Microbial Palaeontology and the Origin of Life: a Personal Approach

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A Bollettino della Società Paleontologica Italiana, 55 (2), 2016, 85-103. Modena L

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N N Invited Paper N Microbial palaeontology and the origin of life: a personal approach

Frances Westall

F. Westall, CNRS-Centre de Biophysique Moléculaire, Rue Charles Sadron, CS 80054, Orléans cedex 2, France; [email protected]

Key words - Microbial palaeontology, Early Archaean, Origin of life, Extraterrestrial life.

ABSTRACT - Palaeontology is an essential tool for tracing the history of life in the geological record. However, access to the origin of life is blocked because of the lack of preservation of suitable rocks dating from the fi rst billion years of Earth’s history. Nevertheless, study of Early Archaean rocks (~4-3.3 Ga) indicates that the environmental conditions of the early Earth, upon which life emerged, were very different to those of today and provides essential information for guiding investigations into the origin of life in terms of realistic environmental scenarios and possible timing of the appearance of life. Microbial palaeontology investigations of well-preserved, Early Archaean rocks ~3.5 to 3.3 Ga show that the earliest preserved life was diverse and widespread and suggest that it probably appeared in the Hadean, as soon as the Earth’s surface was habitable. The extreme, anaerobic conditions characterising the early Earth, together with the ingredients of life, i.e. carbon molecules, liquid water and energy, were common on other planets and satellites in the early Solar System. Considering carbon and water-based life forms to be a cosmically frequent phenomenon, it is hypothesised that life could have emerged on some of these bodies and that traces of its appearance may still be preserved, for instance on Mars, Europa or Enceladus. Microbial palaeontology as well as information gleaned from extant extremophiles and experimental data provides us with essential information about what kinds of extant or fossilised life forms to look for on another planet or satellite. Moreover, the methods evolved to study and understand the remains of fossil traces of primitive microbial life will aid the search for life and its origins on Mars or other satellites. The perspective of returning to Earth rocks from Mars (or other samples from Europa or Enceladus?) containing potential traces of extraterrestrial life, most likely primitive anaerobic chemotrophs, will be a challenge for microbial palaeontology that we need to start addressing now. Most importantly, it will open up the possibility of establishing the universality of life.

