Comparing petrographic signatures of bioalteration in recent to Mesoarchean pillow lavas: Tracing subsurface life in oceanic igneous rocks

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1 Precambrian Research 158 (2007) Comparing petrographic signatures of bioalteration in recent to Mesoarchean pillow lavas: Tracing subsurface life in oceanic igneous rocks Harald Furnes a,, Neil R. Banerjee b, Hubert Staudigel c, Karlis Muehlenbachs d, Nicola McLoughlin a, Maarten de Wit e, Martin Van Kranendonk f a Centre for Geobiology and Department of Earth Science, University of Bergen, Allegt. 41, 5007 Bergen, Norway b Department of Earth Sciences, University of Western Ontario, London, Ontario, Canada N6A 5B7 c Scripps Institution of Oceanography, University of California, La Jolla, CA , USA d Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E3 e AEON and Department of Geological Sciences, University of Cape Town, Rondebosch 7701, South Africa f Geological Survey of Western Australia, 100 Plain St. East Perth, Western Australia 6004, Australia Received 31 October 2006; received in revised form 12 March 2007; accepted 28 April 2007 Abstract Bioalteration of basaltic glass in pillow lava rims and glassy volcanic breccias (hyaloclastites) produces several distinctive traces including conspicuous petrographic textures. These biologically generated textures include granular and tubular morphologies that form during glass dissolution by microbes and subsequent precipitation of amorphous material. Such bioalteration textures have been described from upper, in situ oceanic crust spanning the youngest to the oldest oceanic basins (0 170 Ma). The granular type consists of individual and/or coalescing spherical bodies with diameters typically around 0.4 m. These are by far the most abundant, having been traced up to 550 m depths in the oceanic crust. The tubular type is defined by distinct, straight to irregular tubes with diameters most commonly around 1 2 m and lengths exceeding 100 m. The tubes are most abundant between 50 m and 250 m into the volcanic basement. We advance a model for the production of these bioalteration textures and propose criteria for testing the biogenicity and antiquity of ancient examples. Similar bioalteration textures have also been found in hyaloclastites and well-preserved pillow lava margins of Phanerozoic to Proterozoic ophiolites and Archean greenstone belts. The latter include pillow lavas and hyaloclastites from the Mesoarchean Barberton Greenstone Belt of South Africa and the East Pilbara Terrane of the Pilbara Craton, Western Australia, where conspicuous titanite-mineralized tubes, have been found. Petrographic relationships and age data confirm that these structures developed in the Archean. Thus, these biologically generated textures may provide an important tool for mapping the deep oceanic biosphere and for tracing some of the earliest biological processes on Earth and perhaps other planetary surfaces Elsevier B.V. All rights reserved. Keywords: Bioalteration textures; Volcanic glass; Oceanic crust; Ophiolites; Greenstone belts; Evidence for early life 1. Introduction Corresponding author. Tel.: ; fax: address: harald.furnes@geo.uib.no (H. Furnes). Life on Earth may have evolved well before the oldest preserved rocks, prior to 3.8 Ga, and most likely in the vicinity of hydrothermal vents in the oceanic crust (Nisbet and Sleep, 2001; Canfield et al., 2006). Evidence /$ see front matter 2007 Elsevier B.V. All rights reserved. doi: /j.precamres

2 H. Furnes et al. / Precambrian Research 158 (2007) for the earliest ( 3.8 Ga) purported life on Earth is solely geochemical and consists of isotopically light carbon in graphite contained within amphibolite- to granulitegrade supracrustal rocks in the Itsaq Gneiss Complex of the North Atlantic Craton in southwest Greenland (Schidlowski, 1988, 2001; Mojzsis et al., 1996; Rosing, 1999), but this evidence has been controversial (van Zuilen et al., 2002; Lepland et al., 2005). The earliest candidate fossilized microorganisms, on the other hand, are found in rocks 3.5 Ga from the Pilbara Craton in Australia (Walter et al., 1980; Schopf, 1993; Hoffman et al., 1999; Ueno et al., 2001; Van Kranendonk et al., 2003; Allwood et al., 2006) and the Barberton Greenstone Belt in South Africa (Muir and Grant, 1976; Knoll and Barghoorn, 1977; Walsh and Lowe, 1985; Walsh, 1992; Westall et al., 2001, 2006), but many of these claims have likewise proved controversial (e.g. Lowe, 1994; Brasier et al., 2002, 2005; Garcia-Ruiz et al., 2003). Until recently, only sediments were considered to provide habitats for microbial activity, leaving volcanic rocks largely unexplored by biogeoscience research. Recent studies have shown that submarine glassy basaltic rocks also provide habitats for microbial life, first convincingly shown by Thorseth et al. (1992). Moreover, it has been suggested that soon after eruption, when the ambient temperature (<113 C) is tolerable for life to exist (Stetter et al., 1990; Stetter, 2006), colonization of the glassy rim of pillow lavas by microorganisms occurs contemporaneously wherever seawater has access (Thorseth et al., 2001). Microbial colonization of the glassy selvages of pillow lavas is most commonly observed along fractures, leaving behind several traces of their former presence. The most ubiquitous are microscopic alteration textures found within the fresh glass at the interface with altered glass. These are empty or mineral-filled pits and channels with sizes and shapes that are comparable to modern microbes. Furthermore, samples with these petrographic alteration textures commonly show very low δ 13 C values (e.g. Furnes et al., 1999, 2001a; Banerjee and Muehlenbachs, 2003), elevated concentrations of elements such as C, N, P, K and S (e.g. Furnes et al., 2001b; Banerjee and Muehlenbachs, 2003), and in younger samples the presence of DNA (e.g. Torsvik et al., 1998; Furnes et al., 2001a; Banerjee and Muehlenbachs, 2003), all of which are strongly suggestive of a biogenic origin. Several studies have documented alteration textures, element distributions and carbon isotope compositions of pillow lavas from in situ oceanic crust world-wide that are indicative of microbial alteration processes (Thorseth et al., 1995a, 2001, 2003; Furnes et al., 1996, 1999, 2001a,b; Fisk et al., 1998, 2003; Torsvik et al., 1998; Furnes and Staudigel, 1999; Banerjee and Muehlenbachs, 2003). Furthermore, Furnes and Staudigel (1999) have demonstrated that the bioalteration process can be traced as deep as 550 m into the oceanic crust and that these biotic alteration processes dominate in the upper 350 m of the volcanic crust. Thus, a large body of evidence collected over the last decade has convincingly demonstrated that the upper volcanic part of the in situ oceanic crust is a habitat for microbial life. Moreover, the bioalteration of pillow lava glass is a widespread and common process that may have a profound effect on the chemical reactions, fluxes and products of seawater rock interactions (e.g. Staudigel and Furnes, 2004; Staudigel et al., 2004). Textural studies of pillow lavas from in situ oceanic crust can only record bio-interaction with pillow lavas dating back to the oldest intact example of 170 Ma (Fisk et al., 1999). This represents only a small fraction of Earth s history and to extend the record of bioalteration further back in Earth s history, it is therefore necessary to investigate pillow lavas of former oceanic crust represented by ophiolites and greenstone belts. These studies have so far confirmed that similar microbe-rock interactions have taken place within formerly glassy volcanic rocks since the Mesoarchean (Furnes and Muehlenbachs, 2003; Furnes et al., 2004, 2005; Banerjee et al., 2006a). Thus bioalteration textures provide a new search tool for the earliest signs of life on Earth and other planetary surfaces (e.g. Banerjee et al., 2004a,b, 2006b; McLoughlin et al., 2007). In this paper, we first describe the range of alteration textures that are found within the glassy rims of pillow lavas from in situ oceanic crust. We then present a model for the biotic alteration of oceanic pillow lavas and proposed criteria for testing the antiquity and biogenicity of these bioalteration textures. We then proceed to demonstrate that similar bioalteration textures are preserved in ancient pillow lavas from ophiolites and greenstone belts back to 3.5 billion years ago. We outline the petrographic characteristics of mineralised bioalteration structures in ancient pillow lava rims and hyaloclastites and review what is currently known about how these biostructures are preserved. Lastly, we explore how bioalteration textures found in terrestrial pillow lavas may be sought in extraterrestrial rocks. 2. Alteration textures in pillow lava of the modern oceanic crust There are two fundamentally different modes of alteration of basaltic glass in modern seafloor setting, i.e. abiotic and biotic alteration. The abiotic alteration results

