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

www.elsevier.com/locate/epsl

Earth and Planetary Science L

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, Norwayb 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, USAd 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

During the last decade several studies have shown

that the upper volcanic part of the modern oceanic crust

0012-821X/$ - see front matter D 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.epsl.2005.11.011

* Corresponding author. Present address: Department of Earth

Sciences, University of Western Ontario, London, Ontario, Canada

N6A 5B7.

E-mail address: [email protected] (N.R. Banerjee).

is a habitat for microorganisms. In this environment

microbes colonize fractures in the glassy selvages of

pillow lavas, extracting energy and/or nutrients from

the glass by dissolving it, leaving behind biomarkers

that reveal their former presence [1–12]. The biomar-

kers consist of (1) corrosion structures (commonly

filled by secondary minerals) that have textural criteria

indicative of a biogenic origin (size, morphology, dis-

tribution as populations), (2) enrichment of C, N, P, and

etters 241 (2006) 707–722

N.R. Banerjee et al. / Earth and Planetary Science Letters 241 (2006) 707–722708

S associated with the corrosion structures, (3) charac-

teristically low d13C values of disseminated carbonate

within the altered glass rims of pillows compared to

their crystalline interiors, and (4) presence of DNA

associated with corrosion structures.

The methods developed for tracing biomarkers in

modern oceanic crust have been successfully applied to

pillow lava sections of ophiolites. The ophiolites inves-

tigated so far range in age from Cretaceous to Middle

Proterozoic, range in metamorphic grade from near

unmetamorphosed to lower amphibolite facies, and con-

tain all the principal components of a Penrose-type

ophiolite (summarized in [13]). Further, in a recent

study of pillow lavas of the ~3.2–3.5 Ga Barberton

Greenstone Belt (BGB) in South Africa, Furnes et al.

[14] reported biomarkers related to the initial alteration

of glassy pillow lava rims. Most products of biological

activity are too delicate to survive geological processes

like weathering, erosion, and dynamothermal-metamor-

phism. As such destructive processes compound through

geological time, it has proven to be increasingly difficult

to find preserved evidence for life as the age of a rock

approaches the age of the oldest rocks on Earth. Studies

of the earliest history of life are plagued also by pro-

blems of fossil preservation and poor and ambiguous

evidence for fossil material. In this paper we build upon

our previous work, present a new dataset of the biomar-

kers found in the volcanic rocks of the BGB, and stress

the importance of how the study of basaltic volcanic

rocks in Archean greenstone belts may contribute to the

discussion of the early life on Earth.

2. Basaltic glass as a geological setting for microbial

life

Biologically mediated corrosion of synthetic glass

is a well-known phenomenon [15] that has also been

proposed for the pitting of natural volcanic glass [16].

Thorseth et al. [17] first suggested that bio-corrosion

was produced by colonizing microbes that cause local

variations in pH which allows them to actively dis-

solve the natural basaltic glass substrates thereby pro-

ducing tubular structures. This process was later

verified in experiments [18–20]. The microbial disso-

lution experiments by Thorseth et al. [18] showed that

etch marks on the basaltic glass surface were produced

after a relatively short time (46 days). The etch marks

produced were of uniform size (0.3–0.5 Am in diam-

eter) and they had a chain or bcolonyQ shape, similar

to the size and arrangement of the live bacteria that

were removed from the glass surface. Although we are

unaware of any experiment that has produced long

(several tens of micrometers) tubular structures, the

experiment by Thorseth et al. [18] demonstrates the

onset of a dissolution process. We suggest that given

enough time the etching process, ultimately might

produce the long tubular structures. Over the past

decade numerous studies have shown that microbe-

sized corrosion structures are commonly produced by

biological activity in natural basaltic glasses through-

out the upper few hundreds of meters of the oceanic

crust of any age, including the oldest oceanic crust in

the western Pacific Ocean [18,2,21,3,4,22,5–7,9,11,

10,23]. These structures are very distinct and cannot

be explained by abiotic processes, as supported by

evidence from petrography, geochemistry and molec-

ular biology.

Key petrographic arguments for a biogenic origin for

the corrosion structures include their size similarity to

microbes, their biotic morphology, and distribution as

populations. In particular, these structures commonly

occur as irregular tubes that consistently originate from

fractures. The structures are also observed to bifurcate

and never occur with a symmetric counterpart on the

other side of the fracture. Geochemical evidence

includes the common enrichment of biologically im-

portant elements such as C, N, P, K, and S associated

with the microbial alteration structures (e.g. [4,6,7,11])

and characteristically low d13C values of disseminated

carbonate within microbially altered basaltic glass

[4,8,11]. Molecular arguments include the presence of

DNA associated with biological corrosion textures (e.g.

