same specimen (Supplementary Fig. 6a), representing a 0.2-mm-thick slice through the equatorial plane of the vesicle sphere, reveals a solid mass of mutually compressed cells. Some of these interior cells (Fig. 1h) retain a dense ‘spot’, probably the plasmolysed remnants of original cell contents. Figure 2b illustrates a large fusiform vesicle (475 mm wide) with a pitted (Fig. 2c) interior wall structure. Figure 2d shows a dark, heterogeneous central body (cb) enclosed within a large cyst with a peripheral asymmetrical structure (as), which itself appears to consist of several cylindrical cells or membranous outgrowths of the vesicle wall (Fig. 2e). The enclosed central body does not appear multicellular when viewed in transmitted infrared light (Fig. 2f). Another example of a large vesicle with asymmetric features is illustrated in Fig. 2g. This specimen lacks complex internal 2 | N AT U R E | VO L 0 0 0 | 0 0 M O N T H 2 0 1 1 features, but does contain a single degraded central body (cb) and a clearly differentiated asymmetric structure (as) composed of several stubby projections. Not all the fossils recovered are vesicular in their gross organization. The specimen in Fig. 3a possesses two arm-like projections (arm) with bluntly rounded tips attached to a large elliptical disk. One of the arms appears to be constricted at its basal attachment site (ba), giving the impression of either multicellular or coenocytic organization. This fossil is unlike any previously described acritarch. The tri-lobate thalloid form illustrated in Fig. 3b is 915 mm wide and represents the largest intact fossil recovered to date from the Torridonian sequence. The thallus is preserved as a dense, thick, organic layer, the upper surface of which appears as a dense cuticle-like protective layer. Internally the thallus appears irregularly reticulate when viewed in transmitted infrared light (Fig. 3c). This could be a reflection of an underlying parenchymatous cell structure which is now considerably degraded, and we interpret this specimen to be an example of biological structure that was approaching a tissue-level grade of organization. There is no evidence that the thallus was composed of filaments or has retained an underlying filamentous structure which might be construed as evidence for fungal or lichen affinity. Several examples of poorly preserved, spine-like structures ©2011 Macmillan Publishers Limited. All rights reserved LETTER RESEARCH a b c d e f as g cb cb as Figure 2 | Cell clusters and large, morphologically complex vesicles. Lines in b and d demarcate edges of separate images used to construct the photo mosaics. a, Cell cluster exhibiting mutually adpressed cells with included ‘spots’ (arrowed). This image is a photomontage of three different focal planes (thin section from phosphatic nodule, Diabaig Formation). b, Large fusiform vesicle with pitted/reticulate wall structure; TOR08-9b/Kinloch Formation. c, Detail from b, showing a portion of the inside of the vesicle wall. d, Large vesicle with a a arm dense central body (cb) and an asymmetric structure (as); TOR08-34/Diabaig Formation. e, Detail of the asymmetric structure in d. f, Transmitted infrared (.830 nm) image of the central body in c, showing it to be a thick-walled, probably unicellular cyst. g, Large vesicle with a single-layered inner cyst and a large asymmetric structure (as) which appear as stubby projections from the main vesicle wall; TOR08-12/Kinloch Formation. Scale bars: 10 mm (a, c, e, f); 50 mm (b); 25 mm (d, g). b arm ba c d Figure 3 | Non-vesicular organic structures. a, Oval plate with two blunttipped arms (arm), one of which is attached (ba, arrowed) with what appears to be a basal plug; TOR08-32/Diabaig Formation. b, Tri-lobed thalloid organism with a dense upper surface showing small cracks and a heterogeneous inner layer. Image is a photomontage of four photographs; TOR08-40/Diabaig Formation. c, Detail of b photographed in infrared (.830 nm) transmitted light to reveal the internal structure. d, Spine (appendage?) tip; TOR08-34/ Diabaig Formation. Scale bars: 50 mm (a); 100 mm (b); 10 mm (c, d). 