3 158 H. Furnes et al. / Precambrian Research 158 (2007) in the formation of the long-recognized, but enigmatic material termed palagonite. The other alteration mode is the more recently-recognized biotic etching generated by the microbial colonization of rock surfaces. The two alteration processes may be contemporaneously active within the temperature limits of life. Below we briefly comment on the products of abiotic alteration and provide a comprehensive description of biogenic alteration Abiotic alteration The alteration of basaltic glass is traditionally viewed as a purely physio-chemical process and commonly yields a pale yellow to dark brown material referred to as palagonite. It appears as banded material of approximately equal thickness on both sides of fractures, with smooth alteration fronts between the fresh and altered glass that are symmetric with respect to the fracture. Peacock (1926) divided palagonite into two types, gelpalagonite (amorphous) and fibro-palagonite (consisting of clays, zeolites and ferrohydroxides). Palagonitization, however, involves a continuous aging process from the amorphous to crystalline stage involving complicated processes of incongruent and congruent dissolution and contemporaneous precipitation, hydration, and pronounced chemical exchange, that takes place at low to high-temperature (e.g. Thorseth et al., 1991; Stroncik and Schmincke, 2001; Walton and Schiffman, 2003; Walton et al., 2005). Fig. 1. Progressive development of granular texture from the incipient stage along fractures (A and B), to a more advanced stage along fracture (C), at intersection between fractures (D), to advanced stages (E and D). Note the regular palagonite rim adjacent to the fracture in (E), and different stages of alteration along the fractures in (F). The images are from the following samples: (A) ODP Site 648B-1R-1, unit 3, piece 7, cm; (B) detail from A (central fracture); (C) DSDP Site 418A-52-5, cm; (D) DSDP/OPD (Leg 70) Site 504B-46-3, unit 30A, piece 803, cm; (E) DSDP Site 417D, 30-6, cm; (F) DSDP Site 418A-55-4, cm.

4 H. Furnes et al. / Precambrian Research 158 (2007) Biotic alteration Two types of textural development have been observed and related to microbial alteration (subsequently referred to as bioalteration). These are granular and tubular textures which are texturally and geochemically distinguishable from the smooth and/or banded palagonite alteration fronts which result from solely abiotic alteration Granular alteration textures The granular alteration type consists of individual, spherical bodies filled with cryptocrystalline to very fine-grained phyllosilicate phases. In the initial stages of bioalteration the granular type appears as isolated spherical bodies along fractures in the glass (Fig. 1A and B). At more advanced stages of bioalteration these become more numerous and coalesce to define granular aggregates along fractures (Fig. 1C), or at the intersection between fractures (Fig. 1D). These granular aggregates can develop into irregular bands that protrude into the fresh glass from one or several fractures (Fig. 1E). In this way the development of granular alteration generally shows no symmetry on opposite sides of fractures (Fig. 1C F), and the thickness and distribution of granular alteration fronts around fractures is commonly variable (Fig. 1F). In some cases it is evident that abiotic palagonitization started before the onset of granular bioalteration (Fig. 1E) Tubular alteration textures The tubular alteration type is defined by tubes which are invariably rooted on surfaces where water has permeated. The tubes may be empty but are most commonly filled with similar material to the granular type. They may occur as straight and/or curved tubes and develop from tiny individuals into dense bundles of long, numerous tubes, attached to fractures in the glass (Fig. 2). Individual tubes may show segmentation structures and swelling to bud-like structures in various stages of growth. These eventually develop into new tubes and bifurcating branches (Fig. 3). In most cases the tubules propagated perpendicular to the alteration front (Fig. 2), although random orientations are also seen (Fig. 4A). Tube alignment independent from the orientation of fractures has also been observed (Fig. 4B). In rare cases parallel tubes may abruptly change growth direction by 180 when they meet another tube or fracture (Fig. 4C). In cases where vesicles are present it is common to see tubular growth from the vesicle walls radially outwards Fig. 2. Various stages in the development of tubular texture protruding into fresh glass (yellow in A, C, D, and greenish in B), showing beginning growth stage with only few tubules (A), relatively dense population of tubules (B) to extremely dense concentration of tubules (C and D). Picture A: from DSDP sample B, 35-1, 24, piece 274, cm. Note the buds on some of the tubules. Picture B: from DSDP sample B, 20R-4, piece 5, cm. Note that the tubules have grown predominantly on only one side of the fractures. Picture C: from DSDP sample 418A, 62-4, cm. Picture D: detail from (C) showing the long and thin tubules.