[21,4,11]). As to the timing of formation of microbial

alteration structures and subsequent filling of the struc-

tures, it is important to mention that we have found

filled tubules in the glassy rinds of Quaternary pillow

lavas (e.g. Fig. 3A of [8]). This shows that microbial

etching and subsequent filling of the empty structures

can be a penecontemporaneous process. In the absence

of abiotic explanations for these phenomena, microbial

etching is the most likely explanation for these petro-

graphic, geochemical, and biomolecular biomarkers in

the glassy margins of submarine lavas. The breadth of

these arguments and the abundance of these features

make it unlikely that microbial processes do not play an

important role during alteration of basaltic glass on the

present-day seafloor. Recent work by Lysnes et al. [24]

on the microbial community diversity in young (V1Ma) seafloor basalts has revealed eight main phyloge-

netic groups of Bacteria and one group of Archaea that

differ from those of the surrounding seawater including

autolitotrophic methanogens and iron reducing bacteria.

It should be stressed, however, that it has not yet been

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-

tures described here.

3. Evidence for early life

The evidence for earliest life on Earth fall in three

main categories: chemical evidence (e.g., carbon isoto-

pic evidence), micro-morphological evidence (e.g., mi-

croscopic observation of microfossils), and macroscopic

interpretation of sedimentary structures preserved in the

rock record that are commonly associated with modern

microbial mats (e.g., stromatolites). The oldest proposed

evidence for life in the geological record traces back to

3.5–3.8 Ga and is based on chemical signatures in high-

grade schists and paragneisses of the Isua Supracrustal

Belt (ISB), Southwestern Greenland. Graphite from

these rocks and within apatite crystals has unusually

low d13C values indicative of biological fractionation

of carbon [25–30]. However, recent studies have pointed

out that low d13C values in at least some of the ISB

graphite occur in secondary carbonate veins and may

thus be also explained by abiotic processes, which brings

into question much of the evidence from Isua [31–33].

In addition, reports of low d13C signatures from

graphite inclusions in apatite crystals from ~3.85 Ga

granulite-facies rocks on Akilia island have also been

questioned [34]. However, the occurrence of low d13C

signatures in a sequence of graded metasediments inter-

preted as turbidites from the ISB [30], remains widely

accepted as biogenic and are thus possibly the oldest

chemical evidence of life on Earth.

The next-oldest evidence for life in the geological

record is based on micro-textural observations sup-

ported by laser-Raman imaging of features interpreted

as filamentous microfossils in ~3465 Ma metasedi-

ments (Apex chert) from the Pilbara Craton in South-

western Australia (e.g., [35,36]). However, Garcia-Ruiz

et al. [37] have recently shown that morphologically

similar filamentous microstructures can be generated

from abiotic processes. This specifically calls into ques-

tion the uniqueness of the biogenic interpretation for

the filaments in the Apex cherts. In addition, Brasier

et al. [38] interpreted the filamentous structures in the

Apex cherts as secondary artifacts consisting of amor-

phous graphite produced from inorganic synthesis or

organic compounds in hydrothermal veins. In contrast,

the 3472 and 3447 Ma low-grade metasediments (now

mostly cherts) from the middle and uppermost Onver-

wacht Groups of the BGB contain microstructures

and carbon isotope evidence for the presence of fos-

sil bacteria and biofilm [39–41]. Nevertheless, there is

widespread skepticism for the biogenic nature of these

micromorphs (F. Westall, personal communication

2004).

These searches for early life in Greenland, Australia,

and South Africa show very clearly that geochemical or

morphological evidence for life is controversial and

underscores the need for more and better evidence for

Archean life in the oldest rock sequences. In this paper,

we describe textures and associated geochemical data in

formerly glassy pillow lavas, a suite of rocks that has

not been previously considered in the search for Arche-

an life. This new morphological and geochemical evi-

dence provide a consistent set of criteria for biogenicity

because it is firmly based on observations of a modern

analogue in oceanic basalts that has not been credibly

explained to form through abiotic processes. This ap-

proach offers an integrated data set that is substantially

more powerful than evidence based on a single data

type.

