Preservation of ~3.4–3.5 Ga microbial biomarkers in pillow lavas

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<ul><li><p>www.elsevier.com/locate/epsl</p><p>Earth and Planetary Science L</p><p>Preservation of ~3.43.5 Ga microbial biomarkers in pillow lavas</p><p>and hyaloclastites from the Barberton Greenstone Belt, South Africa</p><p>Neil R. Banerjee a,b,*, Harald Furnes a, Karlis Muehlenbachs b,</p><p>Hubert Staudigel c, Maarten de Wit d</p><p>a Department of Earth Science, University of Bergen, Allegt. 41, 5007 Bergen, Norwayb Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E3</p><p>c Scripps Institution of Oceanography, University of California, La Jolla, CA 92093-0225, USAd AEON and Department of Geological Sciences, University of Cape Town, Rondebosch 7701, South Africa</p><p>Received 11 April 2005; received in revised form 3 November 2005; accepted 4 November 2005</p><p>Available online 19 December 2005</p><p>Editor: H. Elderfield</p><p>Abstract</p><p>Exceptionally well-preserved pillow lavas and inter-pillow hyaloclastites from the Barberton Greenstone Belt in South Africa</p><p>contain textural, geochemical, and isotopic biomarkers indicative of microbially mediated alteration of basaltic glass in the</p><p>Archean. The textures are micrometer-scale tubular structures interpreted to have originally formed during microbial etching of</p><p>glass along fractures. Textures of similar size, morphology, and distribution have been attributed to microbial activity and are</p><p>commonly observed in the glassy margins of pillow lavas from in situ oceanic crust and young ophiolites. The tubes from the</p><p>Barberton Greenstone Belt were preserved by precipitation of fine-grained titanite during greenschist facies metamorphism</p><p>associated with seafloor hydrothermal alteration. The presence of organic carbon along the margins of the tubes and low d13Cvalues of bulk-rock carbonate in formerly glassy samples support a biogenic origin for the tubes. Overprinting relationships of</p><p>secondary minerals observed in thin section indicate the tubular structures are pre-metamorphic. Overlapping metamorphic and</p><p>igneous crystallization ages thus imply the microbes colonized these rocks 3.43.5 Ga. Although, the search for traces of early life</p><p>on Earth has recently intensified, research has largely been confined to sedimentary rocks. Subaqueous volcanic rocks represent a</p><p>new geological setting in the search for early life that may preserve a largely unexplored Archean biomass.</p><p>D 2005 Elsevier B.V. All rights reserved.</p><p>Keywords: early life; biomarker; volcanic glass; pillow lava; greenstone belt; Archean</p><p>1. Introduction</p><p>During the last decade several studies have shown</p><p>that the upper volcanic part of the modern oceanic crust</p><p>0012-821X/$ - see front matter D 2005 Elsevier B.V. All rights reserved.</p><p>doi:10.1016/j.epsl.2005.11.011</p><p>* Corresponding author. Present address: Department of Earth</p><p>Sciences, University of Western Ontario, London, Ontario, Canada</p><p>N6A 5B7.</p><p>E-mail address: neil.banerjee@gmail.com (N.R. Banerjee).</p><p>is a habitat for microorganisms. In this environment</p><p>microbes colonize fractures in the glassy selvages of</p><p>pillow lavas, extracting energy and/or nutrients from</p><p>the glass by dissolving it, leaving behind biomarkers</p><p>that reveal their former presence [112]. The biomar-</p><p>kers consist of (1) corrosion structures (commonly</p><p>filled by secondary minerals) that have textural criteria</p><p>indicative of a biogenic origin (size, morphology, dis-</p><p>tribution as populations), (2) enrichment of C, N, P, and</p><p>etters 241 (2006) 707722</p></li><li><p>N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707722708</p><p>S associated with the corrosion structures, (3) charac-</p><p>teristically low d13C values of disseminated carbonatewithin the altered glass rims of pillows compared to</p><p>their crystalline interiors, and (4) presence of DNA</p><p>associated with corrosion structures.