5 160 H. Furnes et al. / Precambrian Research 158 (2007) Fig. 3. Tubules showing budding and branching (b) (A), and segmentation (B). Picture A: from DSDP sample B, 20R-4, piece12f, cm. Picture B: sample from Site 1184A. into the fresh glass (Fig. 5A). Tubular textures are also observed around varioles and phenocrysts, where concentric cooling/stress fractures have developed (Fig. 5B) Size distribution of granular and tubular textures The size distribution of bioalteration textures from six different DSDP/ODP Sites in the Atlantic Ocean, Pacific Ocean (at the Costa Rica Rift), and the Lau Basin, from crust varying in age from 6 Ma to 110 Ma, have been measured. The diameter of the granules, regardless of age, location, as well as depth into the crust, varies from 0.1 m up to rare examples of 1.5 m. The most common size is around 0.4 m (Fig. 6). In comparison, the diameters of the tubular structures are substantially larger and there is only a minor overlap in their size distributions (Fig. 7A). The smallest and largest diameters measured are 0.4 m and 6 m, respectively, and the most common size range is 1 2 m(fig. 7A), the average diameter being 1.4 m. The lengths of the tubes are highly variable, from a few micrometers up to several hundred micrometers (Fig. 2). Fig. 4. Tubules showing random growth orientation (A), preferred alignment independent from the orientation of the fractures (B), and a change of 180 in the growth orientation of tubules (C). Picture A: from ODP sample A, 11R-1, piece10, cm. Picture B: from DSDP sample B, 47-2, piece 889, cm. Picture C: from sample 417D, 53-2, cm Textural type versus depth The variation in measured bioalteration as a percentage of total alteration (i.e. abiotic plus biotic) and how this changes with depth and temperature into the volcanic crust is shown in Fig. 8. The data are predominantly from the oceanic crustal sections collected at Sites 417 and 418 of the 110 Ma Western Atlantic and at Sites 504B and 896A of the 5.9 Ma Costa Rica Rift. (The percentage

6 H. Furnes et al. / Precambrian Research 158 (2007) Fig. 5. Tubular texture developed and rooted around a vesicle (A and B), and varioles (C and D). Picture A: from DSDP sample 418A, 62-4, cm. Note the radial arrangement of the tubular texture. Picture B: detail from A showing straight to highly irregular tubules. Picture C: from DSDP sample B, 20R-4, cm. Picture D: detail from C. Note the segmented nature of the tubules. bioalteration is recalculated from Furnes and Staudigel, 1999; Furnes et al., 2001b. The temperature data was collected at Site 504B, where the volcanic basement is overlain by 275 m of sediments). Fig. 8 shows that the total amount of alteration within the uppermost part of the volcanic sequence is generally low and in these locations the granular type of bioalteration is completely dominant relative to abiotic alteration. With increasing depth and temperature however, abiotic alteration take over as the dominant alteration process. Of the two bioalteration morphologies the granular type is by far the most common and can be found at all depths into the volcanic basement where the presence of fresh glass allows bioalteration to be traced (down to 550 m). In the upper 350 m of the crust the granular alteration type is dominant, though most pronounced in the upper 200 m at temperatures less than 80 C, and decreases steadily to become subordinate at temperatures of about 115 C. The tubular alteration textures meanwhile, constitute only a small fraction of the total alteration and show a clear maximum at m depth at temperatures of around 70 C. At the surface, as well as below 350 m the tubular textures are generally absent or rare. This dataset documenting the depth distribution of bioalteration textures is the time-integrated product of microbial bioalteration in the oceanic crust as it cools, subsides and is buried (e.g. Crosby et al., 2006). The build up of oceanic crust may take s of 1000 years depending on the spreading rate. The time required to build the 650 m thick volcanic sequence found at the intermediate-spreading rate Costa Rica Rift is estimated to be between 15,000 and 20,000 years (Pezard et al., 1992). The stratigraphy of volcanic successions described from in situ oceanic crust and ophiolites indicates construction during two to seven main volcanic cycles each with several sub-cycles (see summary in Furnes et al., 2001c, 2003). This implies that during the build-up of the volcanic pile microbial colonization and bio-corrosion may have commenced immediately after a new eruption and subsequently waned several times. Reports of bioalteration textures in samples dredged from the ocean floor suggest that bioalteration starts very early (Thorseth et al., 2001), but it is as yet unknown as to when and where in the volcanic pile bioalteration is most vigorous. Changes in fluid flux, nutrient supply and temperature are likely to be important controls on the location of bioalteration in the oceanic crust that could be investigated by detailed downhole studies. It should be remembered, however, that most drill holes in the volcanic rocks of relatively young oceanic crust have rather low ( 20%) recoveries. In addition, this net distribution pattern includes preservational variables such as the differential precipitation of minerals within the bioalteration textures that may act to enhance their chance of surviving in the rock record.