4. Geological background and sampling locations

The Mesoarchean BGB of South Africa contains

some of the world’s oldest and best-preserved pillow

lavas [42,43]. The magmatic sequence, consisting of

the Theespruit, Komati, Hooggenoeg, and Kromberg

Formations (the Onverwacht Group) comprises 5–6 km

of predominantly basaltic and komatiitic extrusive (pil-

low lavas, minor hyaloclastite breccias and sheet

flows) and intrusive rocks. This sequence is inter-

layered with cherts and is overlain by cherts, banded

iron formations (BIF) and shales of the Fig Tree and

Moodies Groups (Fig. 1). The Onverwacht Group has

been interpreted to represent fragments of Archean

oceanic crust, termed the Jamestown Ophiolite Com-

plex [42,44], that developed in association with sub-

duction and island arc activity approximately 3550 to

3220 Ma [45–47]. The magmatic sequence of the

Onverwacht Group is exceptionally well-preserved,

relatively undeformed away from its margins with

the surrounding granitoids, and upwards from the mid-

dle to the upper part of the sequence the metamorphic

grade decreases from greenschist to prehnite–pumpel-

lyite facies. Tectono-stratigraphically downward into

the Theespruit Formation and across a major shear

zone (the Komatii Fault), there is a rapid increase in

the metamorphic grade to higher pressure–lower tem-

perature amphibolite facies concomitant with the de-

velopment of tectonic fabrics related to structural

emplacement (~3.4 Ga) and subsequent exhumation

(~3.2 Ga) of the BGB [46,48,49].

Well away from the margin of the greenstone belt,

about midway into the Komati Formation, 40Ar / 39Ar

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-

nized komatiitic basalts give a metamorphic age of

3486F8 Ma [50]. This 40Ar / 39Ar age overlaps with

an ~3482 Ma U/Pb date of magmatic zircon from an

interbedded airfall tuff in the same outcrop [51,52].

The overlapping metamorphic and igneous crystalliza-

tion ages, perfect preservation of fine igneous micro-

structures such as spinifex tectures pseudomorphed by

metamorphic minerals, abundant pillow lavas, and

oxygen isotope stratigraphy through the sequence,

are taken as evidence that the metamorphism repre-

sents ocean-floor type hydrothermal alteration that

occurred penecontemporaneously with igneous activity

[53,42,54,44].

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

hyaloclastite from the best-exposed parts of the

Komati-, Hooggenoeg-, and Kromberg Formations

(Fig. 1). Pillow lavas were sampled from locations 3,

4, 6, 7, 10 and 11 (Fig. 1). Individual pillows are highly

variable with respect to size and vesicle density (Fig. 2).

The pillow lavas invariably display a well-developed

chilled margin (commonly 10 mm thick) grading in-

wards into a variolitic zone (5–10 mm thick), consisting

of a mixture of altered glass and microcrystalline ma-

terial. Interpillow hyaloclastites were sampled from

locations 6 and 7 (Fig. 1). Hyaloclastite breccias are

confined to minor inter-pillow occurrences (Fig. 2).

5. Analytical methods

Samples were first carefully trimmed with a saw and

the sawn surfaces ground to remove any trace of surface

contamination. Samples containing open fractures or

pore spaces were avoided completely. No open pore

spaces were observed in the sample collection as con-

firmed by SEM and petrographic analysis.

Scanning electron microscopy (SEM) observations

were performed on a JEOL JSM-6301FXV instrument

at the University of Alberta connected to a Princeton

Gamma Tech IMIX energy-dispersive spectrometer

system. The analyses were performed at an accelerating

voltage of 20 kV and a working distance of 15 mm.

Thin sections and grain mounts were sputter coated

with a thin film of iridium, approximately 40 A thick

[11].

X-ray mapping on the same iridium-coated thin

sections was carried out with a JEOL JXA-8900R

electron microprobe at the University of Alberta,

using an accelerating voltage of 15 kV, and a probe

current of 3.0�10�8 A. Carbon and nitrogen peak

positions were determined using synthetic silicon car-

bide and boron nitride standards, respectively. Instru-

ment calibration for all other elements was performed

on natural standards. Carbon was routinely measured

on two different spectrometers to monitor the reproduc-

ibility of observed signals.

Stable C-isotope analyses of carbonates were per-

formed by pouring 100% phosphoric acid on whole-

rock powders under vacuum [55] and analyzing the

exsolved CO2 on a Finnegan MAT 252 mass spec-

trometer at the University of Alberta. Yields of CO2 in

the samples varied from 0.011% to 19% by weight as

carbonate. The error in calculated carbonate yields

range from ~F1% to ~F15% for samples rich and

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.



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 inter-

pillow 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. 5. Photomicrographs of well-preserved interpillow hyaloclastites.

