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. 2024 Jan 26;10(4):eadk3208.
doi: 10.1126/sciadv.adk3208. Epub 2024 Jan 24.

1.63-billion-year-old multicellular eukaryotes from the Chuanlinggou Formation in North China

Lanyun Miao  1 , Zongjun Yin  1 , Andrew H Knoll  2 , Yuangao Qu  3 , Maoyan Zhu  1   4
Affiliations

1.63-billion-year-old multicellular eukaryotes from the Chuanlinggou Formation in North China

Lanyun Miao et al. Sci Adv. .

Abstract

Multicellularity is key to the functional and ecological success of the Eukarya, underpinning much of their modern diversity in both terrestrial and marine ecosystems. Despite the widespread occurrence of simple multicellular organisms among eukaryotes, when this innovation arose remains an open question. Here, we report cellularly preserved multicellular microfossils (Qingshania magnifica) from the ~1635-million-year-old Chuanlinggou Formation, North China. The fossils consist of large uniseriate, unbranched filaments with cell diameters up to 190 micrometers; spheroidal structures, possibly spores, occur within some cells. In combination with spectroscopic characteristics, the large size and morphological complexity of these fossils support their interpretation as eukaryotes, likely photosynthetic, based on comparisons with extant organisms. The occurrence of multicellular eukaryotes in Paleoproterozoic rocks not much younger than those containing the oldest unambiguous evidence of eukaryotes as a whole supports the hypothesis that simple multicellularity arose early in eukaryotic history, as much as a billion years before complex multicellular organisms diversified in the oceans.

