Dubiofossils from a Mars‐analogue subsurface palaeoenvironment: The limits of biogenicity criteria

Abstract

The search for a fossil record of Earth's deep biosphere, partly motivated by potential analogies with subsurface habitats on Mars, has uncovered numerous assemblages of inorganic microfilaments and tubules inside ancient pores and fractures. Although these enigmatic objects are morphologically similar to mineralized microorganisms (and some contain organic carbon), they also resemble some abiotic structures. Palaeobiologists have responded to this ambiguity by evaluating problematic filaments against checklists of “biogenicity criteria”. Here, we describe material that tests the limits of this approach. We sampled Jurassic calcite veins formed through subseafloor serpentinization, a water–rock reaction that can fuel the deep biosphere and is known to have occurred widely on Mars. At two localities ~4 km apart, veins contained curving, branched microfilaments composed of Mg‐silicate and Fe‐oxide minerals. Using a wide range of analytical techniques including synchrotron X‐ray microtomography and scanning transmission electron microscopy, we show that these features meet many published criteria for biogenicity and are comparable to fossilized cryptoendolithic fungi or bacteria. However, we argue that abiotic processes driven by serpentinization could account for the same set of lifelike features, and report a chemical garden experiment that supports this view. These filaments are, therefore, most objectively described as dubiofossils, a designation we here defend from criticism and recommend over alternative approaches, but which nevertheless signifies an impasse. Similar impasses can be anticipated in the future exploration of subsurface palaeo‐habitats on Earth and Mars. To avoid them, further studies are required in biomimetic geochemical self‐organization, microbial taphonomy and micro‐analytical techniques, with a focus on subsurface habitats.

False biosignatures on Mars: anticipating ambiguity

“…Many variations on this theme have been explored, including chemical gardens formed on the injection of acidic solutions rather than the dissolution of salts, 'inverse' chemical gardens formed on the injection of the alkaline solution into the acid and quasi-2D chemical gardens confined in a narrow space between two flat plates (see Barge et al 2015 for review). It is clear that chemical gardens can produce tubules from naturally occurring alkaline solutions and minerals, so they should not be dismissed as 'exotic' to natural environments (García-Ruiz 2000;García-Ruiz et al 2017;McMahon 2019;McMahon et al 2021).…”

“…Once solidified, they resemble fossil microorganisms, particularly Fe-mineralized fossil bacteria and fungi, in size, shape and composition. They may be relevant to the remarkable profusion of filaments composed of metal oxides, oxyhydroxides and (alumino)silicates found in siliceous and calcareous mineral deposits of all ages on Earth, including cavity fills in many volcanic and metavolcanic rocks (McMahon 2019;McMahon and Ivarsson 2019;McMahon et al 2021). Many of these are probably fossilsindeed, fossils from a deep biosphere hosted in igneous rocks, with special relevance to some scenarios for life on Marsbut some are probably not and may result from chemical-garden-like processes and/or other types of self-organization that lead to filamentous crystals and aggregates (e.g.…”

“…The sheath exteriors can accumulate a flocculent Fe-oxyhydroxide coating up to several tens of micrometres thick (Schmidt et al 2014). These microstructures are easily preserved in a silica matrix (chert) or in calcium carbonate and have a putative fossil record reaching back over million-to billion-year timescales (Dodd et al 2017;Georgieva et al 2021), although some of these purported fossils may be abiotic (Hopkinson et al 1998;McMahon 2019;Johannessen et al 2020;McMahon et al 2021). Other Fe-oxidizing bacteria (e.g.…”

Keratose sponges in ancient carbonates – a problem of interpretation

“…This grey zone comprises objects that may be considered in three types: a) biogenic but require interpretation in terms of basic taxonomic placement ( Problematica sensu lato ; Jenner & Littlewood, 2008; e.g. Paleozoic Halysis as red alga, cyanobacteria, green alga or tabulate coral; Zheng et al ., 2020), b) distinct structures but inconclusive in terms of biogenicity (dubiofossils of Hofmann, 1972), and c) distinct structures that are certainly abiotic in nature (pseudofossils, full discussion in McMahon et al ., 2021). Another aspect is that the granularity of carbonate deposits does not necessarily relate to sedimentary processes; it might be post-depositional in nature due to meio-to endofaunal activity, localized microburrow nests or even diagenesis (Debrenne et al ., 1989; Wood et al ., 1993; Pemberton & Gingras, 2005; Löhr & Kennedy, 2015; McMenamin, 2016; Wright & Barnett, 2020).…”

“…Another aspect is that the granularity of carbonate deposits does not necessarily relate to sedimentary processes; it might be post-depositional in nature due to meio-to endofaunal activity, localized microburrow nests or even diagenesis (Debrenne et al ., 1989; Wood et al ., 1993; Pemberton & Gingras, 2005; Löhr & Kennedy, 2015; McMenamin, 2016; Wright & Barnett, 2020). Furthermore, this grey zone applies to cases that extend into deep time and even touches exobiology (Cloud, 1973; e.g., biogenicity criteria for tubular filaments and lamination; chemical gardens comprising inorganic processes resulting in structures resembling organisms; molar-tooth structures; see Grotzinger & Rothman, 1996; Awramik & Grey, 2005; McMahon et al ., 2017, 2021; McMahon & Cosmidis, 2021). This range of fabrics persists throughout the Phanerozoic in various ways; examples are: the biogenicity of stromatactis and lamination (Bathurst, 1982; Bourque & Boulvain,1993; Awramik & Grey, 2005; McMahon et al ., 2021); the formation of peloids (Macintyre, 1985); the significance of the polymud fabric (Lees & Miller, 1995; Neuweiler et al ., 2009); or some drag marks, Rutgersella and Frutexites (Cloud, 1973; Retallack, 2015; McMahon et al ., 2021).…”