Metabolically diverse primordial microbial communities in Earth's oldest seafloor-hydrothermal jasper

Abstract

The oldest putative fossils occur as hematite filaments and tubes in jasper-carbonate banded iron formations from the 4280- to 3750-Ma Nuvvuagittuq Supracrustal Belt, Québec. If biological in origin, these filaments might have affinities with modern descendants; however, if abiotic, they could indicate complex prebiotic forms on early Earth. Here, we report images of centimeter-size, autochthonous hematite filaments that are pectinate-branching, parallel-aligned, undulated, and containing Fe²⁺-oxides. These microstructures are considered microfossils because of their mineral associations and resemblance to younger microfossils, modern Fe-bacteria from hydrothermal environments, and the experimental products of heated Fe-oxidizing bacteria. Additional clusters of irregular hematite ellipsoids could reflect abiotic processes of silicification, producing similar structures and thus yielding an uncertain origin. Millimeter-sized chalcopyrite grains within the jasper-carbonate rocks have ³⁴S- and ³³S-enrichments consistent with microbial S-disproportionation and an O₂-poor atmosphere. Collectively, the observations suggest a diverse microbial ecosystem on the primordial Earth that may be common on other planetary bodies, including Mars.

Fig. 1.. Hematite filaments and spheroids in NSB jasper-carbonate BIF.

(A) Transmitted light image of a bundles of pectinate-branching hematite filaments with undulations and tubes and co-occurring clusters of irregular ellipsoids. (B) Corresponding interpretive drawing showing straight filaments (blue lines), undulated or coiled filaments (red lines), tubes (orange lines), rosettes (purple circles), clusters of irregular ellipsoids (green ovals), and areas for other figure panels and videos. The four photos in inset show four examples of branching filament intersections in this structure. (C) Cluster of irregular ellipsoids inside a coarse quartz granule rimmed by two undulated filaments (red arrows). (D) Parallel-aligned hematite filaments and associated irregular ellipsoids. (E) Raman image showing a filament with coarse Fe²⁺-bearing hematite (yellow) and hematite (purple) (spectra shown in fig. S4N). (F) BSE image of a cross-sectioned undulated filament (shown in fig. S4K) with graphitic carbon (white arrows) associated with ferrous hematite (yellow contour) and quartz inclusions (blue arrows). (G) Histogram of the sizes of the irregular ellipsoids (average of major and minor axes).

Fig. 2.. Petrography of outsized calcite and chalcopyrite in jasper-carbonate BIF.

(A and B) Visually correlated Raman-SEM (scanning electron microscopy) images (in BSEs) of criss-crossing millimeter-size calcite laths with a recrystallized texture of collapsed rosettes with apatite inclusions (white circles) (PC0822). Colors in the micro-Raman images are as follows: blue for quartz, green for carbonate, purple for hematite, and turquoise for apatite. (C and D) Outsized subhedral chalcopyrite crystals with ³⁴S- and ³³S-enrichments (spot analyses shown as small red dots and averages with one SD specified), associated with magnetite (PC0824). The chalcopyrite in PC0844 has inclusions of (E) apatite-quartz in direct contact with galena and (F) of micrometer-size euhedral to anhedral galena (white), including with selenium enrichments as shown in spectrum in inset and in (G) table of three energy-dispersive spectroscopic analyses.

Fig. 3.. Trace element and rare earth element plots for NSB Fe-silicate BIF and jasper-carbonate BIF.

(A) Trace metals and phosphorus profile for NSB BIF (red is jasper-carbonate BIF and blue is Fe-silicate BIF) compared to Dales Gorge average [green; data from (62)]. New data are shown in table S1. (B) REE plots of hydrothermal sedimentary rocks of the NSB; data are from this study (table S1) and (93), normalized to average post-Archean Australian shale [PAAS; (99)]. (C) For comparison, Archean hydrothermal jasper and Fe-rich chert; data are from (53), (84), and (85).

Fig. 4.. Three sulfur isotope plot for NSB sulfide minerals based on NanoSIMS and EA-IRMS analyses.

Chalcopyrite in the jasper-carbonate BIF (red triangles) compared to pyrite and pyrrhotite in the Fe-silicate BIF (blue squares). Filled symbols are NanoSIMS spot analyses; open symbols are IRMS analyses of drilled powders. Comparison with other sulfur isotope compositions from NSB Fe-silicate BIF is shown. Detailed data are shown in the Supplementary Materials, and the data with green open squares and purple filled squares are from (23) and (24).

Fig. 5.. Illustrative model for the inferred origin of microfossils in NSB jasper-carbonate BIF.

(A) Metabolizing, organic-poor, pectinate-branching filaments of ferrihydrite with symbiotic colonies of irregular ellipsoids (red circles). (B) Postmortem colloidal silica (gray) precipitation on filaments and spheroids. (C) Ferrihydrite (red dots) coats the silica-permineralized filaments, forming parallel-aligned tubular structures, and onset of biomass oxidation in the siliceous ooze. (D) Early diagenetic nonequilibrium reactions of Liesegang diffusion of Fe-oxides form sedimentary layers, and chemically oscillating reactions during biomass oxidation produce jasper nodules and granules around microfossil colonies as well as hematite and carbonate rosettes (purple circles). (E) Decreased alkalinity during these reactions leads to quartz lithification and to the precipitation of micrometer-size carbonate (green), apatite (turquoise), hematite, and magnetite (black). (F and G) Prograde metamorphism leads to the formation of coarse-grained submillimeter carbonate, apatite, chalcopyrite (yellow), quartz, and magnetite (black), which blurs and partly deforms original textures and filaments. (H) Later retrograde metamorphism causes apatite to open and leak Pb, which forms galena in contact with apatite inside chalcopyrite, rendering U-Pb ages inconsistent with the age of the rock.