3.4–3.5 Ga Microbial Biomarkers in Pillow Lavas and Hyaloclastites from the Barberton Greenstone Belt, South Africa

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Earth and Planetary Science Letters 241 (2006) 707–722 www.elsevier.com/locate/epsl

Preservation of ~3.4–3.5 Ga microbial biomarkers in pillow lavas and hyaloclastites from the Barberton Greenstone Belt, South Africa

Neil R. Banerjee a,b,*, Harald Furnes a, Karlis Muehlenbachs b, Hubert Staudigel c, Maarten de Wit d

a Department of Earth Science, University of Bergen, Allegt. 41, 5007 Bergen, Norway b Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E3 c Scripps Institution of Oceanography, University of California, La Jolla, CA 92093-0225, USA d AEON and Department of Geological Sciences, University of Cape Town, Rondebosch 7701, South Africa Received 11 April 2005; received in revised form 3 November 2005; accepted 4 November 2005 Available online 19 December 2005 Editor: H. Elderfield

Abstract

Exceptionally well-preserved pillow lavas and inter-pillow hyaloclastites from the Barberton Greenstone Belt in South Africa contain textural, geochemical, and isotopic biomarkers indicative of microbially mediated alteration of basaltic glass in the Archean. The textures are micrometer-scale tubular structures interpreted to have originally formed during microbial etching of glass along fractures. Textures of similar size, morphology, and distribution have been attributed to microbial activity and are commonly observed in the glassy margins of pillow lavas from in situ oceanic crust and young ophiolites. The tubes from the Barberton Greenstone Belt were preserved by precipitation of fine-grained titanite during greenschist facies metamorphism associated with seafloor hydrothermal alteration. The presence of organic carbon along the margins of the tubes and low d13C values of bulk-rock carbonate in formerly glassy samples support a biogenic origin for the tubes. Overprinting relationships of secondary minerals observed in thin section indicate the tubular structures are pre-metamorphic. Overlapping metamorphic and igneous crystallization ages thus imply the microbes colonized these rocks 3.4–3.5 Ga. Although, the search for traces of early life on Earth has recently intensified, research has largely been confined to sedimentary rocks. Subaqueous volcanic rocks represent a new geological setting in the search for early life that may preserve a largely unexplored Archean biomass. D 2005 Elsevier B.V. All rights reserved.

Keywords: early life; biomarker; volcanic glass; pillow lava; greenstone belt; Archean

1. Introduction is a habitat for microorganisms. In this environment microbes colonize fractures in the glassy selvages of During the last decade several studies have shown pillow lavas, extracting energy and/or nutrients from that the upper volcanic part of the modern oceanic crust the glass by dissolving it, leaving behind biomarkers that reveal their former presence [1–12]. The biomarkers consist of (1) corrosion structures (commonly * Corresponding author. Present address: Department of Earth Sciences, University of Western Ontario, London, Ontario, Canada filled by secondary minerals) that have textural criteria N6A 5B7. indicative of a biogenic origin (size, morphology, dis- E-mail address: [email protected] (N.R. Banerjee). tribution as populations), (2) enrichment of C, N, P, and