RIASSUNTO - [L’origine della vita e la Paleontologia Microbica: il punto di vista dell’autore] - La Paleontologia è uno strumento essenziale per la ricostruzione della vtoria della vita sulla base di informazioni conservate nel record geologico e dell’evoluzione geo-biologica del nostro Pianeta. Lo studio dell’origine della vita e, quindi, delle prime forme in cui essa apparve, è reso inevitabilmente complicato dalla scarsa disponibilità di rocce terrestri più antiche di 3,5 miliardi di anni, e, in generale, dal loro stato di conservazione. Tuttavia, grazie allo studio delle rocce della prima parte dell’eone Archeano (da ~4,0 a ~3,2 Ga), ovvero fra le rocce più antiche del nostro Pianeta, oggi sappiamo non solo che le condizioni ambientali della Terra primitiva, sulla quale la vita si sviluppò, erano profondamente differenti da quelle attuali, ma abbiamo anche ottenuto informazioni (geologiche e ambientali) essenziali per indirizzare la ricerca sulla sua origine in termini di ricostruzione di scenari ambientali realistici e dei potenziali step evolutivi (almeno in termini di metabolismi possibili) da essa seguiti. Studi di paleontologia microbica condotti negli ultimi anni in rocce sedimentarie e vulcaniche del Paleoarcheano (da ~3,6 a 3,2 miliardi di anni), hanno rivelato la presenza di abbondanti forme di vita (di tipo microbico) fra le più antiche oggi note, diversifi cate, abbastanza evolute e complesse, nonché diffuse in differenti habitat. Inoltre, è stato stabilito che molto probabilmente la vita popolò il nostro Pianeta già all’inizio dell’Archeano, e, forse, già durante l’eone Adeano (~4,6-4,0 Ga), quando il nostro Pianeta era già potenzialmente abitabile (~4,4 Ga). Le condizioni ambientali estreme e fortemente anaerobiche che caratterizzavano la Terra primitiva, e gli ingredienti per la vita così come noi la conosciamo (per es., molecole di carbonio, elementi bio-essenziali, acqua liquida e sorgenti di energia), erano aspetti che il nostro Pianeta aveva in comune con altri pianeti e satelliti del neonato sistema solare. Allora, pensando alla vita basata sul carbonio e acqua (come è il caso della vita terrestre che comunque ad oggi è l’unica conosciuta) come ad un fenomeno cosmico comune nell’Universo (carbonio e acqua nei differenti stati fi sici sono elementi comuni dell’Universo), è stato ipotizzato che essa potrebbe essersi originata anche su altri pianeti o satelliti dove, possibilmente, queste tracce (di tipo microbico) potrebbero ancora essere conservate nel relativo record roccioso, come per esempio potrebbe essere il caso di Marte, Europa o Encelado. Oggi la paleontologia microbica che si occupa di studiare fossili microbici di tipo procariotico nel record fossile dall’Archeano al Recente con una attenzione particolare allo studio di ambienti estremi moderni e fossili e allo studio in laboratorio di processi tafonomici e di fossilizzazione, di biomineralogia e geomicrobiologia (relazioni microbi-minerali), ci fornisce informazioni preziose circa quali forme di vita (microrganismi viventi o fossili) e quale strategia seguire nella ricerca della vita fuori dal nostro Pianeta. Così i metodi investigativi messi a punto per studiare, riconoscere e comprendere i resti fossilizzati di forme di vita primitiva (procarioti), potrebbero essere importanti sia per riconoscere tracce di vita terrestri sempre più antiche (per es., gechimica isotopica e tracce molecolari), sia per la ricerca di vita e delle sue origini su Marte o su altri pianeti o satelliti. La possibilità di riportare sulla Terra rocce da Marte (o da Europa o Encelado), che potrebbero contenere tracce di vita extraterrestre, molto probabilmente di tipo procariotico, anaerobico e chemiotrofi co, sono gli obiettivi delle imminenti missioni spaziali, e nello stesso tempo una grande sfi da per la paleontologia (microbica) e una opportunità per i paleontologi di mettere a punto strategie investigative (alla scala micro- e nano- metrica) nel tentativo di stabilire l’universalità della vita.

INTRODUCTION and large impacts; Kamber, 2015, Fig. 1), we have no direct evidence of the appearance of the fi rst cellular life Palaeontology is the most important tool for studying and its earliest evolution. Nevertheless, well-preserved, the history of life. Unfortunately, owing to the non- Early Archaean rocks, 3.5 to ~3.3 Ga, provide essential preservation of suitable rocks older than 3.5 Ga on Earth information about the environment in which life appeared (Hadean crust having been recycled by tectonic activity and evolved, documenting a planet that was habitable for

ISSN 0375-7633 doi:10.4435/BSPI.2016.09 86 Bollettino della Società Paleontologica Italiana, 55 (2), 2016

