ASTROBIOLOGY Volume 7, Number 1, 2007 © Mary Ann Liebert, Inc. DOI: 10.1089/ast.2006.0122 Research Paper On Biogenicity Criteria for Endolithic Microborings on Early Earth and Beyond NICOLA MCLOUGHLIN,1,2 MARTIN D. BRASIER,1 DAVID WACEY,1 OWEN R. GREEN,1 and RANDALL S. PERRY1,3 ABSTRACT Micron-sized cavities created by the actions of rock-etching microorganisms known as euen- doliths are explored as a biosignature for life on early Earth and perhaps Mars. Rock-dwelling organisms can tolerate extreme environmental stresses and are excellent candidates for the colonization of early Earth and planetary surfaces. Here, we give a brief overview of the fos- sil record of euendoliths in both sedimentary and volcanic rocks. We then review the current understanding of the controls upon the distribution of euendolithic microborings and use these to propose three lines of approach for testing their biogenicity: first, a geological set- ting that demonstrates a syngenetic origin for the euendolithic microborings; second, micro- boring morphologies and distributions that are suggestive of biogenic behavior and distinct from ambient inclusion trails; and third, elemental and isotopic evidence suggestive of bio- logical processing. We use these criteria and the fossil record of terrestrial euendoliths to out- line potential environments and techniques to search for endolithic microborings on Mars. Key Words: Euendoliths—Microborings—Etch pits—Early life—Biosignatures—Extreme en- vironments—Mars. Astrobiology 7(1), 10–26. INTRODUCTION doliths that inhabit fissures and cracks in rocks are known as chasmoendoliths, those that dwell NDOLITHS ARE macro- and microorganisms within pore spaces as cryptoendoliths, and those Ethat live within rocks. Many microbial en- that actively bore into rock substrates and create doliths can tolerate extreme environmental microtubular cavities as euendoliths (Golubic et al., stresses, including repeat desiccation, intense ul- 1981). The same microorganism can adopt these traviolet irradiation, oligotrophy, and tempera- various modes of life at different stages in its life ture extremes that make them strong candidates cycle or in response to a changing external envi- for the colonization of early Earth and planetary ronment (e.g., De los Ríos et al., 2005). This arti- surfaces (e.g., Friedmann and Koriem, 1989). En- cle focuses upon intragranular microborings, 1Earth Sciences, Oxford University, Oxford, United Kingdom. 2Department of Earth Science, University of Bergen, Bergen, Norway. 3Planetary Science Institute, Seattle, Washington. 10 ENDOLITHIC MICROBORING BIOGENICITY CRITERIA 11 which can be termed trace fossils, as they record and in shell and bone substrates to understand pre- the behavior of organisms. Euendolithic micro- dation patterns (e.g., Kowalewski et al., 1989). borings are found in a range of environments that More recently, it has been discovered that euen- include marine carbonates (e.g., Campbell, 1982) doliths inhabit volcanic rocks deep beneath the and volcanic glasses (e.g., Thorseth et al., 1991, seafloor, at depths of up to 4,000 feet (e.g., Fisk et 1992; Fisk et al., 1998). Euendoliths have a higher al., 2003, and references therein), and these findings preservation potential compared to non-boring have generated many questions regarding the crypto- and chasmo-endoliths or surface and mat- metabolic strategies of these “volcanic” dwelling dwelling microorganisms, which require early euendoliths. Molecular profiling work suggests mineralization to be preserved. The recent dis- that iron and manganese cycling may be among coveries of euendoliths in modern in situ oceanic the metabolic strategies employed (Thorseth et al., crust and putative fossilized equivalents from 2001; Lysnes et al., 2004). Molecular profiling also ophiolites and greenstone belts have greatly ex- suggests that autotrophic microbes dominate the panded the range of environments in which mi- early colonizing communities in modern seafloor crobial endoliths are sought and increased their volcanics, followed by heterotrophs in older, more potential as planetary biosignatures (e.g., Furnes altered samples (Thorseth et al., 2001). et al., 1996; Fisk et al., 1998; Furnes and Muehlen- The distribution of euendolithic microborings in bachs, 2003, and references therein). Herein, we sedimentary and volcanic substrata is controlled review the nature and distribution of euendoliths by a number of variables. Light levels and hence in the terrestrial rock record and propose the first changes in paleo-depths are a key control on the synthesis of criteria for testing their biogenicity. distribution of euendoliths in carbonate substrates We then discuss approaches to searching for and that are well documented. Other