</p><p>The methods developed for tracing biomarkers in</p><p>modern oceanic crust have been successfully applied to</p><p>pillow lava sections of ophiolites. The ophiolites inves-</p><p>tigated so far range in age from Cretaceous to Middle</p><p>Proterozoic, range in metamorphic grade from near</p><p>unmetamorphosed to lower amphibolite facies, and con-</p><p>tain all the principal components of a Penrose-type</p><p>ophiolite (summarized in [13]). Further, in a recent</p><p>study of pillow lavas of the ~3.23.5 Ga Barberton</p><p>Greenstone Belt (BGB) in South Africa, Furnes et al.</p><p>[14] reported biomarkers related to the initial alteration</p><p>of glassy pillow lava rims. Most products of biological</p><p>activity are too delicate to survive geological processes</p><p>like weathering, erosion, and dynamothermal-metamor-</p><p>phism. As such destructive processes compound through</p><p>geological time, it has proven to be increasingly difficult</p><p>to find preserved evidence for life as the age of a rock</p><p>approaches the age of the oldest rocks on Earth. Studies</p><p>of the earliest history of life are plagued also by pro-</p><p>blems of fossil preservation and poor and ambiguous</p><p>evidence for fossil material. In this paper we build upon</p><p>our previous work, present a new dataset of the biomar-</p><p>kers found in the volcanic rocks of the BGB, and stress</p><p>the importance of how the study of basaltic volcanic</p><p>rocks in Archean greenstone belts may contribute to the</p><p>discussion of the early life on Earth.</p><p>2. Basaltic glass as a geological setting for microbial</p><p>life</p><p>Biologically mediated corrosion of synthetic glass</p><p>is a well-known phenomenon [15] that has also been</p><p>proposed for the pitting of natural volcanic glass [16].</p><p>Thorseth et al. [17] first suggested that bio-corrosion</p><p>was produced by colonizing microbes that cause local</p><p>variations in pH which allows them to actively dis-</p><p>solve the natural basaltic glass substrates thereby pro-</p><p>ducing tubular structures. This process was later</p><p>verified in experiments [1820]. The microbial disso-</p><p>lution experiments by Thorseth et al. [18] showed that</p><p>etch marks on the basaltic glass surface were produced</p><p>after a relatively short time (46 days). The etch marks</p><p>produced were of uniform size (0.30.5 Am in diam-eter) and they had a chain or bcolonyQ shape, similarto the size and arrangement of the live bacteria that</p><p>were removed from the glass surface. Although we are</p><p>unaware of any experiment that has produced long</p><p>(several tens of micrometers) tubular structures, the</p><p>experiment by Thorseth et al. [18] demonstrates the</p><p>onset of a dissolution process. We suggest that given</p><p>enough time the etching process, ultimately might</p><p>produce the long tubular structures. Over the past</p><p>decade numerous studies have shown that microbe-</p><p>sized corrosion structures are commonly produced by</p><p>biological activity in natural basaltic glasses through-</p><p>out the upper few hundreds of meters of the oceanic</p><p>crust of any age, including the oldest oceanic crust in</p><p>the western Pacific Ocean [18,2,21,3,4,22,57,9,11,</p><p>10,23]. These structures are very distinct and cannot</p><p>be explained by abiotic processes, as supported by</p><p>evidence from petrography, geochemistry and molec-</p><p>ular biology.</p><p>Key petrographic arguments for a biogenic origin for</p><p>the corrosion structures include their size similarity to</p><p>microbes, their biotic morphology, and distribution as</p><p>populations. In particular, these structures commonly</p><p>occur as irregular tubes that consistently originate from</p><p>fractures. The structures are also observed to bifurcate</p><p>and never occur with a symmetric counterpart on the</p><p>other side of the fracture. Geochemical evidence</p><p>includes the common enrichment of biologically im-</p><p>portant elements such as C, N, P, K, and S associated</p><p>with the microbial alteration structures (e.g. [4,6,7,11])</p><p>and characteristically low d13C values of disseminatedcarbonate within microbially altered basaltic glass</p><p>[4,8,11]. Molecular arguments include the presence of</p><p>DNA associated with biological corrosion textures (e.g.