S associated with the corrosion structures, (3) charac- (several tens of micrometers) tubular structures, the teristically low d13C values of disseminated carbonate experiment by Thorseth et al. [18] demonstrates the within the altered glass rims of pillows compared to onset of a dissolution process. We suggest that given their crystalline interiors, and (4) presence of DNA enough time the etching process, ultimately might associated with corrosion structures. produce the long tubular structures. Over the past The methods developed for tracing biomarkers in decade numerous studies have shown that microbe- modern oceanic crust have been successfully applied to sized corrosion structures are commonly produced by pillow lava sections of ophiolites. The ophiolites inves- biological activity in natural basaltic glasses through- tigated so far range in age from Cretaceous to Middle out the upper few hundreds of meters of the oceanic Proterozoic, range in metamorphic grade from near crust of any age, including the oldest oceanic crust in unmetamorphosed to lower amphibolite facies, and con- the western Pacific Ocean [18,2,21,3,4,22,5–7,9,11, tain all the principal components of a Penrose-type 10,23]. These structures are very distinct and cannot ophiolite (summarized in [13]). Further, in a recent be explained by abiotic processes, as supported by study of pillow lavas of the ~3.2–3.5 Ga Barberton evidence from petrography, geochemistry and molec- Greenstone Belt (BGB) in South Africa, Furnes et al. ular biology. [14] reported biomarkers related to the initial alteration Key petrographic arguments for a biogenic origin for of glassy pillow lava rims. Most products of biological the corrosion structures include their size similarity to activity are too delicate to survive geological processes microbes, their biotic morphology, and distribution as like weathering, erosion, and dynamothermal-metamor- populations. In particular, these structures commonly phism. As such destructive processes compound through occur as irregular tubes that consistently originate from geological time, it has proven to be increasingly difficult fractures. The structures are also observed to bifurcate to find preserved evidence for life as the age of a rock and never occur with a symmetric counterpart on the approaches the age of the oldest rocks on Earth. Studies other side of the fracture. Geochemical evidence of the earliest history of life are plagued also by pro- includes the common enrichment of biologically im- blems of fossil preservation and poor and ambiguous portant elements such as C, N, P, K, and S associated evidence for fossil material. In this paper we build upon with the microbial alteration structures (e.g. [4,6,7,11]) our previous work, present a new dataset of the biomar- and characteristically low d13C values of disseminated kers found in the volcanic rocks of the BGB, and stress carbonate within microbially altered basaltic glass the importance of how the study of basaltic volcanic [4,8,11]. Molecular arguments include the presence of rocks in Archean greenstone belts may contribute to the DNA associated with biological corrosion textures (e.g. discussion of the early life on Earth. [21,4,11]). As to the timing of formation of microbial alteration structures and subsequent filling of the struc- 2. Basaltic glass as a geological setting for microbial tures, it is important to mention that we have found life filled tubules in the glassy rinds of Quaternary pillow lavas (e.g. Fig. 3A of [8]). This shows that microbial Biologically mediated corrosion of synthetic glass etching and subsequent filling of the empty structures is a well-known phenomenon [15] that has also been can be a penecontemporaneous process. In the absence proposed for the pitting of natural volcanic glass [16]. of abiotic explanations for these phenomena, microbial Thorseth et al. [17] first suggested that bio-corrosion etching is the most likely explanation for these petro- was produced by colonizing microbes that cause local graphic, geochemical, and biomolecular biomarkers in variations in pH which allows them to actively dis- the glassy margins of submarine lavas. The breadth of solve the natural basaltic glass substrates thereby pro- these arguments and the abundance of these features ducing tubular structures. This process was later make it unlikely that microbial processes do not play an verified in experiments [18–20]. The microbial disso- important role during alteration of basaltic glass on the lution experiments by Thorseth et al. [18] showed that present-day seafloor. Recent work by Lysnes et al. [24] etch marks on the basaltic glass surface were produced on the microbial community diversity in young (V1 after a relatively short time (46 days). The etch marks Ma) seafloor basalts has revealed eight main phyloge- produced were of uniform size (0.3–0.5 Am in diam- netic groups of Bacteria and one group of Archaea that eter) and they had a chain or bcolonyQ shape, similar differ from those of the surrounding seawater including to the size and arrangement of the live bacteria that autolitotrophic methanogens and iron reducing bacteria. were removed from the glass surface. Although we are It should be stressed, however, that it has not yet been unaware of any experiment that has produced long possible to identify specific microbes or specific meta- N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 709 bolic processes that cause the tubular corrosion struc- micromorphs (F. Westall, personal communication tures described here. 2004). These searches for early life in Greenland, Australia, 3. Evidence for early life and South Africa show very clearly that geochemical or morphological evidence for life is controversial and The evidence for earliest life on Earth fall in three underscores the need for more and better evidence for main categories: chemical evidence (e.g., carbon isoto- Archean life in the oldest rock sequences. In this paper, pic evidence), micro-morphological evidence (e.g., mi- we describe textures and associated geochemical data in croscopic observation of microfossils), and macroscopic formerly glassy pillow lavas, a suite of rocks that has interpretation of sedimentary structures preserved in the not been previously considered in the search for Arche- rock record that are commonly associated with modern an life. This new morphological and geochemical evi- microbial mats (e.g., stromatolites). The oldest proposed dence provide a consistent set of criteria for biogenicity evidence for life in the geological record traces back to because it is firmly based on observations of a modern 3.5–3.8 Ga and is based on chemical signatures in high- analogue in oceanic basalts that has not been credibly grade schists and paragneisses of the Isua Supracrustal explained to form through abiotic processes. This ap- Belt (ISB), Southwestern Greenland. Graphite from proach offers an integrated data set that is substantially these rocks and within apatite crystals has unusually more powerful than evidence based on a single data low d13C values indicative of biological fractionation type. of carbon [25–30]. However, recent studies have pointed out that low d13C values in at least some of the ISB 4. Geological background and sampling locations graphite occur in secondary carbonate veins and may thus be also explained by abiotic processes, which brings The Mesoarchean BGB of South Africa contains into question much of the evidence from Isua [31–33]. some of the world’s oldest and best-preserved pillow In addition, reports of low d13C signatures from lavas [42,43]. The magmatic sequence, consisting of graphite inclusions in apatite crystals from ~3.85 Ga the Theespruit, Komati, Hooggenoeg, and Kromberg granulite-facies rocks on Akilia island have also been Formations (the Onverwacht Group) comprises 5–6 km questioned [34]. However, the occurrence of low d13C of predominantly basaltic and komatiitic extrusive (pil- signatures in a sequence of graded metasediments inter- low lavas, minor hyaloclastite breccias and sheet preted as turbidites from the ISB [30], remains widely flows) and intrusive rocks. This sequence is inter- accepted as biogenic and are thus possibly the oldest layered with cherts and is overlain by cherts, banded chemical evidence of life on Earth. iron formations (BIF) and shales of the Fig Tree and The next-oldest evidence for life in the geological Moodies Groups (Fig. 1). The Onverwacht Group has record is based on micro-textural observations sup- been interpreted to represent fragments of Archean ported by laser-Raman imaging of features interpreted oceanic crust, termed the Jamestown Ophiolite Com- as filamentous microfossils in ~3465 Ma metasedi- plex [42,44], that developed in association with sub- ments (Apex chert) from the Pilbara Craton in South- duction and island arc activity approximately 3550 to western Australia (e.g., [35,36]). However, Garcia-Ruiz 3220 Ma [45–47]. The magmatic sequence of the et al. [37] have recently shown that morphologically Onverwacht Group is exceptionally well-preserved, similar filamentous microstructures can be generated relatively undeformed away from its margins with from abiotic processes. This specifically calls into ques- the surrounding granitoids, and upwards from the mid- tion the uniqueness of the biogenic interpretation for dle to the upper part of the sequence the metamorphic the filaments in the Apex cherts. In addition, Brasier grade decreases from greenschist to prehnite–pumpel- et al. [38] interpreted the filamentous structures in the lyite facies. Tectono-stratigraphically downward into Apex cherts as secondary artifacts consisting of amor- the Theespruit Formation and across a major shear phous graphite produced from inorganic synthesis or zone (the Komatii Fault), there is a rapid increase in organic compounds in hydrothermal veins. In contrast, the metamorphic grade to higher pressure–lower tem- the 3472 and 3447 Ma low-grade metasediments (now perature amphibolite facies concomitant with the de- mostly cherts) from the middle and uppermost Onver- velopment of tectonic fabrics related to structural wacht Groups of the BGB contain microstructures emplacement (~3.4 Ga) and subsequent exhumation and carbon isotope evidence for the presence of fos- (~3.2 Ga) of the BGB [46,48,49]. sil bacteria and biofilm [39–41]. Nevertheless, there is Well away from the margin of the greenstone belt, widespread skepticism for the biogenic nature of these about midway into the Komati Formation, 40Ar/ 39Ar 710 N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722

