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. 2015 Apr 21;112(16):4859-64.
doi: 10.1073/pnas.1405338111.

Changing the picture of Earth's earliest fossils (3.5-1.9 Ga) with new approaches and new discoveries

Martin D Brasier  1 , Jonathan Antcliffe  2 , Martin Saunders  3 , David Wacey  4
Affiliations

Changing the picture of Earth's earliest fossils (3.5-1.9 Ga) with new approaches and new discoveries

Martin D Brasier et al. Proc Natl Acad Sci U S A. .

Abstract

New analytical approaches and discoveries are demanding fresh thinking about the early fossil record. The 1.88-Ga Gunflint chert provides an important benchmark for the analysis of early fossil preservation. High-resolution analysis of Gunflintia shows that microtaphonomy can help to resolve long-standing paleobiological questions. Novel 3D nanoscale reconstructions of the most ancient complex fossil Eosphaera reveal features hitherto unmatched in any crown-group microbe. While Eosphaera may preserve a symbiotic consortium, a stronger conclusion is that multicellular morphospace was differently occupied in the Paleoproterozoic. The 3.46-Ga Apex chert provides a test bed for claims of biogenicity of cell-like structures. Mapping plus focused ion beam milling combined with transmission electron microscopy data demonstrate that microfossil-like taxa, including species of Archaeoscillatoriopsis and Primaevifilum, are pseudofossils formed from vermiform phyllosilicate grains during hydrothermal alteration events. The 3.43-Ga Strelley Pool Formation shows that plausible early fossil candidates are turning up in unexpected environmental settings. Our data reveal how cellular clusters of unexpectedly large coccoids and tubular sheath-like envelopes were trapped between sand grains and entombed within coatings of dripstone beach-rock silica cement. These fossils come from Earth's earliest known intertidal to supratidal shoreline deposit, accumulated under aerated but oxygen poor conditions.