important con- testing the biogenicity of candidate microborings trols are thought to include the concentration and on Mars. availability of essential nutrients in the rock ma- trix, the density of physical weaknesses such as mi- crofractures and fluid inclusion trails, the trans- parency of the rock matrix in the case of TERRESTRIAL HABITATS AND FOSSIL photosynthetic euendoliths, and the volume, Eh, RECORD OF EUENDOLITHS pH, salinity, and nutrient content of circulating flu- ids. In the case of “volcanic” euendoliths in par- Microorganisms that adopt a euendolithic ticular, these controlling variables are yet to be mode of life include archaea, bacteria, algae, and fully and systematically documented. fungi. The metabolic strategies employed range Euendolithic microorganisms have been from photosynthesis in the shallow subsurface shown by experimental studies to erode by con- (e.g., cyanobacteria living beneath translucent gruent and incongruent dissolution of the rock quartz) to chemolithoautotrophs in the deep bio- through local changes in pH (e.g., Thorseth et al., sphere. Such subsurface chemolithoautotrophs 1995; Staudigel et al., 1998). Siliceous substrates, 2ϩ 2ϩ utilize H2, H2S, S, CH4, CO, Fe , or Mn as po- for instance, exhibit a solubility minimum at cir- 3ϩ 4ϩ tential electron donors, and CO2, Fe , and Mn cum-neutral pH and become more soluble below Ϫ4 in rocks or SO2 and O2 in circulating fluids as pH 4 and above pH 8—some endoliths exploit electron acceptors (e.g., Stevens and McKinley this, by eroding by either a process of bioalka- 1995). Endolithic microborings have traditionally lization (e.g., Büdel et al., 2004) or producing or- been studied in near-surface sedimentary rocks ganic acids (e.g., Callot et al., 1987). In carbonate and biological substrates as environmental and and calcophosphatic substrates, acidification is ecological indicators. In carbonate environments, also widely suggested as the mechanism of mi- for example, microborings are used as paleo-depth croboring, e.g., Golubic et al. (1984). However, indicators. Cyanobacterial borings dominate inter- Garcia-Pichel (2006) has recently pointed out that tidal and shallow marine carbonate assemblages, oxygenic photosynthesis causes alkalization that whereas red and green algae are more abundant in can lead to carbonate precipitation, and this is ex- deeper euphotic waters, and fungal borings occur actly the opposite effect to microboring by a beneath the photic zone (e.g., Glaub et al., 2001). The process of acidification and dissolution that is presence of microborings is also used in seafloor widely envisaged. It is suggested that this ap- hardgrounds to confirm hiatuses in sedimentation parent paradox may be resolved by temporal or 12 MCLOUGHLIN ET AL. spatial separation of photosynthesis and respira- A review of the terrestrial rock record of eu- tion by euendolithic microorganisms in carbon- endolithic microborings provides some signposts ates (Garcia-Pichel, 2006). Support for spatial sep- for those engaged in the search for biosignatures aration comes from the observation that some beyond Earth. This paper does not aim to provide euendolithic cyanobacteria can bore on their an exhaustive review of the terrestrial microbor- lower surface while encrusting calcite around ing fossil record, but rather summarizes some of their exposed filaments above the substrate the major examples discussed below (see Fig. 1). (Kobluk and Rick, 1977). Indeed, a constructive Reviews of marine bioerosion can be found else- role is played by euendoliths in the lithification where (e.g., Bromley, 2004), and summaries of of Bahamian carbonate stromatolites. Here, mul- candidate microborings described from volcanic ticyclic boring by the coccoid cyanobacterium So- glasses and silicate minerals are given by Furnes lentia sp. and concurrent infilling of these borings et al. (2007) and Fisk et al. (2006), respectively. In by carbonate precipitation welds together the car- Fig. 1, fossil microborings are classified by sub- bonate grains, creating lithified stromatolite lam- stratum type, and current estimates of the time inae (Macintyre et al., 2000). ranges of likely constructing organisms are also Volcanic AITs (ambient inclusion Cyano- Fungi Algae Archea bacteria Sediments Glass (6) trails) 0Ga Polar sandstones (1) and Hawaii (7) Bahamian stromatolites (2). Ontong-Java, plateau (8) abundant microborings in Troodos ophiolite, Cyprus (9) carbonate sediments, Mirdita ophiolite, Albania stromatolites, shells, corals and bones. 0.55Ga SSOC ophiolite, Norway (10) phosphorite, Iran (unpub.) Doushantuo phosphorite, China (14) ? cyanobacterial microborings Hyella and Eohyella (3). ? Discovery Chert, W. Australia (15) cyanobacterial Gunflint Chert, Ontario microborings