7 162 H. Furnes et al. / Precambrian Research 158 (2007) Fig. 6. Relationship between diameter of granular structures and percentage in size classes from different DSDP/ODP Sites. The data sets on which the depth distribution of bioalteration (Fig. 8) has been constructed are mainly derived from the 5.9 Ma Costa Rica Rift and the 110 Ma Western Atlantic oceanic crustal segments. The original data sets from these two oceanic crustal segments show exactly the same maximum bioalteration as a percentage of total alteration despite their very different ages (see Fig. 11 of Furnes et al., 2001b). This would indicate that a substantial part of the bioalteration happens very early and that the alteration pattern is established at

8 H. Furnes et al. / Precambrian Research 158 (2007) Fig. 7. Comparison between diameters of granular and tubular structures in the glassy margin of pillow lavas from in situ oceanic crust (A), and tubular structures from former glassy hyaloclastites of the Euro Basalt (B), Kelly Group, Pilbara Craton (Western Australia), and the Hoeggenoeg Formation (C) of the Barberton Greenstone Belt (South Africa). an early stage in the crustal history, i.e. within 6 Ma. In broad terms this is consistent with the estimates of microbial biomass production from oxidative alteration and hydrolysis within the upper oceanic crust (e.g. Bach and Edwards, 2003). However, as long as fresh glass is present and seawater circulation occurs, the bioalteration process may continue. Hydrothermal convection as a result of convective heat loss in the oceanic crust may occur for time periods up to 65 Ma (e.g. Stein et al., 1995). This age may put some constrains on the upper time limit of bioalteration in the oceanic crust Microbiological constraints on the bioalteration of volcanic glass Microbiological investigations have shown that microorganisms are associated with the alteration of volcanic glass and the aim of this section is to give a brief overview of current knowledge of these organisms and the metabolisms that may be involved. During the alteration of basaltic glass it is envisaged that oxidized compounds (e.g. SO 2 4,CO 2,Fe 3+ and Mn 4+ ) supplied by circulating seawater may be used as electron acceptors and carbon sources, and that reduced Fe and

9 164 H. Furnes et al. / Precambrian Research 158 (2007) Fig. 8. Relationship between bioalteration (granular (blue field) and tubular (red field)) of total alteration, depth and temperature into the volcanic crust. For the construction of this diagram the modes of biotic (granular and tubular) and abiotic alteration were point counted on 72 thin sections. Original data published in Furnes et al. (2001b), and diagram modified from Staudigel et al. (2006). Mn in the volcanic glass may provide electron donors. Staining for nucleic acids, bacterial and archeal RNA has revealed that biological material is concentrated at the interface between fresh and altered glass, and is localized within granular and tubular alteration textures (e.g. Giovannoni et al., 1996; Torsvik et al., 1998, Fig. 2; Banerjee and Muehlenbachs, 2003, Fig. 14). In addition, cells have been observed by SEM on the surface of altered glass with morphologies that included filamentous, coccoid, oval, rod and stalked forms (e.g. Thorseth et al., 2001). Furthermore, these often occur in or near etch marks in the glass that exhibit forms and sizes that resemble the attached microbes (e.g. Thorseth et al., 2003). Along fractures in basaltic glass that are now altered to palagonite bacterial moulds encrusted in iron and manganese rich oxides are found with coccoid forms, also branched and twisted filaments that resemble the Fe-oxidizing bacteria Gallionella; e.g. Thorseth et al. (2001, 2003). This is not surprising, given that Gallionella ferruginea and Leptothrix discophora are considered to be classic examples of organisms capable of lithotrophic Fe-oxidation at circum neutral ph. In addition, diverse manganese oxidizing bacteria have been isolated from basaltic seamounts and are argued to enhance the rate of Mn oxidation during the bioalteration of basaltic glass (e.g. Templeton et al., 2005). Culture independent molecular profiling studies meanwhile, have found that basaltic glass is colonized by microorganism that are distinct from those found in both deep seawater and seafloor sediments. For example, microbial sequences obtained from samples dredged from the Arctic seafloor are affiliated to eight main phylogenetic groups of bacteria and a single marine Crenarchaeota group (Lysnes et al., 2004). With ageing of the basaltic glass it is reported that autotrophic microbes which tend to dominate the early colonizing communities are replaced by heterotrophic microbes in older, more altered samples (Thorseth et al., 2001). Moreover, it has recently been discovered that a group of bacteria distantly related to the heterotrophic organisms Marinobacter sp. and Hyphomonas sp. are also capable of chemolithoautrophic growth and employ Fe-oxidation at circum neutral ph on a range of reduced substrates that include basaltic glass (Edwards et al., 2003). Attempt to generate bioalteration textures in laboratory culture experiments with volcanic glass substrates have had mixed success. Early studies conducted at room temperature, with high nutrient levels and relatively short incubation times of ca. 1 year produced etch pits and altered surfaces (Thorseth et al., 1995b). Some of these etch pits exhibited features interpreted as growth rings which were taken to suggest that these pits may develop into tubular structures and so a model for the bioalteration of volcanic glass was advanced (Thorseth et al., 1992; see also Section 5). Such extended tubular morphologies however, have yet to be produced in the laboratory. More recent microcosm experiments designed to mimic natural, oligotrophic seafloor environments with temperatures of 10 C, low concentrations of N, P and Fe and only ppm total organic carbon content failed to produce however, enhanced bioalteration rates relative to sterile controls (Einen et al., 2006). Thus in summary it appears, that Fe and Mn oxidation are important microbial metabolisms that likely contribute to the bioalteration of volcanic glass. However, the optimal conditions under which this occurs and the diversity of microorganisms that may be involved are yet to be fully documented. 3. Alteration textures in pillow lava of ophiolites and greenstone belts Ophiolites and greenstone belts represent fragments of ancient ocean crust that enable studies of alteration processes in pillow lavas and hyaloclastites which predate in situ oceanic crust. Below we will demonstrate that the methods developed for studying textural biomarkers from in situ oceanic crust have also been successfully applied to ophiolites and greenstone belts. These allow us to search for petrographic traces of life during periods of the Earth s history in which relatively undeformed or little-deformed submarine, formerly glassy volcanic rocks can be found. Suitable pillow lava sequences have been found in 3500 million-years-old rocks South Africa and Western Australia, and perhaps even in con-