Fig. 1. (A) Location of the BGB and adjacent lithologies of South Africa. (B) Map of BGB showing location of study area. (C) Schematic map of study area within the BGB with location of sampling sites. Samples listed in Table 1 come from sites 3, 4, 6, 7, 10 and 11 (filled circles). (D) Reconstructed profile of the BGB showing the relative stratigraphic position of sampling sites. Samples listed in Table 1 are shown in bold. Modified from [42]. step-heating analyses on amphiboles from serpenti- structures such as spinifex tectures pseudomorphed by nized komatiitic basalts give a metamorphic age of metamorphic minerals, abundant pillow lavas, and 3486F8Ma[50]. This 40Ar/ 39Ar age overlaps with oxygen isotope stratigraphy through the sequence, an ~3482 Ma U/Pb date of magmatic zircon from an are taken as evidence that the metamorphism repre- interbedded airfall tuff in the same outcrop [51,52]. sents ocean-floor type hydrothermal alteration that The overlapping metamorphic and igneous crystalliza- occurred penecontemporaneously with igneous activity tion ages, perfect preservation of fine igneous micro- [53,42,54,44]. N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 711

Fig. 2. Examples of well preserved pillow lavas and interpillow hyaloclastite from the BGB. (A) Pillow lavas surrounded by hyaloclastite breccia from the upper part of the Hooggenoeg formation at location 6. Note the dark chilled margins (up to 2 cm thick). Field of view is ~1 m. (B) Vesicular pillow lavas from the lower part of the Kromberg Formation at location 7. Note the well developed dark chilled margins and excellent preservation of spherical vesicles and interpillow hyalocastite. Field of view is ~50 cm. (C) Pillow lavas and hyaloclastite breccias from the middle part of the Hooggenoeg Formation at location 5. Field of view is ~40 cm. (D) Well preserved pillow lavas and interpillow hyaloclastite from the upper part of the Hooggenoeg Formation at location 6. Field of view is ~80 cm.

We collected samples of pillow lava and interpillow Gamma Tech IMIX energy-dispersive spectrometer hyaloclastite from the best-exposed parts of the system. The analyses were performed at an accelerating Komati-, Hooggenoeg-, and Kromberg Formations voltage of 20 kV and a working distance of 15 mm. (Fig. 1). Pillow lavas were sampled from locations 3, Thin sections and grain mounts were sputter coated 4, 6, 7, 10 and 11 (Fig. 1). Individual pillows are highly with a thin film of iridium, approximately 40 A˚ thick variable with respect to size and vesicle density (Fig. 2). [11]. The pillow lavas invariably display a well-developed X-ray mapping on the same iridium-coated thin chilled margin (commonly 10 mm thick) grading in- sections was carried out with a JEOL JXA-8900R wards into a variolitic zone (5–10 mm thick), consisting electron microprobe at the University of Alberta, of a mixture of altered glass and microcrystalline ma- using an accelerating voltage of 15 kV, and a probe terial. Interpillow hyaloclastites were sampled from current of 3.0Â10À 8 A. Carbon and nitrogen peak locations 6 and 7 (Fig. 1). Hyaloclastite breccias are positions were determined using synthetic silicon car- confined to minor inter-pillow occurrences (Fig. 2). bide and boron nitride standards, respectively. Instru- ment calibration for all other elements was performed 5. Analytical methods on natural standards. Carbon was routinely measured on two different spectrometers to monitor the reproduc- Samples were first carefully trimmed with a saw and ibility of observed signals. the sawn surfaces ground to remove any trace of surface Stable C-isotope analyses of carbonates were per- contamination. Samples containing open fractures or formed by pouring 100% phosphoric acid on whole- pore spaces were avoided completely. No open pore rock powders under vacuum [55] and analyzing the spaces were observed in the sample collection as con- exsolved CO2 on a Finnegan MAT 252 mass spec- firmed by SEM and petrographic analysis. trometer at the University of Alberta. Yields of CO2 in Scanning electron microscopy (SEM) observations the samples varied from 0.011% to 19% by weight as were performed on a JEOL JSM-6301FXV instrument carbonate. The error in calculated carbonate yields at the University of Alberta connected to a Princeton range from ~F1% to ~F15% for samples rich and 712 N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722

Fig. 3. Healed fractures within pillow rims displaying irregular patches consisting of extremely fine-grained titanite (brown mineral in A–C). Extending from these titanite patches are mineralized tubular structures 1–10 Am in width and up to 200 Am in length (A and B=Sample 27C-BG- 03; C=Sample 29-BG-03). Detail of tubular structures within the white boxes in A and B are shown in the insets. Some of these tubular structures exhibit well-defined segmentation where they have been overprinted by the chlorite, indicating that they predate the alteration process (C). Modern microbial tubular structures in basaltic glass (from ODP sample 148-896A, 11R-01, 73–75) are shown for comparison (D). Note the similarity in size, shape, and distribution between the modern and ancient tubular textures.