(A) Original glass shards are completely replaced by chlorite, quartz,

and epidote and the interstitial spaces are filled with quartz and calcite

(Sample 119-BG-04). There is very little evidence of deformation and

preservation of original jigsaw breccia textures between individual

glass shards is clearly visible in thin section. (B) Tubular structures

mineralized by titanite are present both within the glass shards and

along the margins of the shards in the surrounding interstitial quartz

(Sample 27C-BG-03). Inset shows interpretation of original margin of

an individual glass along which numerous titanite tubules are now

located in quartz.

Fig. 6. Individual glass shards in interpillow hyaloclastites also pre

serve fractures along which incipient alteration is observed (A). Areas

of quartz along these fractures contain irregular patches of individua

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 Am in

diameter. These textures are similar to granular microbial alteration

patterns observed at the interface between fresh glass and microbia

alteration fronts in pillow basalts (from ODP sample 148-896A, 9R-1

17–21) from in situ oceanic crust (C).

-

l

l

,

consisting of very fine-grained titanite (Fig. 3). The

development of these alteration features along fractures

is irregular and non-symmetric. Extending from these

titanite patches are mineralized tubular structures 1–10

Am in width (average 4 Am) and up to 200 Am in length

(most commonly about 50 Am; Fig. 3). Some of these

tubular structures exhibit well-defined segmentation.

The segmentation results from the partial replacement

of the titanite tubule by chlorite. Since the tubule pre-


dated the chlorite formation they must have formed

early in the alteration process (Fig. 3C). These struc-

tures have largely similar shape and size as tubular

textures found in glassy pillow rims of young pillow

lavas of in situ ocean crust (Fig. 3D).

The mineralized tubular structures are most com-

mon and best developed in the interpillow hyaloclastite

(Fig. 4) in the upper part of the Hooggenoeg Forma-

tion (dated between 3472 and 3456 Ma; [45,46]; and

de Wit, unpublished data). The interpillow hyaloclas-

tite samples show no evidence of deformation and

preserve original jigsaw breccia textures with individ-

ual glass shards clearly visible in thin section (Fig. 5)

Fig. 7. Series of X-ray element maps (C, Ca, N, P, and Ti) and backscattered

Sample 29-BG-03 from location 6. Carbon 1 and Carbon 3 refer to carbon m

the patterns observed in the two carbon maps are an artifact produced in sam

of the X-rays and the different physical orientation of the spectrometers on

spatial distribution of P and N are due to the same artifact. In the maps label

the BSE image showing the association of carbon with the margins of the t

green–yellow–red–pink. Scale bar is 20 Am.

and also in hand specimen. Original glass shards are

completely replaced by chlorite, quartz, and epidote

and the interstitial spaces are filled with quartz and

calcite. Tubular structures mineralized by titanite are

present both within the glass shards and along the

margins of the shards in the surrounding interstitial

quartz (Fig. 5). The mineralized tubular structures in

the interpillow hyaloclastite also have the same size,

shape, and distribution as those observed in the pillow

rims (Fig. 3).

Individual glass shards in interpillow hyaloclastites

also preserve fractures along which incipient alteration

is observed (Fig. 6A). These fractures contain patches

electron (BSE) images within the formerly glassy chilled pillow rim of

aps collected on spectrometers 1 and 3, respectively. The differences in

ples that are not perfectly flat by the combination of the take off angle

the microprobe (approximately 1508 apart). Slight differences in the

ed C1+BSE and C2+BSE the carbon map has been superimposed on

ubular features. Increasing order of elemental abundance black–blue–

Fig. 8. SEM–BSE images and transmitted light photomicrograph o

area mapped in Fig. 7 from Sample 29-BG-03. (A) BSE image clearly

shows a healed fracture trending from upper left to bottom right of the

image cutting the formerly glassy margin now replaced by predomi

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 o

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(C) Transmitted light photomicrograph of titanite tubules mapped in

Fig. 7 (area in box). This image clearly shows the titanite tubules are

connected to the main titanite patch below the surface and are no

isolated grains. The apparently isolated nature of some tubules in the

BSE images is an artifact of the thin section making process. Scale ba

is 50 Am.


of quartz along their length that host irregular patches

of individual and/or coalesced spherical bodies miner-

alized 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 mi-

crobial 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 micro-

probe on iridium-coated thin sections show elevated

levels of carbon, and possibly nitrogen and phospho-

rus, 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 photo-

micrograph 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 repre-

sents 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

these elements do not show enrichments and argue

against the possibility that carbon highs are due to

inorganic carbonate material (e.g., Ca, Mg, Fe) or

epoxy (e.g., Cl).

