A one-billion-year-old multicellular chlorophyte

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Abstract

Chlorophytes (representing a clade within the Viridiplantae and a sister group of the Streptophyta) probably dominated marine export bioproductivity and played a key role in facilitating ecosystem complexity before the Mesozoic diversification of phototrophic eukaryotes such as diatoms, coccolithophorans and dinoflagellates. Molecular clock and biomarker data indicate that chlorophytes diverged in the Mesoproterozoic or early Neoproterozoic, followed by their subsequent phylogenetic diversification, multicellular evolution and ecological expansion in the late Neoproterozoic and Palaeozoic. This model, however, has not been rigorously tested with palaeontological data because of the scarcity of Proterozoic chlorophyte fossils. Here we report abundant millimetre-sized, multicellular and morphologically differentiated macrofossils from rocks approximately 1,000 million years ago. These fossils are described as Proterocladus antiquus new species and are interpreted as benthic siphonocladalean chlorophytes, suggesting that chlorophytes acquired macroscopic size, multicellularity and cellular differentiation nearly a billion years ago, much earlier than previously thought.

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Fig. 1: Gross morphology of P. antiquus new species from the Nanfen Formation.
Fig. 2: Cellular structures of P. antiquus new species.
Fig. 3: Comparison of extant Siphonocladales of genera Cladophora and Rhizoclonium to Proterocladus.
Fig. 4: Artist’s reconstruction of P. antiquus.

Data availability

All specimens illustrated in this paper are reposited and available at Virginia Polytechnic Institute Geoscience Museum (Blacksburg, VA, USA; museum catalogue nos. VPIGM-4749–4794 and VPIGM-4799).

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Acknowledgements

S.X. and Q.T. were supported by NASA Exobiology and Evolutionary Biology (grant no. 80NSSC18K1086). X.Y. and K.P. were supported by the National Natural Science Foundation of China (grant nos. 41602007 and 41921002), the Chinese Academy of Sciences (grant nos. QYZDJ-SSW-DQC009 and XDB26000000), the National Key Research and Development Programme of China (grant no. 2017YFC0603100), the Science Foundation of Jiangsu Province of China (grant no. BK20161090) and the State Key Laboratory of Palaeobiology and Stratigraphy of the Nanjing Institute of Geology and Palaeontology (grant nos. 193126 and 20162109). We thank J. Wang for field assistance.

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Q.T. and S.X. designed the research. Q.T. and K.P. conducted fieldwork. Q.T. conducted microscopic observation. S.X. and Q.T. developed the interpretation and prepared the manuscript with input from other co-authors.

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Correspondence to Qing Tang or Shuhai Xiao.

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Extended data

Extended Data Fig. 1 Geological map and stratigraphic column of Proterozoic successions in southern Liaoning Province, North China.

Question mark in stratigraphic column denotes poor age constraint on the Dalinzi Formation, which could be either Neoproterozoic or Cambrian in age. Stars in geological map and stratigraphic column mark sample locality (near Shileicun, 39°35.6566’N, 121°35.8379’E) and sample horizon, respectively. Ca=Cambrian, Pa=Paleoproterozoic, Fm=Formation, CLZ=Changlingzi, NGL=Nanguanling, GJZ=Ganjingzi, YCZ=Yingchengzi, SSLT=Shisanlitai, MJT=Majiatun, CJT=Cuijiatun, XMC=Xingmincun, GT=Getun. Radiometric ages (924 ± 5 Ma and 947.8 ± 7.4 Ma) of diabase sills emplaced in the Cuijiatun and Qiaotou formations are from ref. 22 and ref. 25; detrital zircon ages (<924 ± 25 Ma and <1056 ± 22 Ma) are from ref. 24. See ref. 25 for a compilation of ratiometric ages from Neoproterozoic successions in North China. Geological map drawn by authors based on ref. 22 with permission, and stratocolumn drawn by authors.

Extended Data Fig. 2 Proterocladus antiquus new species on bedding surface, showing lateral branches.

af, VPIGM-4763, VPIGM-4764, VPIGM-4765, VPIGM-4766, VPIGM-4767, and VPIGM-4768, respectively. All photos taken by authors.