Fig. 4. Tubular structures mineralized by titanite observed in samples of interpillow hyaloclastite (brownish-black mineral in A–C; Sample 27C-BG- 03). The structures in the interpillow hyaloclastite also have the same size, shape, and distribution as those shown in the pillow rims (Fig. 3). Modern microbial tubular structures (from DSDP sample 46-396B-20R-4, 112–122) are shown for comparison (D). Again note the similarity in size, shape, and distribution between the modern and ancient tubular textures. N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 713 poor in carbonate, respectively. The errors on isotopic analyses for carbon are better than F0.1x. The data are reported in the usual delta-notation with respect to VPDB for carbon [56,57].

6. Results

6.1. Transmitted light petrography

The outermost 10–20 mm of most pillows is defined by a dark zone that represents the chilled, originally glassy rim (Fig. 2). In many cases part of the glassy margin spalled off during pillow growth to form interpillow hyaloclastite (Fig. 2; see also [52]). Due to the pervasive greenschist facies metamorphic overprint, these rims now consist of very fine-grained chlorite with scattered grains of quartz, epidote, and amphibole. Within this originally glassy zone, there are healed fractures along which occur dense, irregular patches

Fig. 6. Individual glass shards in interpillow hyaloclastites also preserve fractures along which incipient alteration is observed (A). Areas of quartz along these fractures contain irregular patches of individual and/or coalesced spherical bodies mineralized by titanite that protrude away from the filled fracture (Sample 119-BG-04; inset A; B). The individual spherical bodies or patches are commonly 1–4 Amin diameter. These textures are similar to granular microbial alteration patterns observed at the interface between fresh glass and microbial alteration fronts in pillow basalts (from ODP sample 148-896A, 9R-1, 17–21) from in situ oceanic crust (C).

Fig. 5. Photomicrographs of well-preserved interpillow hyaloclastites. consisting of very fine-grained titanite (Fig. 3). The (A) Original glass shards are completely replaced by chlorite, quartz, and epidote and the interstitial spaces are filled with quartz and calcite development of these alteration features along fractures (Sample 119-BG-04). There is very little evidence of deformation and is irregular and non-symmetric. Extending from these preservation of original jigsaw breccia textures between individual titanite patches are mineralized tubular structures 1–10 glass shards is clearly visible in thin section. (B) Tubular structures Am in width (average 4 Am) and up to 200 Am in length mineralized by titanite are present both within the glass shards and (most commonly about 50 Am; Fig. 3). Some of these along the margins of the shards in the surrounding interstitial quartz (Sample 27C-BG-03). Inset shows interpretation of original margin of tubular structures exhibit well-defined segmentation. an individual glass along which numerous titanite tubules are now The segmentation results from the partial replacement located in quartz. of the titanite tubule by chlorite. Since the tubule pre- 714 N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 dated the chlorite formation they must have formed and also in hand specimen. Original glass shards are early in the alteration process (Fig. 3C). These struc- completely replaced by chlorite, quartz, and epidote tures have largely similar shape and size as tubular and the interstitial spaces are filled with quartz and textures found in glassy pillow rims of young pillow calcite. Tubular structures mineralized by titanite are lavas of in situ ocean crust (Fig. 3D). present both within the glass shards and along the The mineralized tubular structures are most com- margins of the shards in the surrounding interstitial mon and best developed in the interpillow hyaloclastite quartz (Fig. 5). The mineralized tubular structures in (Fig. 4) in the upper part of the Hooggenoeg Forma- the interpillow hyaloclastite also have the same size, tion (dated between 3472 and 3456 Ma; [45,46]; and shape, and distribution as those observed in the pillow de Wit, unpublished data). The interpillow hyaloclas- rims (Fig. 3). tite samples show no evidence of deformation and Individual glass shards in interpillow hyaloclastites preserve original jigsaw breccia textures with individ- also preserve fractures along which incipient alteration ual glass shards clearly visible in thin section (Fig. 5) is observed (Fig. 6A). These fractures contain patches

Fig. 7. Series of X-ray element maps (C, Ca, N, P, and Ti) and backscattered electron (BSE) images within the formerly glassy chilled pillow rim of Sample 29-BG-03 from location 6. Carbon 1 and Carbon 3 refer to carbon maps collected on spectrometers 1 and 3, respectively. The differences in the patterns observed in the two carbon maps are an artifact produced in samples that are not perfectly flat by the combination of the take off angle of the X-rays and the different physical orientation of the spectrometers on the microprobe (approximately 1508 apart). Slight differences in the spatial distribution of P and N are due to the same artifact. In the maps labeled C1+BSE and C2+BSE the carbon map has been superimposed on the BSE image showing the association of carbon with the margins of the tubular features. Increasing order of elemental abundance black–blue– green–yellow–red–pink. Scale bar is 20 Am. N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 715 of quartz along their length that host irregular patches of individual and/or coalesced spherical bodies mineralized by titanite that protrude away from the filled fracture (Fig. 6B). The individual spheres or patches are commonly 1–4 Am in diameter and resemble microbial alteration patterns observed at the interface between fresh glass and microbial alteration fronts observed in basaltic glass from in situ oceanic crust (Fig. 6C) (e.g., [5,8,11]).