6.3. Carbon isotopes

A series of sub-samples from the outermost glassy

rims and crystalline interiors of individual pillow lavas

were carefully prepared. The bulk-rock carbonate from

the bglassyQ and bcrystallineQ sub-samples was ana-

lyzed for carbon isotope ratios in order to investigate

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-

lation between isotope ratio and carbonate abundance

is observed.

Carbon-isotope analyses of disseminated carbonate

in formerly glassy pillow rims and interpillow hyalo-

clastites, in which there are textural and geochemical

evidence for microbial activity, display a significantly

greater range in the d13C values (+3.9x to �16.4x)

f

-

)

f

.

t

r

than the crystalline interiors of pillow lavas (+0.7xto �6.9x). Secondary carbonate in vesicles has d13C

values that cluster near zero. The d13C values from

the crystalline pillow lava interiors are bracketed

between primary mantle CO2 (�5x to �7x;

[58,59]) and values close to marine carbonates (0x;

[59,60]). This distribution is very similar to that

observed in studies of ophiolites (Fig. 9B) and in

Table 1

Carbon isotope analyses of disseminated carbonates

Sample wt.% carb d13C

Glassy samples

P1A-02 1.253 �0.3

P1A-02 1.261 1.8

P1A-02 0.016 �5.7

P1A-02 1.322 0.1

P1A-02 0.02 �3.5

P1A-02 3.453 0.4

P1A-02 0.765 0.3

P1B-02 0.054 �2.6

P1B-02 2.4 3.9

P1B-02 0.057 �1.9

P2B-02 0.025 �12.7

P2B-02 0.035 �3.4

P2B-02 0.037 �4

P2B-02 0.019 �9.7

P2B-02 0.02 �7.1

P2B-02 0.03 �6.6

PB3-02 0.027 �16.7

PB3-02 0.967 0.3

PB3-02 0.011 �1.2

PB3-02 0.016 �15.6

PB3-02 0.99 0.4

PB3-02 0.81 0.5

PB3-02 1.08 0.3

8A-BG-03 0.756 �1.1

9A-BG-03 0.03 �4.4

12A-BG-03 2.336 3

14A-BG-03 4.372 0.3

17A-BG-03 0.04 �4.2

17B-BG-03 0.042 �5.7

24-BG-03 2.219 �0.1

26-BG-03 0.018 �5.1

29-BG-03 5.327 �4.8

30B-BG-03 0.027 �6.1

33-BG-03 0.033 �3.3

37A-BG-03 0.045 �6.9

37B-BG-03 0.035 �5.2

38-BG-03 0.014 �7.1

39A-BG-03 0.039 �5.2

39B-BG-03 0.035 �9.4

39C-BG-03 0.035 �6

40A-BG-03 0.031 �7.9

40B-BG-03 0.038 �1.6

40C-BG-03 0.053 �3.7

40D-BG-03 0.015 �5.8

41A-BG-03 0.027 �5.9

41B-BG-03 0.03 �7

41C-BG-03 0.029 �9.1

41D-BG-03 0.025 �4.4

42A-BG-03 0.025 �5.8

42B-BG-03 0.018 �11.3

43A-BG-03 0.019 �8.1

43B-BG-03 0.011 �8.4

43C-BG-03 0.054 �9

56-BG-03 0.05 �8.8

57-BG-03 0.065 �6.5

58A-BG-03 0.071 �1.5

58B-BG-03 0.106 �1.6

Table 1 (continued)