Fig. 1 - Distribution of Archaean cratons showing the locations of the Pilbara Craton in northwest Australia and the Barberton Greenstone Belt in South Africa (drawn from many sources). The latter two, dating from 3.5 Ga, are the only two cratons where Early Archaean sedimentary rocks are well preserved. anaerobic microorganisms but completely different to the all that remain of a history that was perhaps already many present day Earth. Thus, because of the lack of crust old hundreds of millions of years old. enough to have preserved traces of the transition from Nevertheless, the remains of early life, although prebiotic molecules to cellular life, study of the oldest relatively evolved compared to what must have been preserved fossil remains and the environmental context in the first cellular life forms, provide precious indications which they occur is an important means of approaching the concerning the kinds of life forms that first appeared and, emergence of life. Morphological and chemical microbial especially, the environment in which the emergence of life traces dating back to 3.5 Ga tell us that life was already likely took place. Moreover, the environmental context evolved, phototrophs coexisting with chemotrophs in an of the preserved biosignatures is important not only for anaerobic world and widely distributed (Walsh, 1992; aiding interpretation and identification of early life, indeed Hofmann et al., 1999; Tice & Lowe, 2004; Westall et al., it is indispensable for understanding, but it is also of 2011a, b). But when did life emerge? Many hypotheses critical importance for understanding the early habitable suggest that life could not have appeared until after the conditions of the Earth. Thus, microbial palaeontology end of the hypothesised period of heavy bombardment studies of early traces of life provide invaluable (~4.0-3.85 Ga; Ryder et al., 2000) but the degree of information related to the origin of life. However, the evolution of life demonstrated already by 3.5 Ga, plus lack of Hadean crust is a huge limitation. Nevertheless, if its global distribution, suggest that the emergence of life life appeared as a natural evolution of chemical processes may have occurred during the Hadean and, theoretically, (de Duve, 1995), it could have appeared on any other as soon as water had condensed on Earth’s surface and extraterrestrial body having environmental conditions had reached a balmy temperature of about 100°C (e.g., similar to those on the early Earth. This includes Venus Westall, 2012; Cavalazzi & Barbieri, 2016; Cavalazzi and Mars during their early histories, as well as a number et al., 2016). Models indicate that water condensation of other satellites that now have icy crusts, such as occurred rapidly after the Moon-forming impact (~4.5 Europa and Calisto, orbiting Jupiter, and Enceladus and Ga) but the earliest direct evidence for its presence dates Titan around Saturn (e.g., Westall & Brack, 2016). All of back to 4.35 Ga, the age of recycled zircon crystals formed them had water in contact with hot rock and a constant by fractionation of hydrated crust (Mozjsis et al., 2001). stream of prebiotic molecules arriving in meteorites, The Early Archaean rocks, in which the earliest preserved micrometeorites and cometary dust particles, as well as traces of life occur, formed a billion years after the massive carbon molecules formed in situ on the planets. impact that formed the Moon (Kleine et al., 2009) and well One of the major objectives of the on-going mission after the appearance of habitable conditions. We do not Mars Science Laboratory and its rover Curiosity and the know how long it took for life to appear (Orgel, 1998) but future missions ExoMars-2020 (Europe/Russia) and Mars those working in the origins of life field consider that the 2020 (NASA) is the search for traces of past life on the process had to have been relatively rapid, i.e. probably less surface of Mars. In this respect, microbial palaeontology than a few million years rather than hundreds of millions investigations of the oldest traces of life on Earth are of years. Thus, the precious traces in rocks 3.5-3.3 Ga are invaluable because they show us the nature of early life, F. Westall - Early life 87 how it is preserved, the types of signatures that can be used largely anaerobic until the advent of the mutation that led to identify it, the challenges involved in its identification, to oxygenic photosynthesis sometime in the Late Archaean and the analytical methods needed to study it (Westall et (Buick, 2008). At first a poison for all life forms except al., 2015a). Without these studies it would not be possible the oxygenic photosynthesisers, many microbes adapted to search for life on Mars or elsewhere. to the presence of small amounts of oxygen, becoming In the following, I will set the scene by describing the micro-aerophilic to completely oxygenic. Nevertheless, environment of the early Earth in order to decipher and more than two billion years were needed before the reconstruct the potential early habitat. This is important reduced surface of the Earth was oxidised sufficiently for because the Hadean-Early Archaean Earth can be viewed oxygen to start building up in the atmosphere (Zahnle & environmentally as a totally different planet and therefore Catling, 2016). the early life forms living on it were very different from One corollary of the high radiation flux is that early even the simplest of microbes living on Earth today - life must have developed efficient strategies to deal with they were what would today be termed as extremophiles radiation damage. We will see below that there is plenty (e.g., Arndt & Nisbet, 2012). I will then describe the of evidence of life in early Archaean shallow water biosignatures preserved, and the diversity and distribution environments and even briefly exposed on the beach of early life. Finally, I will address the implications of (cf. Westall et al., 2006a, 2011b). Perhaps early life used early life for the search for life on Mars and on the icy strategies similar to those used by microbes living today satellites, Europa and Enceladus. in environments exposed to high doses of radiation, such as UV-protective pigmentation, thick layers of polymer (extracellular polymeric substances, EPS), protection from THE HADEAN-EARLY ARCHAEAN ENVIRONMENT layers of minerals, an efficient gene repair mechanism, rapid cell division, and rapid development of radiation-resistant The Hadean/Early Archaean Earth was volcanic and mutants (e.g., Vítek et al., 2010; Moeller et al., 2012). hot. It was still cooling down after the magma ocean The Early Archaean rocks record an Earth characterised episode that followed the Moon-forming impact, as by thick, plateau-like accumulations of mafic and attested by a very specific type of lava, komatiites, formed ultramafic volcanics (Kamber, 2015; van Kranendonk, from very hot magmas that only occurred on the early 2015) (Fig. 2). Associated with the volcanic eruptions Earth (Arndt, 1994). While no Hadean crust has been was hydrothermal activity. In the preserved enclaves, preserved, there are some remnants of Early Archean crust. hydrothermal activity was pervasive and strongly Most are highly metamorphosed but two enclaves of well- influenced the seawater at the interface between hot preserved volcanics and sedimentary deposits, dating from rocks and the sedimentary deposits upon them. Attempts 3.5-3.3 Ga ago, occur in the Barberton Greenstone Belt in to interpret Early Archaean seawater temperatures using South Africa and the Pilbara Craton in Australia. These silicon and oxygen isotopes have produced a wide variety rocks have suffered burial metamorphism ranging from of results ranging from 70-80°C (Knauth & Lowe, 2003), upper prehnite-pumpellyite to lower greenschist facies. through about 50-55°C (van den Boorn et al., 2007) to However, we will see that, apart from a maturation of the a cool 35°C (Blake et al., 2010). What can be stated is carbon associated with microfossils, the metamorphism that, given the widespread distribution of hydrothermal has not affected the biosignatures. The volcanic and associated sedimentary rocks document an anaerobic Earth (Westall, 2012). Some suggestion has been made for local oxygenic conditions (Ohmoto et al., 2014) but there were numerous abiotic processes that could have resulted in the production of small amounts of oxygen: photolysis of water vapour in the atmosphere, radiolysis of water at the surface of the ocean (without significant oxygen in the atmosphere and a protective layer of ozone, UV radiation reached the surface of the Earth uninhibited [Lammer et al., 2008]), as well as dissociation of water by boiling of hydrothermal fluids as they reach the surface (in shallow water and subaerial environments). Today’s 21% O2 in the atmosphere is a consequence of interrelated biogenic and geological factors, the biological input owing to the evolution of oxygenic phototrophs. Had such organisms developed by the Early Archaean, with their vastly more efficient metabolisms they would have rapidly overrun the Earth. However, there is no indication that this happened (Westall, 2011). Anaerobic conditions are mandatory for the emergence of life. No prebiotic reactions can take place in the presence of oxygen because of the immediate oxidation Fig. 2 - Figurative sketch of Early Archaean oceanic plateaux. (TTG: of the reduced carbon species. This means that the first Tonalite-Trondhjemite-Granodiorite series). After van Kranendonk cellular life was anaerobic and, indeed, life continued to be (2015). 88 Bollettino della Società Paleontologica Italiana, 55 (2), 2016