6.2. Element mapping

X-ray element maps collected by electron microprobe on iridium-coated thin sections show elevated levels of carbon, and possibly nitrogen and phosphorus, associated with the mineralized tubular features (Fig. 7). SEM images of the area mapped in Fig. 7 clearly show the tubules extending away from a healed fracture (Fig. 8A and B). A transmitted light photomicrograph of the tubules mapped in Fig. 7 is shown in Fig. 8C. The observed enrichments are highly re- stricted to the margins of the mineralized tubes and diminish sharply away from these areas. Although the intensity of the carbon signal observed in Fig. 7 represents a qualitative indication of the amount of carbon present and does vary, elevated levels of carbon are observed in several samples where mineralized tubes occur. Element maps for calcium, magnesium, iron, aluminum, sodium, potassium, silicon, sulfur, chlorine, and titanium were also routinely produced. Most of Fig. 8. SEM–BSE images and transmitted light photomicrograph of these elements do not show enrichments and argue area mapped in Fig. 7 from Sample 29-BG-03. (A) BSE image clearly against the possibility that carbon highs are due to shows a healed fracture trending from upper left to bottom right of the inorganic carbonate material (e.g., Ca, Mg, Fe) or image cutting the formerly glassy margin now replaced by predomi- epoxy (e.g., Cl). nantly quartz and chlorite. Two titanite patches (light gray material) with mineralized tubules extend away from the healed fracture. Area in box is shown in B. Scale bar is 100 Am. (B) Detailed BSE image of 6.3. Carbon isotopes titanite tubules mapped in Fig. 7 (area in box). The healed fracture is clearly visible at the center of the titanite patch. Scale bar is 50 Am. A series of sub-samples from the outermost glassy (C) Transmitted light photomicrograph of titanite tubules mapped in rims and crystalline interiors of individual pillow lavas Fig. 7 (area in box). This image clearly shows the titanite tubules are connected to the main titanite patch below the surface and are not were carefully prepared. The bulk-rock carbonate from isolated grains. The apparently isolated nature of some tubules in the the bglassyQ and bcrystallineQ sub-samples was ana- BSE images is an artifact of the thin section making process. Scale bar lyzed for carbon isotope ratios in order to investigate is 50 Am. if there was any indication of biological fractionation. The results are given in Table 1 and Fig. 9. No trend with depth within the stratigraphic sequence or corre- than the crystalline interiors of pillow lavas (+0.7x lation between isotope ratio and carbonate abundance to À6.9x). Secondary carbonate in vesicles has d13C is observed. values that cluster near zero. The d13C values from Carbon-isotope analyses of disseminated carbonate the crystalline pillow lava interiors are bracketed in formerly glassy pillow rims and interpillow hyalo- between primary mantle CO2 (À5x to À7x; clastites, in which there are textural and geochemical [58,59]) and values close to marine carbonates (0x; evidence for microbial activity, display a significantly [59,60]). This distribution is very similar to that greater range in the d13C values (+3.9x to À16.4x) observed in studies of ophiolites (Fig. 9B) and in 716 N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722

