as found in Nature 405, 676 - 679 (2000)
Filamentous microfossils in a 3,235-million-year-old volcanogenic massive sulphide deposit
BIRGER RASMUSSEN
Department of Geology and Geophysics, University of Western Australia , Nedlands, Western Australia 6907, Australia
The record of Archaean microfossils is sparse[1]. Of the few bona fide fossil assemblages, most are from shallow-water
settings, and they are typically associated with laminated, stromatolitic sedimentary
rocks[2-4]. Microfossils from deep-sea hydrothermal systems have not been reported in Precambrian rocks (> 544 million years old), although thermophilic
microbes are ubiquitous in modern sea-floor hydrothermal settings[5, 6], and apparently have the most ancient
lineages[7, 8]. Here, I report the discovery of pyritic filaments, the probable fossil remains of thread-like microorganisms, in a
3,235-million-year-old deep-sea volcanogenic massive sulphide deposit from the Pilbara Craton of Australia. From their
mode of occurrence, the micro-organisms were probably thermophilic chemotropic prokaryotes, which inhabited
sub-sea-floor hydrothermal environments. They represent the first fossil evidence for microbial life in a Precambrian
submarine thermal spring system, and extend the known range of submarine hydrothermal biota by more than 2,700 million
years[9]. Such environments may have hosted the first living systems on Earth, consistent with proposals for a thermophilic
origin of life[10-13].
The Pilbara Craton of Australia contains one of the most complete sections of well preserved Archaean
volcano-sedimentary rocks and is the site of several previous fossil discoveries[4,
14]. From this region, the probable fossil remains of microorganisms were identified in a volcanogenic massive sulphide (VMS) deposit at Sulphur Springs. The
deposit is located in low-strain, very low metamorphic grade (prehnite–pumpellyite facies) rocks of the northern
Soanesville belt in the eastern Pilbara Craton (Fig. 1a), and displays exceptional textural and structural preservation despite
its great age[15]. Mineralization is associated with syn-volcanic faults and lies below a regionally extensive unit of silicified
sedimentary and volcaniclastic rocks ('marker chert') which caps a succession of mafic, intermediate and felsic volcanic
rocks and syn-volcanic dacitic intrusions (Fig. 1b). These rocks are intruded by the 3,235-Myr-old co-magmatic Strelley
granite, which is synchronous with hydrothermal mineralization[16-18]. The succession was deposited in a deep marine setting,
with water depths probably exceeding 1,000 m, as indicated by volcanic textures, sedimentary facies and style of metal
precipitation[15, 16].
Figure 1 Location and geology of the Sulphur Springs deposit. a, Map showing the geology of the
northern Soanesville belt and the location of the Sulphur Springs deposit (after ref. 16). b, Stratigraphic
column of the Sulphur Springs group (after ref. 18).
The deposit (UTM grid 728976594) consists of stratabound lenses of pyrite, sphalerite, chalcopyrite, tennantite, galena,
barite and quartz, and an underlying stringer zone with veins of quartz, pyrite, chalcopyrite, and minor sphalerite and
carbonate. The lower part is characterized by massive, granular, honeycomb and filigree sulphide textures, whereas the
upper part contains dendritic, colloform and pellet textures[15]. Bitumen occurs in small quantities throughout the deposit as
blocky fragments and films that are intergrown with sulphides, and oil is present as fluid inclusions in hydrothermal
barite[19]. The deposit displays an upward and outward zonation from Cu to Zn–Pb, a diagnostic feature of VMS-style
mineralization. Galena from the deposit gives a Pb–Pb model age of 3,260 Myr (ref. 15). The composition of the ore
indicates that fluid temperatures probably reached 300 °C (ref. 15), but distal areas were probably much cooler. Much of
the mineralization formed by replacement of volcanic and volcaniclastic rocks close to the sea floor16, although it has been
argued that open-space sulphide textures indicate a setting resembling black-smoker chimneys at hydrothermal
vents[15].
Polished thin sections from the deposit were examined by optical microscopy (using transmitted and reflected light) and
scanning electron microscopy. Filaments are located in the siliceous cores and bands of colloform structures (Fig. 2a, b)
from samples in the upper part of the deposit. These rocks consist of pyrite and microcrystalline quartz (chert), with minor
sphalerite, chalcopyrite, tennantite, arsenopyrite, galena, chlorite and carbonate, and up to 10% of silicified volcanic rock
fragments. The colloform structures range in size from <0.1 mm to several centimetres, and include botryoidal, coalesced
and branching forms. The structures are almost entirely composed of inclusion-rich pyrite, and are enclosed by
paragenetically late chert. Much of the pyrite has been recrystallized to massive pyrite by the influx of late-stage
hydrothermal fluids, and many of the structures show evidence of progressive replacement by later sulphides.
