Reassessing the biogenicity of Earth’s oldest trace fossil with implications for biosignatures in the search for early life Eugene G. Grosch1 and Nicola McLoughlin Department of Earth Science and Centre for Geobiology, University of Bergen, N-5007 Bergen, Norway Edited* by Norman H. Sleep, Stanford University, Stanford, CA, and approved April 28, 2014 (received for review February 10, 2014) Microtextures in metavolcanic pillow lavas from the Barberton argued biogenic origin from pillow lavas of the in situ oceanic greenstone belt of South Africa have been argued to represent crust and ophiolites (1, 2, 9). In young, in situ pillow lavas, Earth’s oldest trace fossil, preserving evidence for microbial life abundant microbial DNA and geochemical signatures support in the Paleoarchean subseafloor. In this study we present new in the presence of a deep subseafloor biosphere (10, 11). Given situ U–Pb age, metamorphic, and morphological data on these therefore the major implications that the Archean titanite titanite microtextures from fresh drill cores intercepting the type microtextures may hold for the earliest evidence of life on Earth, locality. A filamentous microtexture representing a candidate bio- we have conducted syngenicity and biogenicity tests to evaluate signature yields a U–Pb titanite age of 2.819 ± 0.2 Ga. In the same a proposed subseafloor bioalteration model for their origin. We drill core hornfelsic-textured titanite discovered adjacent to a local report in situ U–Pb dating of the titanite, quantitative microscale mafic sill records an indistinguishable U–Pb age of 2.913 ± 0.31 Ga, mapping of metamorphic conditions, and morphological evi- overlapping with the estimated age of intrusion. Quantitative mi- dence to evaluate the biogenicity of the titanite microtextures. croscale compositional mapping, combined with chlorite thermo- dynamic modeling, reveals that the titanite filaments are best Results developed in relatively low-temperature microdomains of the The titanite microtextures were originally described from pillow chlorite matrix. We find that the microtextures exhibit a morpho- lavas of the ca. 3.472-Ga Hooggenoeg Formation of the BGB logical continuum that bears no similarity to candidate biotextures ca. EARTH, ATMOSPHERIC, that stratigraphically overlies 3.482 Ga ultramafic komatiites AND PLANETARY SCIENCES found in the modern oceanic crust. These new findings indicate of the Komati Formation (Fig. S1). The current study includes that the titanite formed during late Archean ca. 2.9 Ga thermal samples from drill core KD2b of the Barberton Scientific Dril- contact metamorphism and not in an early ca. 3.45 Ga subseafloor ling Project (BSDP) that intercepted the pillow lava type section environment. We therefore question the syngenicity and biogenic- for the proposed biotextures (12, 13) (Fig. S1). Petrographic ity of these purported trace fossils. It is argued herein that the investigation of the drill core samples reveals that the original titanite microtextures are more likely abiotic porphyroblasts of titanite bioalteration textures (1) form part of a morphological thermal contact metamorphic origin that record late-stage retro- continuum that was previously only partially illustrated. The size, grade cooling in the pillow lava country rock. A full characteriza- morphology, and distribution of these titanite microtextures are tion of low-temperature metamorphic events and alternative evaluated against biogenicity criteria proposed for endolithic biosignatures in greenstone belt pillow lavas is thus required microborings (14, 15). The simplest morphological endmember before candidate traces of life can be confirmed in Archean is hornfelsic titanite spheres (Fig. 1 A–E) that may coalesce to subseafloor environments. form irregular bands. The spheres and bands develop filamentous Archean habitats | astrobiology | Archean Earth | ichnofossil | bioalteration Significance ilamentous titanite microtextures in ca. 3.472–3.432 Ga It has been argued that Archean subseafloor pillow lava Fmetavolcanic pillow lavas of the Barberton greenstone belt sequences provide an environment in which to seek evidence (BGB), South Africa, have been argued to represent Earth’s for the earliest traces of life. Candidate titanite biosignatures oldest trace fossils (1–4). Subsequent work in other Archean of microbial activity have been reported in ∼3.45-Ga meta- terrains, such as the Pilbara Craton of Western Australia and the volcanic glass from the Barberton greenstone belt of South Abitibi greenstone belt of Canada, have made similar claims for Africa. In this paper we present new in situ U–Pb age data, trace fossils in early metabasaltic pillow lavas (5, 6). The current metamorphic constraints, and