Fig. 3 - Artist’s depiction of the early Earth. Note impact craters, hydrothermal activity and the closer moon. From http://www.cosmographica.com/. activity and fluids, temperatures at the rock/sediment/ produces alkaline solutions (Kempe & Degens, 1985). On water interface must have been warm to hot. This the other hand, an Earth characterised by a mainly CO2 means that any life living in these habitats was probably atmosphere (Walker, 1985; Zahnle et al., 2010) would thermophilic. If the water column were cooler, especially have acid rainfall and slightly acidic oceans. In addition, in deeper water areas, early planktonic life forms could hydrothermal fluids may be acidic, especially if they are have been mesophilic. high temperature, or alkaline if they are lower temperature. There is much debate about the composition of the The rock/sediment/seawater interface and the adjacent early oceans since compositional signatures of seawater layers of water would have represented the mixing zone are difficult to preserve. Studies of fluid inclusions in of fluids of different origins, compositions and pH, thus the Early Archaean rocks suggest that the seawater was presenting a variety of habitats suitable for alkaliphilic to perhaps twice as salty as it is today (de Ronde & Ebbersen, acidophilic microorganisms. 1996). One major difference in the ion content of the early In conclusion, environmental conditions in the Early oceans compared to today would have been the lack of Archaean pose constraints on the type of life forms and significant amounts of sulphate (SO4) owing to the anoxic their mode of life during that period. In the first place, all conditions (e.g., Habicht et al., 2002; Lyons et al., 2014). life was anaerobic. One could envisage the possibility of Today’s oceans are sulphate-rich. Nevertheless, the small the development of tolerance of small amounts of oxygen amounts of abiotic oxygen would have meant that some through mutation for organisms living in environments sulphate would have been available as a nutrient for where oxygen was produced by abiotic means, such as in microbes, such as sulphate- or sulphur-reducing bacteria. the photic zone or close to shallow hydrothermal springs. Moreover, given the prevalence of mafic and ultramafic If the oceans were more salty than today, they were also lithologies being leached by hot hydrothermal fluids, iron probably halophiles. Microorganisms living on or close and magnesium contents would probably have been higher to the sediment/rock/water interface were likely to have than today. The significant hydrothermal influence, at been thermophilic and, in terms of pH tolerance, ranged least in the layers of seawater close to the sediment/rock from acidophiles to alkaliphiles. Those living in the photic interface, meant that that the seawater was saturated with zone must have been radiation resistant. respect to silica (e.g., Hofmann, 2011). This compositional From all points of view, the early Earth was an extreme information is important because it has a bearing on the environment - and its inhabitants were extremophiles solutes available to microbes and, especially, on the (Fig. 3). Note that these extreme conditions were normal preservation of the biosignatures and the associated rocks. on habitable planets in the early history of the Solar There is also much debate about the pH of the early System and will be far more common on habitable oceans. A priori alteration of mafic and ultramafic rocks planets elsewhere in the Galaxy and Universe than the F. Westall - Early life 89 present day oxygenic environment of the Earth. In fact, the Earth today is rather unusual and should be therefore considered extreme, and the oxygenic life forms on it are the extremophiles.