Keywords: astrobiology; biogeochemistry; early life; microfossils; paleontology.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Comparison of carbonaceous material between Precambrian microfossils and pseudofossils. (A−C) Microfossils from the 1.88-Ga Gunflint chert. (A) Eosphaera showing thin (ca. 100 nm) plausible outer cell membrane (o), thicker (ca. 200 nm) inner cyst-like sphere (i), plus part of a thin (<100 nm) tubercle cell membrane (t). (B) Huroniospora, a probable cyst showing a thick (ca. 500 nm) carbonaceous wall partly impregnated with silica crystals. (C) Gunflintia, a probable sheath showing a thick (maximum 500 nm) wall partially disrupted by silica crystal growth. (D) A probable sheath from the 3.43-Ga Strelley Pool Formation showing a thick (ca. 500 nm) wall partially disrupted by silica crystal growth. (E) Pseudofossil comparable to Primaevifilum spp. from the 3.46-Ga Apex chert, showing carbon (and closely associated iron) of variable thickness interleaved between aluminosilicate and quartz grains with no evidence for cellular architecture. Scale bar is 500 nm for the seven false color elemental maps in center of figure. Yellow, carbon; black, silica; red, aluminosilicate; green, iron. A−E obtained using FIB-SEM (A) and bright-field TEM (B−E); center false color elemental maps obtained using SEM–energy dispersive X-ray spectroscopy (maps from A) and energy-filtered TEM (maps from B−E). B–D are modified with permission from ref. .
Fig. 2.
Fig. 2.
Exceptional preservation and novel morphology of 1.88-Ga complex carbonaceous microfossil Eosphaera tyleri from the Gunflint chert, Schreiber Beach, Ontario. (A) Four levels of optical focus through a thin section in nonstromatolitic microfabric, showing a well-preserved Eosphaera complete with inner sphere (red arrow) and outer sphere (green arrow) plus several rounded tubercles (e.g., yellow arrow) within the intervallar space. (B−E) The 3D reconstructions (from FIB-SEM sequential slicing) of a different Eosphaera specimen (see Fig. S4). Note the thicker and more robust inner sphere (red, 20 μm across) with linear rupture (beneath white arrow), thinner and more membranous outer sphere (green, 30 μm across), and about 10 hollow, spherical to elliptical cell-like tubercles (various colors including yellow, 1–5.8 μm) plus two external tubercles (blue, <7 μm; pale green at left, 1.8 μm). (B and C) Viewed from center of specimen visualizing approximately half the organism; (D and E) Viewed from outside the specimen showing both inner and outer spheres (D) or just the inner sphere (E), plus tubercle locations. (Scale bar, 10 μm.)
Fig. 3.
Fig. 3.
Apex chert pseudofossil holotypes and paratypes (6), reimaged from the type thin sections (cf. 19), plus newly discovered comparable microstructures from sample CHIN-03. Archaeoscillatoriopsis disciformis holotype (A) plus comparable examples from CHIN-03 (B and C). Dashed box in A is the holotype as presented in ref. , although it was later found to be part of a larger microstructure wrapped around the edge of a rhombic mineral crystal (17). Primaevifilum delicatulum holotype (D) plus comparable examples from CHIN-03 (E and F). Archaeoscillatoriopsis grandis paratype (G) plus comparable examples from CHIN-03 (H and I). Primaevifilum attenuatum holotype (J) plus comparable examples from CHIN-03 (K and L). Note attenuation of trichomes toward apices, a feature that was erected as a defining characteristic of this species (6) (Table S1). Primaevifilum laticellulosum holotype (M) plus comparable examples from CHIN-03 (N and O). Note pillow-shaped terminal cells (arrows), a feature that was erected as a defining characteristic of this species (6) (Table S1). Primaevifilum conicoterminatum holotype (P) plus comparable examples from CHIN-03 (Q and R). Note conical terminal cells (arrows), a feature that was erected as a defining characteristic of this species (Table S1). (S−W) Examples of bifurcated cells and cell pairs (arrows) in the type thin sections (S and T) and CHIN-03 (U−W). Primaevifilum amoenum holotype (X) plus comparable examples from CHIN-03 (Y and Z). Thin black lines separate images taken at different focal depths. (Scale bar: 7 μm in W; 8 μm in B and E; 9 μm in I; 10 μm in O, U, V, Y, and Z; 12 μm in C, F, and N; 13 μm in D and G; 14 μm in A, J, L, M, P−T, and X; 16 μm in K; and 22 μm in H.
Fig. 4.
Fig. 4.
Nanoscale structure and chemistry of a pseudofossil comparable to Primaevifilum spp. from sample CHIN-03. Optical photomicrographs before (A) and after (B) extraction of an ultrathin wafer for analysis by TEM. Position of wafer indicated by red line in B. Thin black lines separate images taken at different focal depths. Bright-field TEM image (C) and corresponding energy-filtered TEM elemental maps of silicon (D), carbon (E), and aluminum (F) from the pseudofossil below the surface of the thin section. These show that the pseudofossil is almost entirely composed of platy aluminosilicate grains. Boundaries of the pseudofossil are indicated by dashed red lines in the TEM image and are marked by a clear transition from aluminosilicate to quartz (see Al and Si maps where brighter white colors equate to higher elemental concentrations). Carbon is abundant throughout the pseudofossil and is found in patches along quartz−aluminosilicate boundaries and interleaved between aluminosilicate grains within the pseudofossil. Carbon does not show any cell-like distribution. (G) False color three-element overlay showing carbon (yellow) and iron (green) interleaved between aluminosilicate (red). Patches of carbon and iron are also seen exterior to the pseudofossil at quartz grain boundaries (arrow).
Fig. 5.
Fig. 5.
Indigenous microfossils preserved within beach-rock dripstone microfabric in chertified quartz arenites of the 3.43-Ga Strelley Pool Formation, Western Australia. (A−D) Optical light micrographs of petrographic thin sections. (A) Chain of globular cells, preserved by enclosure within a microstalactite (see also Fig. S9). (B) Chain-like cluster of globular cells, here preserved within a thin chert lamina draped around a quartz grain (see also Fig. S7). (C) Isolated elliptical cells, here preserved within a chert-filled void between quartz grains. (D) Sheath-like tube preserved within a chert filled void between quartz grains (see also Fig. S8). (E−G) The 3D reconstructions of two cells from the same sample, using FIB-SEM sequential slicing. (E) Five successive stages of reconstruction of cell 1 (arrowed in C) showing a thin, hollow, crumpled wall of carbonaceous matter (green), pierced by holes from decomposition and silica growth. (F) Reconstruction of the silica-filled interior of the same cell (pale blue), showing potential external fold (arrow; unlike botryoidal silica). (G) Three views (partial, exterior, interior) of cell 2 from the same thin section, showing a thin, hollow, crumpled and pierced carbonaceous wall (purple). (Scale bar, 10 μm.)
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