Sample wt.% carb d13C

Glassy samples

59A-BG-03 0.019 �2

59B-BG-03 0.025 �6.9

60A-BG-03 0.015 �5.4

60B-BG-03 0.031 �4.3

Crystalline samples

P1A-02 0.944 �0.1

P1A-02 1.989 0.7

P1A-02 3.538 0.6

P1B-02 0.7 �0.1

P1B-02 5.501 0.1

P1B-02 2.555 0.5

P1B-02 18.287 0.7

P1B-02 4.211 0.6

P1B-02 4.306 0.6

P2B-02 0.42 0

P2B-02 0.03 �6.1

PB3-02 0.332 �1.1

PB3-02 0.287 0.4

PB3-02 0.45 0

8B-BG-03 0.377 �1.8

10B-BG-03 0.152 �1.6

13B-BG-03 0.664 �0.4

15B-BG-03 0.053 �1.9

25-BG-03 5.264 �1.4

31-BG-03 0.289 �1.6

34-BG-03 3.529 �0.5

37D-BG-03 1.037 �1.1

37E-BG-03 5.903 �0.5

39D-BG-03 0.018 �2.4

39E-BG-03 3.232 �0.9

39F-BG-03 0.997 �0.9

39G-BG-03 1.208 �6.5

40E-BG-03 0.022 �2.6

40F-BG-03 0.013 �6.6

43E-BG-03 0.779 �6.4

58C-BG-03 0.049 �5

59C-BG-03 0.037 �5.9

59D-BG-03 0.052 �5.4

60C-BG-03 0.039 �6.5

Vesicles

P1A-02 15.414 0.7

P1B-02 19.094 0.5

PB3-02 2.878 0.5

wt.% carb=weight percentage carbonate. Samples listed come from

the following sites: Site 3=06 to 08-BG-03; Site 4=09 to 20-BG-03;

Site 6=24 to 29-BG-03; Site 7=30 to 46-BG-03; Site 10=56 to 58-

BG-03; and Site 11=59 to 60-BG-03. All samples listed as Pxx-02

were collected at Site 7.


situ oceanic crust (Fig. 9C). The observed shift to

lower d13C values of disseminated carbonates in the

outer glassy rim of pillow lavas is a pattern that is

interpreted to result from microbial fractionation

[7,61,62,13,11,14,63].


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

fromminute pyrite grains observed in Precambrian organ-

ic rich cherts (i.e., [64]) may initially attach some simi-

larity to the tubular structures in the present study. These

Fig. 9. Relationship between weight percent carbonate versus d13C for

the originally glassy rims (filled circles) and crystalline interiors (open

squares) of pillow lavas. (A) Analyses from pillow lavas of the Komati,

Hooggenoeg, and Kromberg Formations of the Onverwacht Group,

BGB. (B) Compilation of analyses from ophiolites worldwide [13,63].

(C) Compilation of analyses from modern oceanic crust [7,8,11].

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 inter-

preted to form by pressure solution initiated by gas

evolution from organic material that drives minute min-

eral 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-

ation features reported from glassy rims in pillow lavas

from the Troodos ophiolite ([61]; Fig. 3A and B), and

basaltic glass from in situ oceanic crust [18,2,21,3–

7,9,11,10] (Fig. 3C and D). Fig. 10 compares the

diameter of tubular structures in the BGB samples


with the diameter of tubular microbial alteration fea-

tures in modern oceanic crust. The observed distribu-

tion shows that on average the mineralized structures

found in the formerly glassy BGB samples are slightly

larger than predominantly unfilled microbial alteration

features in fresh oceanic basaltic glass. This can be

explained if the mineralized structures found in the

BGB samples were once empty corrosion structures

because it would be impossible for a mineralized tube

to be smaller than the original channel it subsequently

filled. Additionally, they may have become thicker by

metamorphic growth. The shape and distribution of the

tubular and granular structures along healed micro

fractures in the BGB lavas is identical to those found

in modern oceanic basalts (Figs. 3D, 4D, 6C).

7.2. Element distributions

The presence of carbon along the margins of the

titanite tubules in the BGB samples unrelated to carbo-

nates is interpreted to represent residual organic matter

[14]. The common association of carbon, and to a lesser

extent nitrogen and phosphorus, with suspected micro-

bial alteration textures and not elsewhere is a common

observation in basaltic glasses from modern oceanic

crust and ophiolites affected by microbial alteration

(e.g., [7,11]). The association of carbon and nitrogen

with the mineralized tubes argues for a biological origin

because abundances of these elements in igneous and

metamorphic rocks are commonly low. Our interpreta-

tion is that these elements were most likely concentrated

from seawater by microbes that colonized the originally

glassy surfaces. As the microbes dissolved the glass,

multiplied, and died, organic remains containing carbon

and nitrogen were left behind within the alteration

textures produced. These organic remnants were then

later trapped along the margins of the tubes as they

became mineralized by titanite, resulting in the elevated

signals observed. Conversely, phosphorous would have

been present in the glass matrix but likely in very low

concentrations relative to seawater. It is uncertain if

the microbes are able to extract P from the glass during

dissolution but element maps show elevated concentra-

tions of P in microbial alteration textures, likely due to

incorporation in cells.

The metabolic requirements of microbes responsible

for alteration of basaltic glass in modern samples have

not been determined. It is thought that elements in the

glass such as iron act as nutrients sought by the

microbes and are released during glass dissolution.

The possibility that the titanite tubules in the BGB

samples represent vestiges of the same microbial pro-

cess found in basaltic glass from the modern seafloor

suggests that endolithic microbes may have been an

early form of life on Earth.