</p><p>[21,4,11]). As to the timing of formation of microbial</p><p>alteration structures and subsequent filling of the struc-</p><p>tures, it is important to mention that we have found</p><p>filled tubules in the glassy rinds of Quaternary pillow</p><p>lavas (e.g. Fig. 3A of [8]). This shows that microbial</p><p>etching and subsequent filling of the empty structures</p><p>can be a penecontemporaneous process. In the absence</p><p>of abiotic explanations for these phenomena, microbial</p><p>etching is the most likely explanation for these petro-</p><p>graphic, geochemical, and biomolecular biomarkers in</p><p>the glassy margins of submarine lavas. The breadth of</p><p>these arguments and the abundance of these features</p><p>make it unlikely that microbial processes do not play an</p><p>important role during alteration of basaltic glass on the</p><p>present-day seafloor. Recent work by Lysnes et al. [24]</p><p>on the microbial community diversity in young (V1Ma) seafloor basalts has revealed eight main phyloge-</p><p>netic groups of Bacteria and one group of Archaea that</p><p>differ from those of the surrounding seawater including</p><p>autolitotrophic methanogens and iron reducing bacteria.</p><p>It should be stressed, however, that it has not yet been</p><p>possible to identify specific microbes or specific meta-</p></li><li><p>N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707722 709</p><p>bolic processes that cause the tubular corrosion struc-</p><p>tures described here.</p><p>3. Evidence for early life</p><p>The evidence for earliest life on Earth fall in three</p><p>main categories: chemical evidence (e.g., carbon isoto-</p><p>pic evidence), micro-morphological evidence (e.g., mi-</p><p>croscopic observation of microfossils), and macroscopic</p><p>interpretation of sedimentary structures preserved in the</p><p>rock record that are commonly associated with modern</p><p>microbial mats (e.g., stromatolites). The oldest proposed</p><p>evidence for life in the geological record traces back to</p><p>3.53.8 Ga and is based on chemical signatures in high-</p><p>grade schists and paragneisses of the Isua Supracrustal</p><p>Belt (ISB), Southwestern Greenland. Graphite from</p><p>these rocks and within apatite crystals has unusually</p><p>low d13C values indicative of biological fractionationof carbon [2530]. However, recent studies have pointed</p><p>out that low d13C values in at least some of the ISBgraphite occur in secondary carbonate veins and may</p><p>thus be also explained by abiotic processes, which brings</p><p>into question much of the evidence from Isua [3133].</p><p>In addition, reports of low d13C signatures fromgraphite inclusions in apatite crystals from ~3.85 Ga</p><p>granulite-facies rocks on Akilia island have also been</p><p>questioned [34]. However, the occurrence of low d13Csignatures in a sequence of graded metasediments inter-</p><p>preted as turbidites from the ISB [30], remains widely</p><p>accepted as biogenic and are thus possibly the oldest</p><p>chemical evidence of life on Earth.</p><p>The next-oldest evidence for life in the geological</p><p>record is based on micro-textural observations sup-</p><p>ported by laser-Raman imaging of features interpreted</p><p>as filamentous microfossils in ~3465 Ma metasedi-</p><p>ments (Apex chert) from the Pilbara Craton in South-</p><p>western Australia (e.g., [35,36]). However, Garcia-Ruiz</p><p>et al. [37] have recently shown that morphologically</p><p>similar filamentous microstructures can be generated</p><p>from abiotic processes. This specifically calls into ques-</p><p>tion the uniqueness of the biogenic interpretation for</p><p>the filaments in the Apex cherts. In addition, Brasier</p><p>et al. [38] interpreted the filamentous structures in the</p><p>Apex cherts as secondary artifacts consisting of amor-</p><p>phous graphite produced from inorganic synthesis or</p><p>organic compounds in hydrothermal veins. In contrast,</p><p>the 3472 and 3447 Ma low-grade metasediments (now</p><p>mostly cherts) from the middle and uppermost Onver-</p><p>wacht Groups of the BGB contain microstructures</p><p>and carbon isotope evidence for the presence of fos-</p><p>sil bacteria and biofilm [3941]. Nevertheless, there is</p><p>widespread skepticism for the biogenic nature of these</p><p>micromorphs (F. Westall, personal communication</p><p>2004).