Figure 2 Remnant cores and bands containing filaments. a, Silica-rich colloform cores containing
filaments, surrounded by replacive pyrite (gold). Combined transmitted and reflected light (TL and
RL) photographic montage. b, Thin banded layer containing filaments within paragenetically early chert (TL and
RL). c, Detail of a showing the partial replacement of quartz-rich colloform structures displaying fine-scale
lamination (TL and RL). Scale bar is 1 mm for a, b and 0.1 mm for c.
The banding and concentric textures preserved in many colloform structures are defined by inclusions after the incomplete
replacement of original minerals by pyrite (Fig. 2c). In the few samples where original minerals are preserved, they
comprise inclusion-rich chert, coarse quartz crystals and rare carbonate rhombs. Although most of the microcrystalline
silica has been recrystallized to coarser quartz, some fine morphological detail is preserved as banding. Individual laminae
are typically 5–50 µm thick, and are defined by alternating light and dark zones and by trails of irregular pyrite crystals that
extend across interlocking quartz crystals. The colloform cores also contain later infilling aggregates of siderite,
inclusion-free quartz and chlorite. The colloform structures are cut by fibrous quartz veins that also contain minor chlorite,
carbonate, sphalerite and pyrite, which extend up to a few millimetres into the surrounding pyrite ( Fig. 2a).
The filaments are located in the paragenetically early chert and coarse-grained quartz, and are absent in later generation
silica, carbonate, chlorite and sulphide. The filaments are threadlike, unbranched and of uniform thickness along their length
(0.5–2 µm in diameter, up to 300 µm long). They include straight, sinuous and sharply curved morphologies which are
intertwined where they are densely distributed (Fig. 3a–f ). They are abundant, with over 300 filaments in a 5 mm
10 mm area in one polished thin section (30 µm thick). In reflected light, the filaments appear to be almost entirely
composed of many sub-micrometre-sized pyrite crystals. In the cores of colloform structures, most filaments appear to be
randomly oriented, but towards the outer margins they are aligned parallel to concentric layering (Fig. 3g) or, less
commonly, are oriented sub-perpendicular to the banding ( Figs 3h, 4). In some bands (<1 mm to 20 mm long) most
filaments lie parallel to lamination ( Fig. 4). The filaments extend across the interlocking crystal boundaries of early chert,
coarse quartz and carbonate rhombs, and in places are disrupted and displaced by silica-filled penetrative fractures (Fig.
3f).
Figure 3 Photomicrographs of filaments from the Sulphur Springs VMS deposit. Scale bar, 10 µm. a–f,
Straight, sinuous and curved morphologies, some densely intertwined. g, Filaments parallel to the
concentric layering. h, Filaments oriented sub-perpendicular to banding.
Figure 4 Rose diagram showing filament orientation relative to lamination for colloform structures and
banded layers using 5° subdivisions.
The filaments can be traced through different focal levels within thin sections, and are present in several thin sections of the
same sample and in many samples from various parts of the deposit. Because the samples are from subsurface
(300–350 m) diamond drill-core, well below the water table and with no evidence of weathering, emplacement by modern
surface fluids can be dismissed. Thus, the filaments are indigenous to the host rocks. The presence of filaments within
paragenetically early minerals which are almost completely replaced by later sulphides and their disruption by cross-cutting
fractures indicates that they are syngenetic and were lithified before the main stage of sulphide mineralization, coincident
with granitoid intrusion 3,235 Myr ago[18].
A biogenic origin is inferred for the filaments from their sinuous morphology, length-wise uniformity and intertwined habit,
which are comparable to those of Archaean and younger microfossils[1-4, 20]. They are entirely dissimilar to abiogenic
filamentous microstructures formed by the displacement of carbonaceous matter during crystal growth or the movement of
ambient pyrite crystals[21, 22]. The limited range of morphotypes may reflect selective diagenetic
preservation[23] or low initial diversity. Perhaps most significantly, the changes in preferred orientation of filaments in different areas of the colloform
structures may indicate behavioural variations in different micro-environments, a distinctly biological feature. Similar patterns
are evident in modern microbial mats[24] and hot-spring communities[25], indicating a biotic tropism or taxis in response to a
gradient or fluctuation in a salient ecological parameter. It therefore seems reasonable to infer that the Sulphur Springs
filaments are probably biogenic, and as such, represent the best available evidence for microbial life in a hydrothermal
setting during the Precambrian.