10 siderably deformed sequences as far back as 3800 million-years-ago in southwest Greenland Ophiolites H. Furnes et al. / Precambrian Research 158 (2007) Pillow lavas from four ophiolite sequences ranging in age from Cretaceous to Early Proterozoic, have been investigated for biosignals: the 92 Ma Troodos ophiolite complex (TOC) in Cyprus (e.g. Schmincke and Bednarz, 1990); the 160 Ma Mirdita ophiolite complex (MOC) in Albania (e.g. Dilek et al., 2005); the 443 Ma Solund- Stavfjord ophiolite complex (SSOC) in western Norway (e.g. Furnes et al., 2003); and the 1953 Ma Jormua ophiolite complex (JOC) in Finland (e.g. Kontinen, 1987). The entire sequences of the TOC, SSOC and JOC display a Penrose-type pseudostratigraphy, i.e. a layered-cake structural organization of oceanic crust components (e.g. Dilek et al., 1998). The western parts of the MOC, however, from which we present bioaltered material, lack a prominent sheeted dike complex (though discrete dike swarms occur in places), and pillow lavas rest on gabbroic and serpentinized ultramafic mantle rocks. This type of development is comparable to the slow-spread Hess type oceanic crust (Dilek, 2003). In the youngest two investigated ophiolites, i.e. the TOC and MOC, which are both at zeolite to lowest greenschist facies metamorphic grade and have experienced minor to no deformation, there are spectacular textural features of purported microbiological origin. Figs. 9 and 10 show a collage of textures for which we attribute biologic origin. Fig. 9 shows granular and tubular biotextures within patches of still preserved fresh glass from pillow rims of the TOC. The most common biotexture is the granular type which may appear as symmetrical or asymmetrical patches rooted in original, now clay-filled fractures (Fig. 9A). Associated with the granular alteration type are also straight to curved, thin (1 2 m thick), empty to mineral-filled tubes that may attain length up to 100 m (Fig. 9B). Another type of tubular texture is much thicker (up to 20 m thick) and shows well-developed segmentation structures (Fig. 9C). Both granular and tubular bioalteration textures have also been found in rare patches of fresh glass in pillow lava rims of the MOC (Fig. 10). The tubular biotextures are enclosed in zeolites (Fig. 10B). It is uncertain however, whether the zeolites represent replacement of basaltic glass or merely fill spaces between originally glass fragments. Chemical and isotopic characteristics associated with the tubular textures in the glassy rim of pillows also strongly support their biological origin (see Furnes et al., 2001d; Furnes and Muehlenbachs, 2003). Fig. 9. Granular (A) and tubular (B and C) textures in glassy pillow lava rims from the Troodos Ophiolite Complex, Cyprus. Note the segmented nature of the tubular structure shown in image (C). Abbreviations FG: fresh glass; GT: granular texture; ST: segmented tube. In the older pillow lavas from the least deformed part of the SSOC which is of lower greenschist facies, possible traces of biogenerated structures were recorded (Furnes et al., 2002a). Whilst even in the strongly recrystallized glassy rims of the lower amphibolite facies JOC, within areas of high carbon content, we have also found mineralized features that strongly resemble organic remains (Furnes et al., 2005).

11 166 H. Furnes et al. / Precambrian Research 158 (2007) interlayered with cherts and overlain by cherts, banded iron formations (BIF) and shales (de Wit et al., 1987). The magmatic sequence consists of the Theespruit, Komati, Hooggenoeg and Kromberg Formations (the Onverwacht Group) and comprises 5 6 km of predominantly basaltic and komatiitic extrusive (pillow lavas, sheet flows, and minor hyaloclastite breccias) and intrusive rocks. These rocks are generally well preserved, locally little-deformed, and have undergone prehnitepumpellyite to greenschist facies metamorphism (de Wit et al., 1987). Samples were collected from the Komati, Hooggenoeg and Kromberg Formations. Bioalteration textures in pillow rims have so far been found in the upper part of the Hooggenoeg Formation and the lower part of the Kromberg Formation (Furnes et al., 2004; Banerjee et al., 2006a). Fig. 10. Granular (A) and tubular (B) textures in glassy pillow lava rims from the Mirdita Ophiolite Complex, Albania. Abbreviations FG: fresh glass; GT: granular texture; T: tubular textures in zeolite; Ze: zeolite Greenstone belts Pillow lavas from two of the oldest and best preserved greenstone belts in the world, the mesoarchean Barberton Greenstone Belt (BGB) of South Africa, and the Pilbara Craton (PC) of Western Australia, have been investigated for biosignals. In both the BGB and PC, the outermost mm of most pillows is defined by a dark zone that represents the chilled, originally glassy rim. In many cases part of the glassy margin spalled off during pillow growth and formed interpillow hyaloclastite. Due to the pervasive prehnite-pumpellyite to greenschist facies metamorphic overprint in both of these localities, these rims now consist of extremely fine-grained chlorite with scattered grains of quartz, epidote, and amphibole Barberton Greenstone Belt The Ma old magmatic sequences (de Ronde and de Wit, 1994) of the BGB comprises 5 6 km of submarine komatiitic and basaltic pillow lavas, with interbedded sheet flows and related intrusions that are Pilbara Craton The Pilbara Craton contains some of the best preserved geological record of the early Earth (Van Kranendonk and Pirajno, 2004; Van Kranendonk et al., 2002, 2004, 2007). The East Pilbara Granite-Greenstone Terrane of the craton contains a 20 km thick succession of low-grade metamorphic, dominantly volcanic supracrustal rocks (Pilbara Supergroup) that were deposited in four autochthonous groups from Ga (Van Kranendonk, 2006; Van Kranendonk et al., 2007) These include, from base to top, the Ga Warrawoona Group, the Ga Kelly Group, the Ga Sulphur Springs Group, and the Ga Soanesville Group. Pillows and interpillow hyaloclastites were collected from the Dresser Formation and Apex Basalt of the Warrawoona Group, and the Euro Basalt of the Kelly Group. The pillow samples that have so far been found to display bioalteration textures come from the lower part of the 5 8 km thick Euro Basalt (Staudigel et al., 2006; Banerjee et al., 2007) Mineralized bioalteration textures Mineralized tubular structures from the BGB and Euro Basalt (Pilbara Craton) pillow lavas and hyaloclastites are now 1 9 m in width (averages of 4 m for the BGB samples and 2.4 m for the Euro Basalt) (Fig. 7), up to 200 m in length (average 50 m), are infilled by extremely fine-grained titanite with some also containing minor amounts of chlorite and quartz (Figs. 11 and 12). These structures are observed to extend away from healed fractures and/or grain boundaries along which seawater may once have flowed. Some of these tubular structures exhibit segmentation into subspherical bodies caused by chlorite overgrowths formed during metamorphism (Figs. 11 and 12). In addition to