0 0 M O N T H 2 0 1 1 | VO L 0 0 0 | N AT U R E | 3 ©2011 Macmillan Publishers Limited. All rights reserved RESEARCH LETTER were recovered (Fig. 3d). None resemble the spines or processes typically associated with acanthomorphic acritarchs. A set of morphological criteria has been put forward18,21 for assessing the record of early eukaryotes recovered in marine habitats by 1,500 Myr ago. Similar arguments can applied to the interpretation of microfossils found in non-marine settings at 1 Gyr ago. The excellent preservation in the Torridonian deposits has permitted the retention of putative vegetative stages; this enables a greater range of form and biological structure to be recognized. In Fig. 1c, a thicker-walled cyst which is ornamented with uniformly distributed granae (Fig. 1d, Lophosphaeridium sp.) is enclosed within a thinner-walled vesicle interpreted to be the original vegetative cell wall. This combination of two different wall types and the sculptured inner wall appears to be a eukaryotic feature. The possession of a pre-determined excystment opening, such as a median split (Fig. 1e), has been taken to indicate cytoskeletal control of excystment consistent with eukaryotic complexity18. This is reinforced in Fig. 1f (arrow), which shows a preformed circular opening which would have functioned in excystment. Several larger microfossils also possess asymmetric features, which appear to be autapomorphies associated with evolution of unicellular eukaryotes. One large specimen (Fig. 2d) from the Sleat Group (Kinloch Formation) sports a singular set of thin-walled cylindrical structures (as) attached at one place on the surface (Fig. 2e). The enclosed dense central body (cb) appears vesicular and cyst-like (Fig. 2f), implying that the outer vesicle was originally vegetative. The folded arms in Fig. 3a arguably required cytoskeletal control of growth of the kind associated with a eukaryotic level of cellular organization. This combination of large size, topology, variable wall texture, and wall structure indicates that most of the Torridonian microfossils recovered from maceration are likely to have been of eukaryotic origin. Taxonomic overlap between sphaeromorph acritarchs recognized here in lacustrine settings (Supplementary Table 2) and nearshore marine settings elsewhere in the Neoproterozoic6,21–23 does not necessarily indicate that non-marine acritarch species are a common component of near-shore marine assemblages. Genera such as Leiosphaeridia, Synsphaeridium and Lophosphaeridium may be too morphologically simple to assure meaningful biological homology between samples of different ages and depositional settings. The preservation of a three-dimensional ball of cells enclosed by a complex cell wall (Fig. 1h, Supplementary Fig. 6a–d) corresponds to a level of complexity that is not typical of prokaryotes. On the other hand, the enclosed cells are only about 2 mm in diameter, seemingly too small (and too ancient) to represent a metazoan blastula. Intriguingly, these seemingly multicellular structures may be compared with the early palintomic phase that forms part of the synzoospore hypothesis ¨ for metazoan origins24, during which the generative cell (oocyte) of a unicellular protoctist cleaves internally to produce smaller cells which remain attached to each other (synzoospores), forming a multicellular ball of cells. The simplicity of these balls of cells precludes their systematic assignment within the Eukarya. However, their morphology, in combination with larger, probably multicellular thalli (Fig. 3 b), indicates that evolutionary processes that preceded tissue-grade multicellularity in marine settings25, such as cell-to-cell adhesion, were also evident in non-marine settings by 1 Gyr ago. Sample to sample heterogeneity seen throughout the Torridonian (Supplementary Table 2, Supplementary Fig. 7) clearly indicates a significant degree of biotic diversity, reflecting adaptation to freshwater aquatic and subaerially exposed habitats by earliest Neoproterozoic time. Early eukaryotes were clearly capable of diversifying within non-marine habitats, not just in marine settings as has been generally assumed. This idea directly supports phylogenomic studies which find that the cyanobacteria evolved first in freshwater habitats and later migrated into marine settings26. Our findings also lend support to recent inferences regarding the impact of Neoproterozoic terrestrial biotas on Earth’s biogeochemical cycles3,13,27–29. Freshwater habitats are ecologically more variable than marine habitats30, providing temporal 4 | N AT U R E | VO L 0 0 0 | 0 0 M O N T H 2 0 1 1 and physiochemical heterogeneity, including wet-drying cycles and direct atmosphere–organism gas exchange. Such habitat heterogeneity translates directly into increased