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Figures

Fig. 1.
Fig. 1.. Transmitted-light (TL) photomicrographs of Q. magnifica from the Chuanlinggou Formation.
(A to D and K) Filaments with cells of varying length and width. (E) Four-celled filament with hemispherical terminal cell. (F and G) Filament with notably decreasing cell width toward one end. Note that (F) and (G) represent the same specimen; (F) lost the narrowest part of the filament as shown in (G). (H to J) Filaments displaying more uniformity of cell dimensions. (L) Two-celled filament with ovoid terminal cell. All specimens were handpicked from organic residues of acid maceration and photographed in wet mounts, except for (K), which was photographed from a permanent strew mount. Solid and empty gray triangles in (A), (C), and (K) indicate the longest and the shortest cells, respectively, within single filaments. tb, transverse band (interpreted as cross wall); tr, transverse ring (interpreted as partially preserved cross wall). Scale bar, 50 μm [(A) to (E), (I), (J), and (L)] and 100 μm [(F) to (H) and (K)].
Fig. 2.
Fig. 2.. Micrographs of Q. magnifica from the Chuanlinggou Formation.
(A) TL photomicrograph of a five-celled filament with constant width and dark narrow transverse bands. (B) SEM image of (A) showing surface features and the preservation as a complete compression. Note the obliquely compressed cross wall of the right terminal cell showing smooth surface and no other particular features. (C to E) Magnifications of (B), showing smooth wall surface and the well-defined contact between adjoining cells manifested by a very shallow groove (marked by cyan arrowheads) along transverse bands. (C) and (E) represent dashed boxes in (A) and (B); (D) corresponds to the dashed box in (C). Scale bars, 50 μm [(A) and (B)], 10 μm (C), and 2 μm [(D) and (E)].
Fig. 3.
Fig. 3.. TL photomicrographs of Q. magnifica with a small round or ovoid inclusion from the Chuanlinggou Formation.
(A, C, and D) Filaments with constant width. (B and E) Magnifications of dashed boxes in (A) and (C), respectively, showing details of round inclusions. (F) Filament of notably varying width. Note that the middle cell of the filament is cyathiform in shape. (G and H) Magnifications of dashed box in (F) and (D), respectively. All specimens were handpicked from organic residues of acid maceration and photographed in wet mounts. Scale bar, 50 μm [(A), (C), (D), and (F)].
Fig. 4.
Fig. 4.. Morphometric analyses of Q. magnifica from the Chuanlinggou Formation.
(A and B) Scatter plot of cell length and cell width of Q. magnifica along with those of selected extant eukaryotic algae and filamentous bacteria. (B) Magnification of the dashed box in (A). (C) Scatter plot of maximum ratio of cell width to minimum cell width (CW/CWmin) within single filaments of Q. magnifica. Filament with constant width has ratio close to 1. Filament with ratio > 1.2 is interpreted with confidence as having varying width. Filaments with ratio in between represent transitional forms, here grouped with filaments having constant width, with consideration of taphonomic influence and measurement error. (D) Scatter plot of maximum ratio of cell length to minimum cell length (CL/CLmin) within single filaments of Q. magnifica. Note that a small number of specimens have ratio > 2, suggesting large variation in cell length within single filament. (E) Grouped floating bar chart showing ratios of CW/CWmin and CL/CLmin within single filaments of Q. magnifica and the selected extant eukaryotic algae and filamentous bacteria. Abbreviations of taxa are provided in the legend of (A). (F) Stacked column chart showing size-frequency distribution of Q. magnifica. Measurements and frequency data of Q. magnifica are provided in data S1. Size data of green algae Chaetomorpha and Urospora, cyanobacteria Oscillatoria, and sulfur bacteria Beggiatoa and Thioploca were measured from scaled illustrations in the literature and are provided in table S1 along with cited references.
Fig. 5.
Fig. 5.. Raman analyses of Q. magnifica and co-occurring cyanobacterial microfossils from the Chuanlinggou Formation.
(A) Representative Raman spectra of the first order region with baseline corrected and intensity normalized (from 0 to 1). (B) Box-and-whisker plot of peak metamorphic temperatures estimated by Raman parameters. T1 to T3 represent temperature calculated on the basis of Raman reflectance (33), FWHM-D1 and FWHM-D2 (34), respectively. Note that T1 (205° to 245°C) and T2 (206° to 251°C) highly overlap with each other across all analyzed specimens, representing reasonable estimates; whereas T3 (293° to 330°C) is far beyond the suggested temperature range (50° to 200°C) for this parameter (34), thus representing a problematic estimate. (C) Box-and-whisker plot of the intensity ratio of D to G peak (ID/IG). (D) Box-and-whisker plot of intensity ratio of D1 to G-function band (ID1/IG-function). (E) Box-and-whisker plot of intensity ratio of D2 to G-function band (ID2/IG-function). (F) Box-and-whisker plot of intensity ratio of D3 to G-function band (ID3/IG-function). (G) Box-and-whisker plot of intensity ratio of D4 to G-function band (ID4/IG-function). Analyzed specimens are illustrated in fig. S2. QIN, Q. magnifica; SIP, S. punctatum; PSEU, Pseudodendron sp.; OSCP, O. princeps. Source data are provided in data S2. a.u., arbitrary units.
Fig. 6.
Fig. 6.. Score plot for PCA of Q. magnifica and co-occurring cyanobacterial microfossils from the Chuanlinggou Formation.
Abbreviations of taxa correspond to those in Fig. 5. Source data are provided in data S2.
Fig. 7.
Fig. 7.. Representative FTIR spectra of Q. magnifica and co-occurring cyanobacterial microfossils from the Chuanlinggou Formation.
Spectra were baseline corrected and normalized in intensity from 0 to 1. The insert shows the aliphatic bands in the 3000 to 2800 cm−1 region. Band assignments and vibration modes (δ, deformation; ν, stretching; s, symmetric; as, asymmetric) are provided in table S2. Analyzed specimens are illustrated in fig. S2. Abbreviations of taxa correspond to those in Fig. 5. Source data are provided in data S2.
Fig. 8.
Fig. 8.. Overview of early evolution of the Eukarya along with fossil records.
(A) Simplified eukaryotic tree with divergence time estimates of major branches by molecular clock study. LECA, last eukaryotic common ancestor. Dashed gray lines represent hypothetical stem-group eukaryotes, which are extinct. Tree topology and molecular clock estimates are from (67). Abbreviation: Pha., Phanerozoic. (B) Representative fossil records of early eukaryotes. The oldest unambiguous eukaryotic fossils are unicellular forms, e.g., Tappania plana and Shuiyousphaeridium macroreticulatum from ~1650-Ma Ruyang Group [images courtesy of L. Yin, reprinted from (75) with permission from Elsevier]; Dictyosphaera macroreticulata, Germinosphaera alveolata, and Valeria lophostriata from the Changzhougou Formation and lowermost Chuanlinggou Formation in North China [reprinted from (76) with permission from Elsevier]. The Q. magnifica represents the current oldest convincing multicellular eukaryote from ~1635-Ma upper Chuanlinggou Formation in North China. The oldest red alga is Bangiomorpha pubescens from ~1050-Ma Hunting Formation, Canada [image courtesy of N. Butterfield, reprinted from (5) Cambridge Univ. Press, reproduced with permission]. The oldest green alga is P. antiquus from ~950-Ma Nanfen Formation in North China [image courtesy of Q. Tang, reprinted from (7) with permission from Springer Nature]. The oldest putative fungus is O. giraldae from ~890-Ma Grassy Bay Formation in Canada [image courtesy of C. Loron, reprinted from (8) with permission from Springer Nature]. The oldest amoebozoans are vase-shaped microfossils, e.g., Cycliocyrillium torquata from ~750 to 730 Ma Kwagunt Formation, Chuar group in Arizona [image courtesy of S. Porter, reprinted from (79) Cambridge Univ. Press, reproduced with permission]. Scale bars, 500 μm (the image of the oldest green algal fossil equals) and 50 μm (the rest).
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