Table 1 Table 1 (continued) Carbon isotope analyses of disseminated carbonates Sample wt.% carb d13C Sample wt.% carb d13C Glassy samples Glassy samples 59A-BG-03 0.019 À2 P1A-02 1.253 À0.3 59B-BG-03 0.025 À6.9 P1A-02 1.261 1.8 60A-BG-03 0.015 À5.4 P1A-02 0.016 À5.7 60B-BG-03 0.031 À4.3 P1A-02 1.322 0.1 P1A-02 0.02 À3.5 Crystalline samples P1A-02 3.453 0.4 P1A-02 0.944 À0.1 P1A-02 0.765 0.3 P1A-02 1.989 0.7 P1B-02 0.054 À2.6 P1A-02 3.538 0.6 P1B-02 2.4 3.9 P1B-02 0.7 À0.1 P1B-02 0.057 À1.9 P1B-02 5.501 0.1 P2B-02 0.025 À12.7 P1B-02 2.555 0.5 P2B-02 0.035 À3.4 P1B-02 18.287 0.7 P2B-02 0.037 À4 P1B-02 4.211 0.6 P2B-02 0.019 À9.7 P1B-02 4.306 0.6 P2B-02 0.02 À7.1 P2B-02 0.42 0 P2B-02 0.03 À6.6 P2B-02 0.03 À6.1 PB3-02 0.027 À16.7 PB3-02 0.332 À1.1 PB3-02 0.967 0.3 PB3-02 0.287 0.4 PB3-02 0.011 À1.2 PB3-02 0.45 0 PB3-02 0.016 À15.6 8B-BG-03 0.377 À1.8 PB3-02 0.99 0.4 10B-BG-03 0.152 À1.6 PB3-02 0.81 0.5 13B-BG-03 0.664 À0.4 PB3-02 1.08 0.3 15B-BG-03 0.053 À1.9 8A-BG-03 0.756 À1.1 25-BG-03 5.264 À1.4 9A-BG-03 0.03 À4.4 31-BG-03 0.289 À1.6 12A-BG-03 2.336 3 34-BG-03 3.529 À0.5 14A-BG-03 4.372 0.3 37D-BG-03 1.037 À1.1 17A-BG-03 0.04 À4.2 37E-BG-03 5.903 À0.5 17B-BG-03 0.042 À5.7 39D-BG-03 0.018 À2.4 24-BG-03 2.219 À0.1 39E-BG-03 3.232 À0.9 26-BG-03 0.018 À5.1 39F-BG-03 0.997 À0.9 29-BG-03 5.327 À4.8 39G-BG-03 1.208 À6.5 30B-BG-03 0.027 À6.1 40E-BG-03 0.022 À2.6 33-BG-03 0.033 À3.3 40F-BG-03 0.013 À6.6 37A-BG-03 0.045 À6.9 43E-BG-03 0.779 À6.4 37B-BG-03 0.035 À5.2 58C-BG-03 0.049 À5 38-BG-03 0.014 À7.1 59C-BG-03 0.037 À5.9 39A-BG-03 0.039 À5.2 59D-BG-03 0.052 À5.4 39B-BG-03 0.035 À9.4 60C-BG-03 0.039 À6.5 39C-BG-03 0.035 À6 40A-BG-03 0.031 À7.9 Vesicles 40B-BG-03 0.038 À1.6 P1A-02 15.414 0.7 40C-BG-03 0.053 À3.7 P1B-02 19.094 0.5 40D-BG-03 0.015 À5.8 PB3-02 2.878 0.5 41A-BG-03 0.027 À5.9 wt.% carb=weight percentage carbonate. Samples listed come from 41B-BG-03 0.03 À7 the following sites: Site 3=06 to 08-BG-03; Site 4=09 to 20-BG-03; 41C-BG-03 0.029 À9.1 Site 6=24 to 29-BG-03; Site 7=30 to 46-BG-03; Site 10=56 to 58- 41D-BG-03 0.025 À4.4 BG-03; and Site 11=59 to 60-BG-03. All samples listed as Pxx-02 42A-BG-03 0.025 À5.8 were collected at Site 7. 42B-BG-03 0.018 À11.3 43A-BG-03 0.019 À8.1 43B-BG-03 0.011 À8.4 43C-BG-03 0.054 À9 situ oceanic crust (Fig. 9C). The observed shift to 56-BG-03 0.05 À8.8 lower d13C values of disseminated carbonates in the 57-BG-03 0.065 À6.5 outer glassy rim of pillow lavas is a pattern that is 58A-BG-03 0.071 À1.5 interpreted to result from microbial fractionation 58B-BG-03 0.106 À1.6 [7,61,62,13,11,14,63]. N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 717

7. Discussion

It is perhaps surprising to find that evidence for early life has come from igneous rather than sedimentary rocks, which to date have been the only Archean rocks subjected to close scrutiny for signs of early life. The granular and tubular structures reported here from the pillow rims and interpillow hyaloclastite of the Hooggenoeg and Krom- berg Formations are interpreted as the mineralized remains of microbial borings in previously glassy rocks. Those familiar with early accounts of microscopic tubular quartz or iron-carbonate pseudofossil trails extending from minute pyrite grains observed in Precambrian organic rich cherts (i.e., [64]) may initially attach some similarity to the tubular structures in the present study. These

Fig. 10. Comparison of tubular structure diameters in the BGB samples with tubular microbial alteration textures in modern oceanic crust. The mineralized structures in BGB samples are similar in size but generally slightly larger than microbial alteration textures in fresh oceanic basaltic glass.

structures, termed ambient inclusion trails, are interpreted to form by pressure solution initiated by gas evolution from organic material that drives minute mineral grains (commonly pyrite) through the chert matrix [65,66]. These trails commonly display spectacular morphologies with straight, curved, coiled, and pseudo- branching patterns having been observed [65,66]. These complex tubular morphologies were originally misinter- preted by Gruner [64] as bmicrofossilsQ but were later shown to form through abiotic pressure solution [65,66]. Although ambient inclusion trail can also be caused by minerals such as titanite or magnetite, the BGB tubules are mineralized by titanite, not associated with mineral grains at their tips, and do not occur in organic-rich cherts, which are necessary requirements for this process to occur [65,66]. For these reasons it is unlikely that the tubular structures in the formerly glassy BGB rocks formed by a similar pressure-solution process.