THE NATURE OF EARLY LIFE AND ITS PRESERVATION

For long the subject of heated debate owing to the challenges involved in studying fossil microbes in extremely old rocks, it is now generally recognised that life was present by 3.5 Ga. Huge advances have been made over the last few decades in our understanding of the preservation potential of microbial life and the methods needed to study and identify its fossil traces in rocks. It is now generally recognised that context is as important as other biosignatures, such as morphological remains or organo-geochemical signatures. This was spectacularly underlined in the famous debate about the biogenicity of certain microstructures occurring in a black chert from the Apex Chert locality in the Pilbara, Australia. Being carbonaceous and having some morphological similarity with filamentous microfossils found elsewhere in the rock record (a typical example are the cyanophytes of the Early Devonian Rhynie Chert in Scotland; Preston & Genge, 2010), they were interpreted as the fossil traces of microbes, including cyanophytes (Schopf, 1993, 2006; Schopf et al., 2002) (Fig. 4a). However these features were found in a hydrothermal chert vein, a fact that had not previously been recognised (Brasier et al., 2002). While phototrophs are known from hydrothermal spring environments, they do not occur within the hydrothermal conduits themselves. This example demonstrates the importance of direct context information and also the uncertainty of relying on only one kind of biosignature - morphology. Primitive microbial cellular morphologies are notoriously simple and many can be confused with abiotic features of similar shape and size (Westall & Cavalazzi, 2009). Another famous example may illustrate this point. A paradigm- changing discovery was made in 1996 when a group headed by David McKay at the Johnson Space Center in Houston announced that they had found fossil microbes in cracks in a meteorite from Mars (McKay et al., 1996) (Fig. 4b). The group had made very careful context, morphological and geochemical studies, concluding that microbes had been able to infiltrate water-filled fractures in what was basically a coarse-grained igneous lava or intrusion. One of their lines of evidence was the finding of small globular or elongated features up to a few hundreds of nanometres in size that were likened to “nanobacteria”. Fig. 4 - Abiotic bacteriomorph structures. a) Carbonaceous structure Nanobacteria, supposedly very small microorganisms, in the Apex Chert, Pilbara craton, Australia, interpreted as a fossil and their possible fossil signatures were much in vogue at cyanophyte (Schopf, 1993). b-c) Interpreted “nanobacteria” (black that point in time (e.g., Folk & Linch, 1997). It was later arrows) in the Martian meteorite ALH84001 (McKay et al., 1996). determined that the “microfossils” in the meteorite were simply mineralogical artefacts produced during corrosion of carbonate deposits within the cracks (Gibson et al., life on the early Earth and its implications for origins of 2001). We will come back to the interesting subject of life studies. In this respect I will first address the traces traces of life on Mars below. of phototrophic microorganisms for the reason that It is not the aim of this contribution to provide an some of them reach macroscopic dimensions and their exhaustive review of the traces of early life. I will morphological remains are more readily observable and highlight a few key studies to illustrate the diversity of identification less contentious (but not always, as we have 90 Bollettino della Società Paleontologica Italiana, 55 (2), 2016 seen from the Apex Chert example cited above). I will then present some case studies of chemotrophic remains, microscopic, less readily identifiable and subject to more debate. However, chemotrophic microorganisms, with their more primitive metabolisms, appeared before the more sophisticated phototrophs and are the most likely elsewhere in the Solar System and in the Universe. It is these signatures that will be the object of search on Mars (Westall et al., 2015a).