Although it is difficult to ascribe metabolic characteristics to fossilized microbes on the basis of
morphology[1, 2], some information can be inferred from their mode of occurrence. In the Sulphur Springs deposit, the presence of volcanic rock
fragments in many of the fossiliferous samples and their location below a silicified cap of sedimentary and volcaniclastic
rocks indicate that the microorganisms probably lived in the pores and crevices of rocks at shallow depths below the sea
floor. In such a setting, proximal hydrothermal fluids would have delivered a near-continuous supply of nutrients and metals
essential for growth[12]. The filaments, which probably acted as nucleation
sites[25, 26], were consequently engulfed by paragenetically early silica, which precipitated as mineral-charged hydrothermal fluids cooled upon approaching the sea
floor. As the hydrothermal system evolved, with the formation of hotter fluids owing to the emplacement of the Strelley
Granite, the early, low-temperature silica was progressively replaced by pyrite and later sulphides. Although there were
several episodes of silicification, with resultant cementation of pores and replacement of precursor sedimentary and
volcaniclastic rocks, it is unclear whether the early silica was generated during volcanism, syn-volcanic intrusion or the
earliest stage of granite intrusion.
Given that the filamentous microfossils are encased in hydrothermal silica, and are within a VMS deposit, it seems likely
that the microbiota were thermophiles, inhabiting 'low-temperature' (<110 °C) sub-sea-floor niches adjacent to discharging
hydrothermal fluids. The oil in the deposit[19] indicates that hydrocarbons entrained by circulating fluids may have provided
readily bioavailable energy and carbon sources for microorganisms living around the hydrothermal
system[6, 27, 28]. The great water depth (>1,000 m) and sediment cover would have offered protection from ultraviolet radiation, and imply that the
filamentous microbiota could not have derived energy for growth through light-dependent processes; instead they must
have used chemical pathways for metabolic processes. The abundance of reduced chemical species in sea-floor
hydrothermal fluids and the probable absence of dissolved oxygen in the Archaean deep
ocean[29] indicates that these pathways were probably anaerobic. As in modern deep-sea hydrothermal
systems[5, 6], the abundance of reduced sulphur in the hydrothermal fluids and the encrustation of filaments by pyrite indicate that sulphur may have been central
to energy-yielding reactions for microbial growth.
Although modern deep-sea hydrothermal systems host diverse microbial
communities[5, 6], reports of microfossils are rare for ancient deposits[9, 30] and nonexistent for Archaean rocks. Indeed, the oldest fossil microorganisms reported are
filamentous bacteria from Cambrian–Ordovician silica–iron oxide exhalites from northeastern
Australia[9]. The discovery of probable microfossils in the Sulphur Springs VMS deposit suggests that a chemotrophic deep-sea hydrothermal biosphere
thrived over 3,235 Myr ago, some 2,700 Myr before previously described
assemblages[9]. Given the likely abundance of submarine thermal springs on the early
Earth[12], it is possible that microbial communities flourished in similar settings well
before the Sulphur Springs microorganisms, consistent with proposals for a thermophilic origin of
life[7, 8, 12, 13] in deep-sea hydrothermal environments[10, 11].
References
1. Schopf, J. W. in The Proterozoic Biosphere (eds Schopf, J. W. & Klein, C.) 25-39 (Cambridge Univ. Press, New York, 1992).
2. Schopf, J. W. & Walter, M. R. in Earth's Earliest Biosphere: Its Origin and Evolution (ed. Schopf, J. W.) 214-239
(Princeton Univ. Press, Princeton, 1983).
3. Walsh, M. M. & Lowe, D. R. Filamentous microfossils from the 3,500-Myr-old Onverwacht Group, Barberton Mountain Land, South Africa. Nature 314, 530-532 (1985).
4. Awramik, S. M., Schopf, J. W. & Walter, M. R. Filamentous fossil bacteria from the Archean of Western Australia.
Precambr. Res. 20, 357-374 (1983).
5. Jannasch, H. W. & Mottl, M. J. Geomicrobiology of deep-sea hydrothermal vents. Science 229, 717-725 (1985).
6. Karl, D. M. The Microbiology of Deep-Sea Hydrothermal Vents (CRC, Boca Raton, 1995).
7. Kandler, O. in Early Life on Earth Nobel Symposium 84 (ed. Bengtson, S.) 152-160 (Columbia, New York, 1994).
8. Stetter, K. O. in Evolution of Hydrothermal Ecosystems on Earth (and Mars?) Ciba Foundation Symposium 202
(eds Bock, G. R. & Goode, J. A.) 1-10 (Wiley, Chichester, 1996).