7.1. Textural evidence for microbial alteration of the BGB lavas

The tubular and granular structures from both the pillow rims and interpillow hyaloclastites are compara- ble in size, shape, and distribution to microbial alter- Fig. 9. Relationship between weight percent carbonate versus d13C for ation features reported from glassy rims in pillow lavas the originally glassy rims (filled circles) and crystalline interiors (open from the Troodos ophiolite ([61]; Fig. 3A and B), and squares) of pillow lavas. (A) Analyses from pillow lavas of the Komati, Hooggenoeg, and Kromberg Formations of the Onverwacht Group, basaltic glass from in situ oceanic crust [18,2,21,3– BGB. (B) Compilation of analyses from ophiolites worldwide [13,63]. 7,9,11,10] (Fig. 3C and D). Fig. 10 compares the (C) Compilation of analyses from modern oceanic crust [7,8,11]. diameter of tubular structures in the BGB samples 718 N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 with the diameter of tubular microbial alteration fea- cess found in basaltic glass from the modern seafloor tures in modern oceanic crust. The observed distribu- suggests that endolithic microbes may have been an tion shows that on average the mineralized structures early form of life on Earth. found in the formerly glassy BGB samples are slightly larger than predominantly unfilled microbial alteration 7.3. Interpretation of carbon isotopes features in fresh oceanic basaltic glass. This can be explained if the mineralized structures found in the Disseminated carbonate in the relic glassy rocks from BGB samples were once empty corrosion structures the BGB is lower in d13C on average (À4.6x) than in because it would be impossible for a mineralized tube crystalline rocks (À2.1x). The crystalline interior sam- to be smaller than the original channel it subsequently ples all display d13C values bracketed between Archean filled. Additionally, they may have become thicker by marine seawater (~0F2x; [60]) and primary mantle metamorphic growth. The shape and distribution of the CO2 (À5x to À7x; [59,58]). The relic glassy samples tubular and granular structures along healed micro also extend to much lower d13C values (À16.7x) than fractures in the BGB lavas is identical to those found the crystalline rocks (À6.9x). The lowest d13C values in modern oceanic basalts (Figs. 3D, 4D, 6C). occur in relic glassy samples with very low carbonate abundances (V0.054 wt.%). Such isotopic contrasts 7.2. Element distributions have been documented in pillow lava rims from Phan- erozoic and Proterozoic ophiolites (Fig. 9B) and recent The presence of carbon along the margins of the oceanic crust (Fig. 9C). The generally low d13C values of titanite tubules in the BGB samples unrelated to carbo- disseminated carbonate are attributed to metabolic by- nates is interpreted to represent residual organic matter products formed during microbial oxidation of dissolved [14]. The common association of carbon, and to a lesser organic matter from pore waters [7,11,13,63]. Two relic extent nitrogen and phosphorus, with suspected micro- glassy samples from the BGB with relatively high car- bial alteration textures and not elsewhere is a common bonate contents (N2 wt.%), have d13C values (3.0x and observation in basaltic glasses from modern oceanic 3.9x) above those expected for seawater carbonate crust and ophiolites affected by microbial alteration (Table 1; Fig. 9A). These high carbonate contents (e.g., [7,11]). The association of carbon and nitrogen argue against a seawater fingerprint and are likely the with the mineralized tubes argues for a biological origin result of an outside, possibly later, source of inorgani- because abundances of these elements in igneous and cally precipitated carbonate. metamorphic rocks are commonly low. Our interpreta- Prior to alteration and metamorphism all the basaltic tion is that these elements were most likely concentrated samples would have had initial magmatic d13C values from seawater by microbes that colonized the originally in the range of À5x to À7x [58,59]. Abiotic inter- glassy surfaces. As the microbes dissolved the glass, action with seawater would have introduced inorgani- multiplied, and died, organic remains containing carbon cally precipitated marine carbonate with d13C values and nitrogen were left behind within the alteration close to zero [58,60]. Based on these starting conditions textures produced. These organic remnants were then we can make some predictions regarding the observed later trapped along the margins of the tubes as they distribution of d13C values in the glassy and crystalline became mineralized by titanite, resulting in the elevated samples. Forty-seven of the 63 relic glassy samples, all signals observed. Conversely, phosphorous would have of the crystalline samples, and all of the vesicle fillings been present in the glass matrix but likely in very low have d13C values between À7x and 2x. These values concentrations relative to seawater. It is uncertain if are best explained as being derived from some combi- the microbes are able to extract P from the glass during nation of carbonate inorganically precipitated from sea- dissolution but element maps show elevated concentra- water and magmatic CO2 values [7,11,13,63]. tions of P in microbial alteration textures, likely due to In contrast, the samples with d13C values lower than incorporation in cells. À7x most likely contain an amagmatic carbon com- The metabolic requirements of microbes responsible ponent with low d13C. The low d13C values of carbon- for alteration of basaltic glass in modern samples have ate in the relic glassy BGB samples, particularly those not been determined. It is thought that elements in the samples that contain low abundances of carbonate and glass such as iron act as nutrients sought by the d13C valuesbÀ7x, are interpreted to be the result of microbes and are released during glass dissolution. microbial fractionation. If the proportion of inorgani- The possibility that the titanite tubules in the BGB cally precipitated calcite (with d13C near 0x) exceeds samples represent vestiges of the same microbial pro- that resulting from precipitation of carbonate from N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 719