12 H. Furnes et al. / Precambrian Research 158 (2007) Fig. 11. (A) Tubular textures in interpillow hyaloclastites from the Hooggenoeg Formation of the Barberton Greenstone Belt, South Africa. The black zone (consisting of titanite) across the middle part of the picture, and in which tubular structures are rooted, marks the healed boundary between originally glassy fragments. The fine grained green mineral is chlorite, and the white, stubby mineral grains below the titanite zone are epidote crystals. The boxed areas (B and C) show the positions of the enlarged pictures. Note the segmented nature of the tubules, and the overgrowth of chlorite. Fig. 12. (A) Tubular textures in interpillow hyaloclastites from the Euro Basalt of the Pilbara Supergroup, Western Australia. Black patchy zones of titanite mark the healed boundary between originally glassy fragments, in which tubular structures are rooted. The fine grained green mineral is chlorite, and the white to light brownish mineral is calcite. The boxed areas (B and C) show the positions of the enlarged pictures. Note the segmented structure of all the tubules.

13 168 H. Furnes et al. / Precambrian Research 158 (2007) the morphological similarities between the ancient structures and modern tubular bioalteration textures, C, N and P enrichments are localized in the linings of the Archean tubular structures. X-ray element maps of these linings are given in Fig. 3 of Furnes et al. (2004) for the Hooggenoeg examples, and Fig. 2 of Banerjee et al. (2007) from the Euro Basalt examples. By analogy to modern examples, these enrichments in biologically significant elements, which coincide with the microtube margins have been taken to represent decayed biological remains. The tubular structures occur within apparently narrow windows of these thick Archean submarine lava sequences. However, when they do occur they are generally present in dense populations. Based on their similarity to textures observed in recent glassy pillow basalts we interpret these structures to represent ancient mineralized traces of microbial activity formed during biogenic etching of the originally glassy pillow rims and hyaloclastites as microbes colonized the glass surface, i.e. that they were originally hollow tubular structures. In contrast to bioalteration textures from in situ oceanic crust where granular textures dominate (Fig. 8), those from investigated Archean greenstone belts are largely titanite-filled tubular textures (Figs. 11 and 12). (Although, one possible occurrence of putative granular textures has been identified along fractures in originally glassy fragments of hyaloclastites from the Hoeggenoeg Formation, see Fig. 6 of Banerjee et al., 2006a). This predominance of the tubular alteration textures in Archean lavas may be attributed to the masking of the typically smaller granular textures by titanite crystallization. Whereas conversely, the early precipitation of titanite to infill many of the larger tubular texture may have enhanced their preservation by limiting morphological changes caused by recrystallization of the host rock (Figs. 11 and 12). 4. Establishing antiquity and biogenicity Several lists of criteria have been proposed for establishing the biogenicity of ancient microfossil and stromatolite remains (see for example Buick et al., 1981; Schopf and Walter, 1983; Brasier et al., 2005). These have provided a useful framework for discussions surrounding the early fossil record and have also generated much controversy (see Rose et al., 2006). To date there have been only preliminary attempts to outline a comparable list of biogenicity criteria for bioalteration textures in volcanic rocks; see for example McLoughlin et al. (2007). Here, we draw upon studies of modern and ancient endolithic organisms in volcanic glasses, carbonates and sandstones to propose the following criteria for investigating volcanic bioalteration textures: (1) an outcrop to thin-section scale geological context that demonstrates the syngenicity and antiquity of the bioalteration textures; (2) morphologies and distribution of the bioalteration textures that are consistent with biogenic behaviour; (3) geochemical evidence that is suggestive of biological processing. To demonstrate that candidate bioalteration textures are syngenetic with the volcanic substrate and are not later contaminants relies upon fabric relationships. At the outcrop scale this involves mapping to show that the phases containing the bioalteration textures are syneruptive and not younger veins or dyke filling phases. At the thin-section scale the bioalteration textures themselves should also be seen to predate cross-cutting fractures, veins and cements. They should be concentrated along paths of early fluid migration and/or weaknesses in the glass and occur as asymmetric masses across fractures that are distinct from symmetric, abiotic palagonite alteration fronts (see Fig. 13A). Further support for their antiquity can be gained from the infilling mineral and/or organic phases that should have experienced degrees of metamorphism comparable to the host rock. For example, in Archean greenschist facies terranes one might hope to find bioalteration textures infilled with chlorite and graphite bearing phases. A new approach that may enable confirmation of such relative age estimates is the direct dating of titanite phases which infill the bioalteration textures, see Section 6.2 and Banerjee et al. (2007). The range of morphologies displayed by candidate bioalteration textures in ophiolites and greenstones is more restricted than that seen in recent volcanic glasses, none-the-less there are number of useful morphological indicators and distribution patterns that can be sought to test their biogenicity. For instance, many examples of ancient tubular bioalteration show branching patterns and sharp changes in direction when they encounter another tube or fracture and both of these features are difficult to explain by purely abiotic alteration (cf. Fig. 4). The size range of these ancient bioalteration textures (see Fig. 6) is consistent with microbial involvement, but is not a strong criterion for inferring their biogenicity and probably reflects significant taphonomic modification. The distribution and abundance of bioalteration textures, especially their concentration around vesicles and varioles (see Fig. 5), is also suggestive of biological behaviour and suggests the selection of sites with localised chemical gradients or concentrated strain that provides weakness in the glass. The key controls on their distribution are yet to be fully documented, but it is envis-