9. Duhig, N. C., Davidson, G. J. & Stolz, J. Microbial involvement in the formation of Cambrian sea-floor silica-iron oxide deposits, Australia. Geology 20, 511-514 (1992).
10. Corliss, J. B., Baross, J. A. & Hoffman, S. E. An hypothesis concerning the relationship between submarine hot springs and the origin of life on Earth. Oceanol. Acta 4, 59-69 (1981).
11. Russell, M. J. & Hall, A. J. The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J. Geol. Soc. Lond. 154, 377-402 (1997).
12. Nisbet, E. G. & Fowler, C. M. R. in Tectonic, Magmatic, Hydrothermal and Biological Segmentation of Mid-Ocean Ridges Geological Society Special Publication 118 (eds MacLeod, C. J., Tyler, P. A. & Walker, C. L.) 239-251 (The Geological Society, London, 1996).
13. Huber, C. & Wchtershuser, G. Peptides by activation of amino acids with CO on (Ni,Fe)S surfaces: Implications for the origin of life. Science 281, 670-672 (1998).
14. Schopf, J. W. & Packer, B. M. Early Archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona Group, Australia. Science 237, 70-73 (1987).
15. Vearncombe, S. et al. 3.26 Ga black smoker-type mineralization in the Strelley Belt, Pilbara Craton, Western Australia. J. Geol. Soc. Lond. 152, 587-590 (1995).
16. Morant, P. The Panorama Zn-Cu VMS deposits, Western Australia. Bull. Aust. Inst. Geosci. 16, 75-84 (1995).
17. Brauhart, C. W., Groves, D. I. & Morant, P. Regional alteration systems associated with volcanogenic massive sulphide mineralisation at Panorama, Pilbara, Western Australia. Econ. Geol. 93, 292-302 (1998).
18. Buick, R. et al. Geochronology of the Sulphur Springs Group and Strelley Granite: a temporally distinct igneous province in the Archaean Pilbara Craton, Australia. Precambr. Res. (submitted).
19. Rasmussen, B. & Buick, R. Oily old ores: Evidence for hydrothermal petroleum generation in an Archean volcanogenic massive sulphide deposit. Geology (in the press).
20. Trewin, N. H. & Knoll, A. H. Preservation of Devonian chemotrophic filamentous bacteria in calcite veins. Palaios 14, 288-294 (1999).
21. Knoll, A. H. & Barghoorn, E. S. Ambient pyrite in Precambrian chert: New evidence and a theory. Proc. Natl Acad.
Sci. USA 71, 2329-2331 (1974).
22. Buick, R. Microfossil recognition in Archean rocks: An appraisal of spheroids and filaments from a 3500 m.y. old chert-barite unit at North Pole, Western Australia. Palaios 5, 441-459 (1991).
23. Knoll, A. H., Strother, P. K. & Rossi, S. Distribution and diagenesis of microfossils from the Lower Proterozoic Duck Creek Dolomite, Western Australia. Precambr. Res. 38, 257-279 (1988).
24. Bauld, J., D'Amelio, E. & Farmer, J. D. in The Proterozoic Biosphere (eds Schopf, J. W. & Klein, C.) 261-269 (Cambridge Univ. Press, New York, 1992).
25. Jones, B., Renaut, R. W. & Rosen, M. R. Biogenicity of silica precipitation around geysers and hotspring vents, North Island, New Zealand. J. Sed. Res. 67, 88-104 (1997).
26. Ferris, F. G., Beveridge, T. J. & Fyfe, W. S. Iron-silica crystallite nucleation by bacteria in geothermal sediment. Nature 320, 609-611 (1986).
27. Bazylinski, D. A., Wirsen, C. O. & Jannasch, H. W. Microbial utilization of naturally-occurring hydrocarbons at the Guaymas Basin hydrothermal vent site. Appl. Environ. Microbiol. 55, 2832-2836 (1989).
28. Rueter, P. et al. Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature 372, 455-458 (1994).
29. Kasting, J. F. Earth's early atmosphere. Science 259, 920-926 (1993).
30. Juniper, S. K. & Fouquet, Y. Filamentous iron-silica deposits from modern and ancient hydrothermal sites. Can. Mineral. 26, 859-869 (1988).