Benthic phototrophic biosignatures Phototrophic biosignatures are perhaps among the most readily observable and interpretable of microbial traces. There are a number of reasons for this. In the first place, the later appearing, more sophisticated phototrophs have an extremely efficient metabolism compared to chemotrophs and, when in a suitable photic environment, Fig. 5 - Domed stromatolite (15 cm in length) from the 3.48 Ga-old are able to produce high biomass (des Marais, 2000). This Dresser Formation, Pilbara craton, Australia. Note the plastically deformed internal laminae (white arrow) within the structure. ability was all the more important on the early Earth since there was no competition from other, more evolved life forms and no limitation due to grazing organisms, as is the case since at least the latest Proterozoic. Biofilms and evidence for the presence of phototrophs in hydrothermal mats formed by photosynthesisers can be thus relatively environments elsewhere at this period, as we will see large (for example, modern phototrophic mats in the Baja below (cf. Westall et al., 2015b). California - e.g., Frank & Stolz, 2009 - cover huge areas Also in the North Pole Dome region of the Pilbara, the up to hundreds of km2). Moreover, their sticky polymeric Strelley Pool Chert contains stromatolites that developed surfaces trap, bind and stabilise sediment surfaces, on a carbonate platform in a restricted, hypersaline basin creating distinctive structures that are recognizable area with little clastic or (supposedly) hydrothermal in the rock record back to 3.2 Ga, if not even 3.5 Ga input (Allwood et al., 2006, 2007; van Kranendonk, (Krumbein, 1983; Hofmann et al., 1999; Allwood et al., 2006). Morphological variations in the domical to conical 2006; Heubeck, 2009; Noffke, 2009; Noffke et al., 2013). stromatolites (up to about 10 cm in height) (Fig. 6) were Early Archaean phototrophs produced macroscopically interpreted to be biological responses to environmental recognisable features in the form of tabular and domical factors, such as water depth, sediment influx and - to conical stromatolites (now silicified), as well as hydrothermal activity (although Allwood et al., 2006, microbially induced sedimentary structures (MISS, cf. stipulate elsewhere that the stromatolites did not form in Noffke, 2009). They also produced microscopic biofilms a hydrothermal environment and that any hydrothermal and mats, whose spectacular degree of preservation was veins are later and cross-cut the strata). The environment, due to very early silicification. a tidal to supra-tidal rocky volcanic platform overlain by a chert boulder conglomerate and carbonate, underwent Case study 1: the North Pole Dome, Pilbara, marine transgression with time. Stromatolites formed in Australia (3.5-3.4 Ga) - A wide variety of macroscopic, relatively high-energy conditions on the rocky shoreline stromatolite-like structures is preserved in the North Pole of the lower member are domical in shape and encrust the region of the Pilbara Craton. Investigators have been a underlying breccia/conglomeritic fragments. With slightly pains to distinguish between those formed in association increasing water depths (from supra-tidal to intertidal), with hydrothermal fluids and those without this association in the belief that stromatolite-like features in the former category could not be phototrophic (Allwood et al., 2006; van Kranendonk, 2006). For instance, van Kranendonk (2006) described tabular to domical structures (up to some tens of cm in height) in the 3.49 Ga Dresser Formation where hydrothermal activity led to barite and chert precipitation, concluding therefore that the wrinkly laminites could not have been formed by phototrophic microorganisms. However, this supposition does not make sense because phototrophic mats and biofilms are common around hot springs today. Moreover, a domical structure of the order of 15 cm in diameter exhibiting plastically deformed laminae was observed in the direct vicinity of a shallow water hydrothermal vent (Westall, 2005) (Fig. 5). The deformation indicates that the dome consisted of laminae that were coherent at the same time Fig. 6 - “Egg-carton” shaped stromatolites in plan view from the as being soft and flexible, very similar to those formed by 3.4 Ga-old Strelley Pool Chert, Pilbara craton, Australia. Hammer microbial phototrophic biofilms. Moreover, there is much for scale. F. Westall - Early life 91