morphological observations on paradigm for these titanite microtextures involves a complex these titanite microtextures. Our data challenges a biological bioalteration model in which endolithic microbes form hollow origin for these oldest purported trace fossils, with implications microtunnels by etching fresh volcanic glass in submarine envi- for the ecological niches where life may have first emerged. We ronments on the early Earth (1–7). Subseafloor hydrothermal therefore suggest alternative biosignatures and approaches alteration is envisioned not only to provide a suitable environ- should be considered in the search for subsurface life on early – ment for microbial activity, but also to result in mineralization of Earth and in extraterrestrial mafic ultramafic rocks, for exam- ple, in martian basalts. the hollow tubes by titanite (CaTiSiO5) preserving the proposed trace fossils (1–3). Thus, it has been suggested that volcanic Author contributions: E.G.G. designed research; E.G.G. and N.M. performed research; E.G.G. habitats represent a previously unexplored geological setting in and N.M. contributed new reagents/analytic tools; E.G.G. and N.M. analyzed data; and which life may have thrived and possibly originated on the early E.G.G. wrote the paper. Earth (1–3). It has also been argued that similar microtextures in The authors declare no conflict of interest. altered extraterrestrial basalts may provide a useful biosignature *This Direct Submission article had a prearranged editor. in the search for life on Mars and beyond (8). Freely available online through the PNAS open access option. The principal argument for a biogenic origin of the purported 1To whom correspondence should be addressed. E-mail: [email protected]. Archean trace fossils is based on their apparent similarity in size, This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. shape, and distribution to partially mineralized microtubules of 1073/pnas.1402565111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1402565111 PNAS Early Edition | 1of6 Downloaded by guest on September 26, 2021 Fig. 1. Titanite microtextures in Archean metavolcanic pillow lavas now comprising a chlorite dominated matrix, compared with partially mineralized microtunnels from younger oceanic crust. (A–F) A continuum of titanite microtextures from spheres with or without filamentous projections, to well- developed clusters with radiating filaments, LA tracks for U–Pb titanite dating are shown (white bands in C). (G) Partially mineralized microtubules radiating at high angles from a fracture in volcanic glass from Ocean Drilling Program hole 418A in the West Atlantic. (H) Curvilinear and spiral-shaped (Inset) microtunnels in volcanic glass of the Troodos ophiolite Cyprus (drill core CY-1A). (I) Histogram of measured Archean titanite filament widths (n = 303) in 12 samples from the Barberton drill core showing that they are much larger in diameter (dark green line = mean of 12 μm and light green band = SD) and span a wider range compared with microtubules in younger volcanic glass (dark purple line = mean of 1.3 μm and light purple band = SD, replotted from ref. 2). (Scale bars: 50 μm A–H except G and H, Insets, which are 10 μm.) projections (Fig. 1 A, C, and D), showing a growth continuum indicate no morphological similarity between the Archean from spheres with one or two short projections to larger clusters titanite microtextures and the modern tubular bioalteration of titanite microtextures with more numerous and longer pro- textures. jections (Fig. 1 B and D–F; Fig. S2). The latter morphotype with As a syngenicity test, the U–Pb age of titanite growth was well-developed titanite filaments has been the focus of all pre- determined by in situ measurements using single- and multi- vious studies but forms only a less abundant endmember of collector laser ablation, inductively coupled plasma mass spec- the morphological continuum. The individual filaments are trometry (LA-ICP-MS). Further details on the methods and highly variable in length (e.g., Fig. 1F, from 14 to 460 μm) and SI Materials and Methods μ analytical standards are presented in . width (from 2 to 39 m) and are either constant in diameter, The 207Pb/206Pb and 238U/206Pb isotopic ratios measured by tapered (Fig. 1E), or club shaped (Fig. 1G). The filaments do not single-collector LA-ICP-MS on spherical hornfelsic titanite uniquely radiate at high angles from titanite “root zones” as in (sample B77) are plotted on a Tera–Wasserburg Concordia modern oceanic basalts (Fig. 1 G and H), but rather at varying diagram (Fig. 2; Tables S1 and S2). The measured U–Pb and angles from irregular titanite bands and spheres disseminated – throughout the chlorite matrix (Fig. 1 E and F). The new drill Pb