14 H. Furnes et al. / Precambrian Research 158 (2007) Fig. 13. Model of alteration modes (abiotic and bioalteration) of basalt glass. (A) Abiotic alteration in which the typically yellowish brown palagonite develops around the glass fragments with approximately equal thickness. With progressive alteration the empty spaces between the grains become filled with authigenic minerals and finally sealed, thus preventing water circulation and thus slowing down the alteration process. (B and C) Biotic alteration of granular (B) and tubular (C) types. In our model microbes attach to the glass surface where water can get access (along fractures and on the outer surface of grains) and start etching. With progressive alteration cell division occurs and the granular and/or segmented tubular structures develop as long as water is accessible. With progressive alteration there is also continuous growth of authingenic minerals in the empty microcavities and micro-tubules. When the authigenic minerals have sealed the structures preventing water access, the bioalteration growth eventually stops. Modified from Staudigel et al. (2006). aged that the temperature, redox state and composition of primary circulating fluids may exert a strong control on their distribution. For comparison, it has been observed that morphologically similar microtubular structures in Archean sandstones preferentially occur in clasts rich in metal inclusions (Brasier et al., 2006; Wacey et al., 2006) and this type of apparent substrate selection may yet be found between volcanic clasts of varying composition. Fine-scale geochemical analyses of the phases that infill candidate bioalteration textures provide our third approach for testing their biogenicity. Thin (less than 1 m wide) linings of C, N, and P have been detected within modern and ancient bioalteration textures and are interpreted to represent preserved organic matter (e.g. Giovannoni et al., 1996; Furnes and Muehlenbachs, 2003). Ideally, accompanying depletions in metabolically significant elements in the surrounding rock matrix would provide further support for their biogenicity. For example, depletions in Mg, Fe, Ca, and Na have been described around bioalteration textures from in

15 170 H. Furnes et al. / Precambrian Research 158 (2007) situ oceanic crust (Alt and Mata, 2000). This type of elemental data may be further strengthened by carbon isotopic measurements on phases associated with the bioalteration textures. For instance, it is reported that disseminated carbonate preserved in altered pillow basalt rims is 13 C-poor, typically between +3.9 and 16.4 compared to carbonate within the unaltered pillow interiors, which has δ 13 C values of +0.7 to 6.9 that are similar to mantle values. This much greater range exhibited in the pillow rims is interpreted to reflect the microbial oxidation of organic matter that gives the more negative values and perhaps the loss of 12 C-enriched methane from Archea to give the more positive values (e.g. Fig. 9 in Furnes et al., 2002b; Banerjee et al., 2006a, and references therein). Corroboration of these findings may be possible by direct in situ analysis of carbon within the bioalteration textures themselves using nanoscale secondary ion mass spectrometry (NanoSIMS; cf. Kilburn et al., 2005). We remind the reader that all such analyses need to be conducted in conjunction with petrographic studies to confirm that the phases analysed are syngenetic and not the result of later water rock interaction. 5. Model of bioalteration Microbial colonization is known to produce pits and channels during etching of basaltic glass. This process has been known since Mellor (1922) described church glasses with surface pitting at locations where lichens grew (see Krumbein et al., 1991 for review). The first description of etching of natural glasses by microorganisms was by Ross and Fisher (1986). However, no convincing mechanism for how microbes may actually facilitate glass dissolution was provided. Later, in a study of subglacial hyaloclastites in Iceland the presence of bacteria hosted within basaltic glass aleration textures was reported (Thorseth et al., 1992). On this basis Thorseth et al. (1992) suggested that microbes may cause local variations in ph and/or secrete ligands that allow them to chemically drill into a silicate substrate. This process was subsequently verified experimentally by Thorseth et al. (1995b) and Staudigel et al. (1995, 1998) who demonstrated that glass alteration was enhanced in the presence of microbes. During microbially driven glass dissolution the total surface area of fresh glass available will progressively increase as the process proceeds. Staudigel et al. (2004) calculated that the fresh surface area would increase by factors of 2.4 and 200 during the formation of tubular and granular textures, respectively. In contrast, abiotic alteration causes the surface area of fresh glass to progressively decrease (Fig. 13A). In some samples we see that these processes are not mutually exclusive with the typical yellow to brown, smooth palagonite zones adjacent to fractures in the core of the alteration zone forming the first alteration product, which is then overtaken by granular and tubular alteration textures that occur on the outer edges adjacent to the fresh glass. Hence, from the numerous samples we have investigated, it is clear that the conditions under which bioalteration takes place, allows for a faster dissolution of the glass than the formation of abiotically-formed palagonite. Based on the textural characteristics shown in Figs we present a biotic alteration model for basaltic glass as shown in Fig. 13B and C. In this model the glass is congruently dissolved by chemical etching caused by microorganisms. The important roles of microorganisms and biofilms in the breakdown and dissolution of minerals and glass is well-established (e.g. Welch et al., 1999; Brehm et al., 2005). The sizes of the alteration textures are of the same order as the size range of candidate microbes. The size variations (Figs. 6 and 7) show log-normal distributions, a common phenomenon observed in biological systems (van Dover et al., 2003). A similar model is here advanced to that proposed by Thorseth et al. (1992) for alteration structures found in the 6 7 mm thick, light-exposed part of subglacial Icelandic hyaloclastites, a phenomenon that was attributed to light-dependent cryptroendolithic cyanobacteria creating a highly alkaline micro-environment which caused the etching. Here, we extend the model of Thorseth et al. (1992) to the deep biosphere. The granular and tubular structures that formed during bioalteration of the fresh glass of pillow rims are commonly filled with authigenic minerals, even in young pillow lavas. Subsequent to the congruent dissolution of the glass adjacent to the microorganisms, some of the chemical components precipitate on the cavity walls. Detailed studies of the authigenic minerals indicate that they are primarily clay minerals, Fe-hydroxides, zeolites and titanite (Storrie-Lombardi and Fisk, 2004; Furnes and Muehlenbachs, 2003; Banerjee et al., 2006a). As long as water continues to flow through the cavities removing waste products and perhaps also supplying nutrients then the bioalteration will proceed, providing also that the ambient temperature is sufficiently low for life to exist. When the voids are completely sealed the bioalteration process will cease (Fig. 13B andcatt 4 ). The biogenicity of structures claimed to represent fossilized microorganisms, of which filamentous features in the 3460 Ma Apex chert of the Pilbara Craton are a prime example (Schopf, 1993; Schopf et al., 2002), have been questioned (Brasier et al., 2002, 2005) and heav-