Fig. 7 - Microbially induced sedimentary structures (MISS) from the 3.48 Ga-old Dresser Formation, Pilbara craton, Australia. After Noffke et al. (2013). Insets a, b, and c show three different types of interpreted microbial mat structures observed in the Pilbara rocks: a) a fragament of mat on a bedding surface; b) a rolled up fragment of mat; c) a torn fragament of mat. The first column is an interpretive drawing of the “mat fragment” photograpahed in the central column. On the right are similar microbial mat features photographed in recent phototrophic mats. these were followed by small crested/conical, wavy and from the Moodies Group in the Barberton Greenstone Belt, “egg carton” laminites, as well as various large complex South Africa (Heubeck, 2009; Noffke, 2010). cones. Continued transgression of the carbonate platform was characterised by wavy laminites. Case study 2: the Barberton Greenstone Belt, More enigmatic, potentially phototrophic features South Africa (3.5-3.2 Ga) - The physical expression have been described as MISS from the 3.49 Ga Dresser of stromatolites in the early Archaean formations Formation in environments characteristic of an ancient (Onverwacht Group) of the Barberton Greenstone Belt, coastal sabkha (Noffke et al., 2013) (Fig. 7). First identified although silicified like those in the Pilbara, is different. in recent sediments (Noffke & Krumbein, 1999), MISS Macroscopic expressions of stromatolites are rare and comprise a series of fabrics and textures resulting from the consist of low amplitude laminae (from mm to cm in interaction of sticky phototrophic microbial biofilms and height) formed on top of basaltic lavas in the 3.3-3.2 Ga mats with the underlying sandy sediment surfaces. The Fig Tree Formation (Byerly et al., 1986) (Fig. 8). The laminae are composed of primary carbonaceous matter laminae are not carbonaceous and were interpreted as and exhibit a range of textures including macroscopic stromatolites on the basis of their wavy, non-conformable polygonal oscillation cracks and gas domes, erosional morphology. remnants and pockets, mat chips, and microscopic tufts, Other expressions of phototrophic biofilms and mats sinoidal structures, and laminae fabrics. Note that MISS are, however, abundant and well preserved in abundance were also identified in sandy lithologies in 3.2 Ga rocks in various strata of the Onverwacht Group. These include 92 Bollettino della Società Paleontologica Italiana, 55 (2), 2016