7.3. Interpretation of carbon isotopes

Disseminated carbonate in the relic glassy rocks from

the BGB is lower in d13C on average (�4.6x) than in

crystalline rocks (�2.1x). The crystalline interior sam-

ples all display d13C values bracketed between Archean

marine seawater (~0F2x; [60]) and primary mantle

CO2 (�5x to �7x; [59,58]). The relic glassy samples

also extend to much lower d13C values (�16.7x) than

the crystalline rocks (�6.9x). The lowest d13C values

occur in relic glassy samples with very low carbonate

abundances (V0.054 wt.%). Such isotopic contrasts

have been documented in pillow lava rims from Phan-

erozoic and Proterozoic ophiolites (Fig. 9B) and recent

oceanic crust (Fig. 9C). The generally low d13C values of

disseminated carbonate are attributed to metabolic by-

products formed during microbial oxidation of dissolved

organic matter from pore waters [7,11,13,63]. Two relic

glassy samples from the BGB with relatively high car-

bonate contents (N2 wt.%), have d13C values (3.0x and

3.9x) above those expected for seawater carbonate

(Table 1; Fig. 9A). These high carbonate contents

argue against a seawater fingerprint and are likely the

result of an outside, possibly later, source of inorgani-

cally precipitated carbonate.

Prior to alteration and metamorphism all the basaltic

samples would have had initial magmatic d13C values

in the range of �5x to �7x [58,59]. Abiotic inter-

action with seawater would have introduced inorgani-

cally precipitated marine carbonate with d13C values

close to zero [58,60]. Based on these starting conditions

we can make some predictions regarding the observed

distribution of d13C values in the glassy and crystalline

samples. Forty-seven of the 63 relic glassy samples, all

of the crystalline samples, and all of the vesicle fillings

have d13C values between �7x and 2x. These values

are best explained as being derived from some combi-

nation of carbonate inorganically precipitated from sea-

water and magmatic CO2 values [7,11,13,63].

In contrast, the samples with d13C values lower than

�7x most likely contain an amagmatic carbon com-

ponent with low d13C. The low d13C values of carbon-

ate in the relic glassy BGB samples, particularly those

samples that contain low abundances of carbonate and

d13C valuesb�7x, are interpreted to be the result of

microbial fractionation. If the proportion of inorgani-

cally precipitated calcite (with d13C near 0x) exceeds

that resulting from precipitation of carbonate from


microbially produced CO2 during oxidation of organic

carbon, the d13C value of a sample may be greater than

�7x. This is commonly seen for samples that are

relatively rich in carbonate (Fig. 9A; Table 1).

The carbon isotope signatures are unlikely to be the

result of some later carbonate formation, more recent

extraneous respired organic matter, or a Rayleigh frac-

tionation of 13C / 12C associated with decarbonation

reactions. If the observed d13C values were due to

deposition of carbonate (such as from more recent

fluid flow) unrelated to biological activity in the glassy

margin, there is no reason that the pillow margins

should be different from the pillow interiors. Instead,

one would expect a homogenization of the isotope data

which is clearly not observed (Fig. 9A). It is also

difficult to explain why extraneous respired organic

matter would preferentially affect the pillow rims

since these would have devitrified early in the alteration

process through replacement by secondary minerals.

This is confirmed by independent petrographic evi-

dence that demonstrates alteration occurred soon after

eruption of the pillow lavas (Fig. 3C; see Section 7.4).

Because the metamorphism occurred early in the histo-

ry of these rocks there would have been no mineralogic

(i.e., different assemblage) or textural (i.e., glass versus

mineral) advantages for respired organic matter to be

deposited in the pillow margins preferentially over the

crystalline interiors since the time of initial alteration. In

addition, if the isotopic signatures observed were a

result of decarbonation reactions one would expect to

see a correlation between weight percent carbonate and

d13C value that fits a Rayleigh fractionation curve.

Instead, we observe no correlation over the d13C

range from �17x to 0x at low carbonate abundances

(b0.1 wt.%; Fig. 9A). At relatively high carbonate

contents (above ~0.1 wt.%) there is again no trend

observed and the d13C values typically fall within the

range of magmatic (�7x to �5x) and Archean ma-

rine carbonate values (~0x). Hence we consider it

unlikely that Rayleigh fractionation, a process that

may fractionate carbon isotope ratios during basalt

degassing and subsequent alteration [59], is responsible

for the pronounced spread in the d13C values of the

glassy components. Instead, the d13C pattern observed

in the Barberton pillow lavas (Fig. 9A) is best inter-

preted as resulting from similar processes observed in

recent oceanic crust and ophiolites [7,11,13,63].