16 H. Furnes et al. / Precambrian Research 158 (2007) ily debated (see Dalton, 2002). Recent experiments have also generated filamentous microfossil-like structures, strikingly similar to those of the Apex chert, by abiotic mechanisms (Garcia-Ruiz et al., 2003). Hence, morphology alone may not be sufficient to argue for a biogenic origin of microbe-looking structures. In light of this discussion there is, however, a fundamental difference between the structures claimed to be fossilized microorganisms in sedimentary rocks and the granular and tubular bioalteration textures presented here. These alteration textures are micro-tracefossils in volcanic rocks; i.e. originally hollow traces that were produced as a result of microbial etching of the original glass and that have a higher preservation potential than the constructing organisms. Once a hollow tube has been produced in the glass and subsequently filled with secondary minerals, it may, in the absence of penetrative deformation and high-grade metamorphism, be preserved for billions of years. The organisms that produced the tube, on the other hand, will easily decay, and only traces of their chemical components may remain associated with the structures. In this context, it should be mentioned that somewhat similar looking structures to those presented above have been observed in Precambrian organic-rich cherts (e.g. Gruner, 1923). The formation of these structures was attributed to a process in which gas produced by the metamorphic heating and/or decay of organic matter drives tiny mineral grains through the rock matrix that act as millstones producing the hollow tubular structures (Tyler and Barghoorn, 1963; Knoll and Barghoorn, 1974). These so-called ambient inclusion trails (AITs) are most commonly found in microcrystalline cherts and phosphorites and may still contain the terminal crystal and sometimes, longitudinal striae along the tube margins. The tubular textures presented here are all hosted in formerly glassy rocks, but do not contain traces of mineral grains at their tips that could have acted as a millstone. Also, the commonly developed budding observed along the stem of the tubes would require several millstones within the same tube. In no way can we see that the textures we report from volcanic glasses, especially the granular textures, are compatible with a pressure solution mechanism and hence we refute this mechanism to account for the generation of the tubular structures presented here (see also Banerjee et al., 2006b; Brasier et al., 2006). Further, the enrichment of typical bio-elements, such as carbon, nitrogen, phosphorous, sulphur and potassium associated with the granular and tubular structures, as well as low ( 13 C values, are all signatures that strongly indicate a microbiological origin of these textures, and would be extremely difficult to account for by an abiotic AIT mechanism. Lastly, it is difficult to explain how the elevated pore fluid pressure necessary to generate AITs concentrated at volcanic clast margins, could be maintained within the complex and partially open network of fractures found in modern oceanic crust. 6. Significance of textural evidence for microbial alteration as a biomarker Presently, we are not aware of any feasible abiotic mechanism that can explain the origin of the granular and tubular textures described herein. Rather, their size distribution, morphological features and inferred growth patterns, as well as the concentration of biologically significant elements (e.g. Furnes et al., 1999, 2001a; Banerjee and Muehlenbachs, 2003; Banerjee et al., 2006a) and associated C-isotope characteristics (e.g. Furnes et al., 2001b, 2002a, 2004, 2005; Banerjee and Muehlenbachs, 2003; Banerjee et al., 2006a) are all suggestive of a microbiological origin. This has a number of important implications for the mapping of bioalteration in submarine, formerly glassy volcanic rocks throughout the terrestrial rock record and provides a new signature for the search for life beyond earth Mapping the deep biosphere in oceanic crust In the in situ oceanic crust where fresh glass is still commonly present, the granular and tubular textures can be very easily observed by ordinary light microscopy. The dark, commonly mineral-filled structures (Figs. 1 5) appear in strong contrast to the light yellowish-brown, isotropic glass. This makes it possible to identify and quantitatively estimate the extent of bioalteration as a function of depth by reinvestigating DSDP/ODP cores. The only study of this kind to date is that of Furnes and Staudigel (1999), which documented the relative proportions of alteration types in basaltic glass as a function of depth and temperature (Fig. 8) to 500 m into the volcanic basement of the oceanic crust. This study (op.cit.) showed that the tubular and granular bioalteration is dominant (up to 80%) of the total alteration in the upper 300 m of the volcanic pile. Whereas the granular alteration type occurs throughout the upper 500 m, the tubular type has only been found in the upper 300 m, has its maximal occurrence at a depth range of m at a present temperature range of C(Fig. 8). However, there are still many unanswered questions related to the controls upon the distribution of bioalteration with depth. Important geological factors will include the permeability at a give place and a given time and hence the flux of nutrients, and