speciation potential. Some of the microfossils illustrated here must have experienced subaerial exposure because they occur in situ in microbially induced sedimentary structures with desiccation cracks (Supplementary Fig. 4), but the extent to which they lived subaerially cannot be ascertained with certainty. Even so, gross morphology, in combination with an apparent lack of planktonic adaptive morphology, in the form of processes or spines, strongly suggests that a range of benthic, freshwater habitats were already colonized by eukaryotes by the beginning of the Neoproterozoic era. METHODS SUMMARY Palynological samples were prepared using conventional acid maceration techniques. Following HCl-HF-HCl acid maceration, the residues were sieved using a 10 mm mesh. They were then treated to a heavy liquid separation using zinc chloride, followed by further sieving at 10 mm. The organic residues were mounting directly onto glass slides using epoxy resin. Phosphatic nodules were studied using petrographic thin sections cut parallel to bedding and crossing bedding. These were ground to varying thicknesses to optimize transparency of the dark phosphate and the position of the fossils within the phosphate. Microscopical analysis was undertaken using transmitted white light supplemented by infrared analysis and laser confocal microscopy. All photomicrographs were recorded as 16 bit raw files (3,043 3 2,036 pixels) using a FujiFilm S5 IS Pro (infrared) digital camera body attached to a Zeiss Universal microscope equipped with Zeiss PlanApo 633 and Zeiss Plan-Neofluor 253 objectives. White light photomicrographs were photographed through a B1W 486 ultraviolet/infrared blocking filter to achieve a visible light colour balance; infrared images were captured using a long pass filter (830 nm, Edmund Scientific). Images were captured with FujiFilm Studio Utility software running on an iMac. An approximately neutral grey background was achieved by setting white to 219 in the levels menu in Photoshop. The image in Supplementary Fig. 6a was obtained with a Leica SP5 confocal laser scanning microscope using ultraviolet excitation at 405 nm and collection between 418 and 780 nm. Except where noted, no sharpening or any other image processing was used. Infrared images were converted to greyscale from RGB using the channel mixer adjustment menu in Photoshop CS4. Received 13 October 2010; accepted 16 February 2011. Published online 13 April 2011. 1. 2. 3. Ohmoto, H. Evidence in pre-2.2 Ga paleosols for the early evolution of atmospheric oxygen and terrestrial biota. Geology 24, 1135–1138 (1996). Gutzmer, J. & Beukes, N. J. Earliest laterites and possible evidence for terrestrial vegetation in the Early Proterozoic. Geology 26, 263–266 (1998). Kennedy, M., Droser, M., Mayer, L. 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Reduction spots in the Mesoproterozoic age: implications for life in the early terrestrial record. Int. J. Astrobiol. 9, 209–216 (2010). 30. Hutchinson, G. E. The paradox of the plankton. Am. Nat. 95, 137–145 (1961). Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Acknowledgements J. Rosenberg produced the confocal laser scanning image (Supplementary Fig. 6a); we thank O. Green for preparation of phosphatic nodules at Oxford. We thank J. Antcliffe, R. Callow and S. Moorhouse for field assistance and the people of Scoraig and Bill (the boatman) for access to Cailleach Head. This research was supported by NASA grant NNX07AU79G (P.K.S.), NERC NE/G015716/1 (C.H.W.) and NERC NE/G524060/1 (L.B.). Author Contributions All authors contributed to the intellectual content, design and writing of the manuscript, and collection and study of phosphatic nodules. C.H.W. and P.K.S. collected the palynological samples. P.K.S. wrote an initial draft, prepared the photographic plates and produced the provisional taxonomic assessment. L.B. and C.H.W. drafted the figures. Author Information All materials (rock sample, remaining organic residues, palynological slides, thin sections) are curated in the collections of the Centre for Palynology of the University of Sheffield, UK. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests. Readers are welcome to comment on the online version of this article at www.nature.com/nature. Correspondence and requests for materials should be addressed to P.K.S. (Strother@bc.edu). 0 0 M O N T H 2 0 1 1 | VO L 0 0 0 | N AT U R E | 5 ©2011 Macmillan Publishers Limited. All rights reserved