7.4. Timing of microbial alteration

The question remains as to when the microbial

activity occurred. To address this question we investi-

gated the overprinting relationships between the tubular

structures and the metamorphic mineral growth. Chlo-

rite is the predominant mineral in the originally glassy

margin of the pillows, and is observed to overgrow the

titaniferous tubular structures and thus obliterate them

in some samples. In other samples fine chlorite has

caused the tubular structures to take on a segmented

character by partly overgrowing them (Fig. 3C). These

petrographic observations indicate that the tubular

structures are pre-metamorphic. Previous 40Ar / 39Ar

step-heating analyses of komatiitic basalts from the

Komati Formation give metamorphic ages of

3486F8 Ma [50]. The 40Ar / 39Ar ages overlap with

the igneous U/Pb ages of the Onverwacht Group [50–

52]. This is taken as evidence that the metamorphism

represents ocean-floor type hydrothermal alteration that

occurred soon after the crust was formed [42,54,44].

7.5. Preservation of microbial alteration textures in the

rock record

The mineralization of tubular microbial alteration

textures in the BGB samples by titanite is not a unique

occurrence. It is well known from studies of recent

oceanic basaltic glass that titanium can be passively

accumulated during etching of the glass by microbes

(e.g., [11]). This process preferentially concentrates

titanium in the channels produced by the microbes.

Titanium enrichments in tubular microbial textures are

also observed in the glassy pillow margins of ophiolitic

rocks. In samples from the Jurassic Mirdita ophiolite

(Albania) and the Stonyford Volcanics (California),

zeolite facies alteration has begun to replace the glass

(Banerjee unpublished data). In these samples open or

clay-filled tubular structures within the glass are min-

eralized by titanite as they pass into the zone of zeolite

alteration. This direct link between open or clay-filled

tubes with titanite-filled tubes suggests that the miner-

alization process follows a step-wise sequence during

progressive alteration conditions (Banerjee unpublished

data). The formation of titanite is thus an early process

that occurs at relatively low temperatures and this

mineralization process is essential if the microbially

produced structures are to be preserved for extended

periods of geological time.

8. Concluding remarks

Evidence for microbial alteration of relic glassy

basaltic rocks in the Archean BGB is widespead in

the former glassy margins of pillows and interstitial

hyaloclastites. The integrated observations suggest that


these features are the result of microbial activity and

that this microbial colonization of the glassy basaltic

rocks took place soon after eruption of the ~3.4–3.5

Ga pillow lavas. During the last decade there has been

an intense search for traces of early life on Earth. This

search has largely been confined to sedimentary rocks,

or rocks interpreted to represent sediments. The search

for traces of early life is difficult and purported bio-

markers found in Archean metasediments, either in the

form of microfossils or as chemical and isotopic tra-

cers, have been questioned (e.g., [38,31,37,34]). Our

claim of ~3.5 Ga traces of life in the originally glassy

selvages of pillow lavas and inter-pillow hyalocastites

is a new geological setting in the search for early life.

Indeed, the birthplace of life may have been connected

to the volcanic environment of the oceanic crust, such

as deep-sea hydrothermal vents (e.g., [67]). Pillow

lavas are the most common rock sequences in Archean

greenstone belts [68]. The early Earth would have

been very different if these did not represent to a

large degree submarine eruptions and some form of

oceanic crust. It may therefore be profitable for the

study of early life on Earth to examine other green-

stone belts and specifically relic glassy lavas for signs

of microbial activity. This new niche has the potential

to represent a largely unexplored Archean biomass.

Acknowledgements

This work benefited from discussions with I. H.

Thorseth and B. Robins. T. Chacko and two anony-

mous reviewers improved an early version of the

manuscript. We thank D. Resultay and M. Labbe for

help preparing thin sections, N.R. Sandsta and G.B.

Carbno for help in the field, O. Levner for help with

carbon isotope analyses, G. Braybrook for help with

the SEM, and S. Matveev for help with the electron

microprobe. Thank you to Fred Daniel of Nkomazi

Wilderness for hospitality and the Mpumalanga Parks

Board for access during field work. Financial support

to carry out this study was provided by the Norwegian

Research Council, the National Sciences and Engi-

neering Research Council of Canada, the US National

Science Foundation, the Agouron Institute, and the

National Research Foundation of South Africa. This

is AEON contribution 007.

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Documents

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