microbially produced CO2 during oxidation of organic gated the overprinting relationships between the tubular carbon, the d13C value of a sample may be greater than structures and the metamorphic mineral growth. Chlo- À7x. This is commonly seen for samples that are rite is the predominant mineral in the originally glassy relatively rich in carbonate (Fig. 9A; Table 1). margin of the pillows, and is observed to overgrow the The carbon isotope signatures are unlikely to be the titaniferous tubular structures and thus obliterate them result of some later carbonate formation, more recent in some samples. In other samples fine chlorite has extraneous respired organic matter, or a Rayleigh frac- caused the tubular structures to take on a segmented tionation of 13C/12C associated with decarbonation character by partly overgrowing them (Fig. 3C). These reactions. If the observed d13C values were due to petrographic observations indicate that the tubular deposition of carbonate (such as from more recent structures are pre-metamorphic. Previous 40Ar/ 39Ar fluid flow) unrelated to biological activity in the glassy step-heating analyses of komatiitic basalts from the margin, there is no reason that the pillow margins Komati Formation give metamorphic ages of should be different from the pillow interiors. Instead, 3486F8Ma[50]. The 40Ar/ 39Ar ages overlap with one would expect a homogenization of the isotope data the igneous U/Pb ages of the Onverwacht Group [50– which is clearly not observed (Fig. 9A). It is also 52]. This is taken as evidence that the metamorphism difficult to explain why extraneous respired organic represents ocean-floor type hydrothermal alteration that matter would preferentially affect the pillow rims occurred soon after the crust was formed [42,54,44]. since these would have devitrified early in the alteration process through replacement by secondary minerals. 7.5. Preservation of microbial alteration textures in the This is confirmed by independent petrographic evi- rock record dence that demonstrates alteration occurred soon after eruption of the pillow lavas (Fig. 3C; see Section 7.4). The mineralization of tubular microbial alteration Because the metamorphism occurred early in the histo- textures in the BGB samples by titanite is not a unique ry of these rocks there would have been no mineralogic occurrence. It is well known from studies of recent (i.e., different assemblage) or textural (i.e., glass versus oceanic basaltic glass that titanium can be passively mineral) advantages for respired organic matter to be accumulated during etching of the glass by microbes deposited in the pillow margins preferentially over the (e.g., [11]). This process preferentially concentrates crystalline interiors since the time of initial alteration. In titanium in the channels produced by the microbes. addition, if the isotopic signatures observed were a Titanium enrichments in tubular microbial textures are result of decarbonation reactions one would expect to also observed in the glassy pillow margins of ophiolitic see a correlation between weight percent carbonate and rocks. In samples from the Jurassic Mirdita ophiolite d13C value that fits a Rayleigh fractionation curve. (Albania) and the Stonyford Volcanics (California), Instead, we observe no correlation over the d13C zeolite facies alteration has begun to replace the glass range from À17x to 0x at low carbonate abundances (Banerjee unpublished data). In these samples open or (b0.1 wt.%; Fig. 9A). At relatively high carbonate clay-filled tubular structures within the glass are min- contents (above ~0.1 wt.%) there is again no trend eralized by titanite as they pass into the zone of zeolite observed and the d13C values typically fall within the alteration. This direct link between open or clay-filled range of magmatic (À7x to À5x) and Archean ma- tubes with titanite-filled tubes suggests that the miner- rine carbonate values (~0x). Hence we consider it alization process follows a step-wise sequence during unlikely that Rayleigh fractionation, a process that progressive alteration conditions (Banerjee unpublished may fractionate carbon isotope ratios during basalt data). The formation of titanite is thus an early process degassing and subsequent alteration [59], is responsible that occurs at relatively low temperatures and this for the pronounced spread in the d13C values of the mineralization process is essential if the microbially glassy components. Instead, the d13C pattern observed produced structures are to be preserved for extended in the Barberton pillow lavas (Fig. 9A) is best inter- periods of geological time. preted as resulting from similar processes observed in recent oceanic crust and ophiolites [7,11,13,63]. 8. Concluding remarks

7.4. Timing of microbial alteration Evidence for microbial alteration of relic glassy basaltic rocks in the Archean BGB is widespead in The question remains as to when the microbial the former glassy margins of pillows and interstitial activity occurred. To address this question we investi- hyaloclastites. The integrated observations suggest that 720 N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722 these features are the result of microbial activity and [2] H. Furnes, I.H. Thorseth, O. Tumyr, T. Torsvik, M.R. Fisk, that this microbial colonization of the glassy basaltic Microbial activity in the alteration of glass from pillow lavas from Hole 896A, in: J.C. Alt, H. Kinoshita, L.B. Stokking, P.J. rocks took place soon after eruption of the ~3.4–3.5 Michael (Eds.), Proc. ODP, Sci. Results, vol. 148, Ocean Dril- Ga pillow lavas. During the last decade there has been ling Program, College Station, TX, 1996, pp. 191–206. an intense search for traces of early life on Earth. This [3] M.R. Fisk, S.J. Giovannoni, I.H. Thorseth, The extent of micro- search has largely been confined to sedimentary rocks, bial life in the volcanic crust of the ocean basins, Science 281 or rocks interpreted to represent sediments. The search (1998) 978–979. [4] T. Torsvik, H. Furnes, K. Muehlenbachs, I.H. Thorseth, O. for traces of early life is difficult and purported bio- Tumyr, Evidence for microbial activity at the glass–alteration markers found in Archean metasediments, either in the interface in oceanic basalts, Earth Planet. Sci. Lett. 162 (1998) form of microfossils or as chemical and isotopic tra- 165–176. cers, have been questioned (e.g., [38,31,37,34]). Our [5] H. Furnes, H. Staudigel, Biological mediation in ocean crust claim of ~3.5 Ga traces of life in the originally glassy alteration: how deep is the deep biosphere? Earth Planet. Sci. Lett. 166 (1999) 97–103. selvages of pillow lavas and inter-pillow hyalocastites [6] H. Furnes, K. Muehlenbachs, O. Tumyr, T. Torsvik, I.H. Thor- is a new geological setting in the search for early life. seth, Depth of active bio-alteration in the ocean crust: Costa Rica Indeed, the birthplace of life may have been connected Rift (Hole 504B), Terra Nova 11 (1999) 228–233. to the volcanic environment of the oceanic crust, such [7] H. Furnes, H. Staudigel, I.H. Thorseth, T. Torsvik, K. Muehlen- as deep-sea hydrothermal vents (e.g., [67]). Pillow bachs, O. Tumyr, Bioalteration of basaltic glass in the oceanic crust, Geochem. Geophys. Geosyst. 2 (2001) (2000GC000150). lavas are the most common rock sequences in Archean [8] H. Furnes, K. Muehlenbachs, T. Torsvik, I.H. Thorseth, O. greenstone belts [68]. 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