</p><p>These searches for early life in Greenland, Australia,</p><p>and South Africa show very clearly that geochemical or</p><p>morphological evidence for life is controversial and</p><p>underscores the need for more and better evidence for</p><p>Archean life in the oldest rock sequences. In this paper,</p><p>we describe textures and associated geochemical data in</p><p>formerly glassy pillow lavas, a suite of rocks that has</p><p>not been previously considered in the search for Arche-</p><p>an life. This new morphological and geochemical evi-</p><p>dence provide a consistent set of criteria for biogenicity</p><p>because it is firmly based on observations of a modern</p><p>analogue in oceanic basalts that has not been credibly</p><p>explained to form through abiotic processes. This ap-</p><p>proach offers an integrated data set that is substantially</p><p>more powerful than evidence based on a single data</p><p>type.</p><p>4. Geological background and sampling locations</p><p>The Mesoarchean BGB of South Africa contains</p><p>some of the worlds oldest and best-preserved pillow</p><p>lavas [42,43]. The magmatic sequence, consisting of</p><p>the Theespruit, Komati, Hooggenoeg, and Kromberg</p><p>Formations (the Onverwacht Group) comprises 56 km</p><p>of predominantly basaltic and komatiitic extrusive (pil-</p><p>low lavas, minor hyaloclastite breccias and sheet</p><p>flows) and intrusive rocks. This sequence is inter-</p><p>layered with cherts and is overlain by cherts, banded</p><p>iron formations (BIF) and shales of the Fig Tree and</p><p>Moodies Groups (Fig. 1). The Onverwacht Group has</p><p>been interpreted to represent fragments of Archean</p><p>oceanic crust, termed the Jamestown Ophiolite Com-</p><p>plex [42,44], that developed in association with sub-</p><p>duction and island arc activity approximately 3550 to</p><p>3220 Ma [4547]. The magmatic sequence of the</p><p>Onverwacht Group is exceptionally well-preserved,</p><p>relatively undeformed away from its margins with</p><p>the surrounding granitoids, and upwards from the mid-</p><p>dle to the upper part of the sequence the metamorphic</p><p>grade decreases from greenschist to prehnitepumpel-</p><p>lyite facies. Tectono-stratigraphically downward into</p><p>the Theespruit Formation and across a major shear</p><p>zone (the Komatii Fault), there is a rapid increase in</p><p>the metamorphic grade to higher pressurelower tem-</p><p>perature amphibolite facies concomitant with the de-</p><p>velopment of tectonic fabrics related to structural</p><p>emplacement (~3.4 Ga) and subsequent exhumation</p><p>(~3.2 Ga) of the BGB [46,48,49].</p><p>Well away from the margin of the greenstone belt,</p><p>about midway into the Komati Formation, 40Ar / 39Ar</p></li><li><p>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</p><p>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)</p><p>Reconstructed profile of the BGB showing the relative stratigraphic position of sampling sites. Samples listed in Table 1 are shown in bold.</p><p>Modified from [42].</p><p>N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707722710</p><p>step-heating analyses on amphiboles from serpenti-</p><p>nized komatiitic basalts give a metamorphic age of</p><p>3486F8 Ma [50]. This 40Ar / 39Ar age overlaps withan ~3482 Ma U/Pb date of magmatic zircon from an</p><p>interbedded airfall tuff in the same outcrop [51,52].</p><p>The overlapping metamorphic and igneous crystalliza-</p><p>tion ages, perfect preservation of fine igneous micro-</p><p>structure...</p></li></ul>