Extended Data Fig. 3 P. antiquus preserved on bedding surface, showing multiple orders of lateral branches (a) and aggregates of thalli (b–d).

a–d, VPIGM-4769, VPIGM-4770, VPIGM-4771, and VPIGM-4772, respectively. All photos taken by authors.

Extended Data Fig. 4 Thallus of P. antiquus with a sub-discoid holdfast preserved on bedding surface.

b is a close-up view of labeled black frame in a. VPIGM-4773. All photos taken by authors.

Extended Data Fig. 5 Heteromorphic cells (a–l) and reproductive cells (m–o) of P. antiquus.

al, Filaments with globose (yellow arrowheads), clavate (black arrowheads), doliform (cyan arrowheads), and cyathiform (blue arrowhead) heteromorphic cells. b, k are magnifications of labeled frames in a and j, respectively. VPIGM-4774, VPIGM-4775, VPIGM-4776, VPIGM-4777, VPIGM-4778, VPIGM-4779, VPIGM-4780, VPIGM-4781, VPIGM-4782, and VPIGM-4783, respectively. mo, Inferred reproductive cells with minute lateral pores (blue arrows), possibly representing openings through which reproductive gametes or zoospores were released. VPIGM-4784, VPIGM-4785, and VPIGM-4786, respectively. Specimens in a and j were photographed on bedding surface, and all other specimens were extracted from the rock matrix using HF acid maceration technique. All scale bars equal 100 µm unless otherwise specified. All photos taken by authors.

Extended Data Fig. 6 Cell branching pattern and apical extensions in extracted specimens of P. antiquus.

a–c, Fragmented filaments with unilateral (a, c) and alternate branches (two lower lateral branches in b). VPIGM-4787, VPIGM-4788, and VPIGM-4789, respectively. d–e, Branching filaments with an inflated apical cell subtending a narrower apical extension (purple arrowhead in d) and an apical cell with septum and constriction (black arrows in e), which is interpreted to have developed from an apical extension. VPIGM-4790 and VPIGM-4791, respectively. All scale bars equal 100 µm. All photos taken by authors.

Extended Data Fig. 7 Branching thallus of P. antiquus with a cell (in black frame) that has a distinct constriction at base (blue arrowhead).

The branching pattern is superficially similar to H-shaped branching in the early vascular plant Zosterophyllum72. b is a magnification of white box in a, showing the basal constriction of the cell that initially may represent an apical extension that subsequently develops septa and branches at maturation. VPIGM-4792. All photos taken by authors.

Extended Data Fig. 8 Dense population of fragmented P. antiquus specimens preserved on bedding surface.

VPIGM-4793. All photos taken by authors.

Extended Data Fig. 9 Taphonomy of P. antiquus preserved in the Nanfen mudstone.

a, b, A partially exposed specimen. b is a backscattered electron scanning electron microscopy (BSEM) photograph of the same specimen in a. VPIGM-4794. c, Energy dispersive X-ray spectroscopy (EDS) point analysis at the blue spot in b, showing the presence of carbon in the fossil specimen. Horizontal axis is energy in KeV, and vertical axis is counts in arbitrary scale. d, EDS elemental maps of labeled box in b, showing the enrichment in C and deficiency in O, Al, and Si in fossil relative to matrix. e–g, Nanfen mudstone fractured obliquely relative to bedding plane, showing darker-colored fossil layers and lighter-colored background layers. f and g are magnifications of labeled boxes in e. hi, Polished slab cut perpendicular to bedding surface, showing darker-colored fossil layers and lighter-colored background layers. i is a close-up view of labeled box in h with blue arrowheads denoting fragmented fossils in a fossil layer. All photos taken by authors.

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Supplementary Table 1. Stratigraphy and sedimentary environment, age constraints, taphonomy and references.

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Tang, Q., Pang, K., Yuan, X. et al. A one-billion-year-old multicellular chlorophyte. Nat Ecol Evol 4, 543–549 (2020). https://doi.org/10.1038/s41559-020-1122-9

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