chemotrophic colonies that relied on the hydrothermal fluids for their nutrients (Westall et al., 2015a). The exceptional preservation of a robust, silicified and evaporite mineral-encrusted phototrophic biofilm in 3D on a sediment bedding surface (Westall et al., 2006a, 2011a) (Fig. 9a) has allowed a wide range of biosignature analyses to be undertaken, providing an unprecedented amount of structural and compositional detail of the kind that is usually only available when studying modern phototrophic mats, and this despite the great age of the rocks and evident maturity of the carbon (i.e., degraded kerogen consistent with the age of the rock matrix and lower greenschist metamorphism of the country rock). It is generally very unusual for individual organisms to be preserved within fossil stromatolitic laminae but the rapidly silicified, ~10µm thick biofilm was formed by Fig. 8 - Low amplitude domal stromatolite from the 3.2 Ga-old Fig Tree Formation, Barberton Greenstone Belt, South Africa. very thin, long filaments < 0.5µm in diameter and up to Photograph from A. Hofmann. tens of microns in length (Fig. 9b), much smaller than those forming phototrophic mats today. The biofilm was coated by a thick layer of EPS (Fig. 9b), a characteristic microscopically observable tabular laminae, perfectly typical of phototrophic films formed in environments preserved by rapid silicification and cementation. prone to desiccation and a protective mechanism against Microscopic remains of phototrophic biofilms in volcanic UV radiation and low water activity. Of interest as sediments in the Barberton greenstone Belt, were first additional biosignatures is the fact that this 10µm thick observed by Walsh (1992). Tice & Lowe (2004) and Tice biofilm had started to be calcified by microcrystalline (2009) made a detailed investigation of the effects of aragonite (5-10nm in size) before it was silicified (Fig. light intensity and/or small variations in ambient current 9c). This is the oldest evidence for in situ calcification energy on the morphology of phototrophic biofilms in in a phototrophic biofilm. As noted above, the carbon shallow-water deposits in the 3.42 Ga Buck Reef Chert at (kerogen) is highly mature, as is to be expected, and the base of the Kromberg Formation (Onverwacht Group, consists mainly of a relatively restricted range of aromatic Barberton). However, in the following I will concentrate molecules, including the sulphur containing molecule discussion on examples of phototrophic biofilms in the thiophene. Nevertheless it is still characterised by an 3.33 Ga-old Josefsdal Chert because their exceptional elemental signature (presence of C, N, and S), as well state of preservation has allowed in situ analysis of a wide as in situ carbon isotope values ~30‰, consistent with variety of associated organo-geochemical biosignatures. microbial fractionation. These are all organo-geochemical It is these kinds of analyses (and the more sophisticated signatures of carbonaceous matter that are characteristic methods that will be developed in the future) that will be of life (Summons et al., 2011; Westall & Cavalazzi, necessary for studying more enigmatic bacteriomorph 2011). Other examples of well-preserved, hydrothermally features in terrestrial rocks and, in the future, in rocks that silicified phototrophic biofilms occur in the Josefsdal will be brought back to Earth from other planets, such as Chert (Westall et al., 2015b) (Fig. 9d). Mars (Westall et al., 2011a, 2015a). The 3.33 Ga Josefsdal Chert, the lateral equivalent of Planktonic phototrophic biosignatures the Footbridge Chert in the Kromberg Formation (Lowe Apart from phototrophic benthic biofilms and mats, it is et al., 2012), consists of shallow water volcanic sediments possible that planktonic forms of phototrophs lived in the deposited in water depths ranging from upper offshore to Early Archaean water column. Rather large carbonaceous upper shore face (and partially exposed). Overprinted on structures with spindle shapes were first identified in the these changing environmental conditions were localised deposits of the Onverwacht Group by Walsh (1992). hydrothermal effusions that left a clearly recognisable Similar, enigmatic, spherical to lenticular features up geochemical signature in all the sedimentary components to > 50 µm in size were subsequently described from a and biosignatures, from alteration of the volcanic detrital number of Early to Mid Archaean strata from the Pilbara clasts and physical disturbance of the sediments, elemental by Sugitani and colleagues (Sugitani et al., 2007, 2009, impregnation (e.g., Fe, Ni, Cu, As) of the inorganic detritus 2015) (Fig. 10). Some of the spindle-like forms at times and organic remains, to control on the distribution of appear to contain spheroidal clumps of carbon and many

Fig. 9 - Silicified phototrophic microbial biofilm from the 3.33 Ga-old Josefsdal Chert, Barberton Greenstone Belt, South Africa (after Westall et al., 2011b). a) SEM view of the surface of an exquisitely preserved biofilm that was partially exposed and therefore exhibits desiccation cracks as well as evaporite mineral encrustation. Note the oriented filamentous texture, desiccation cracks and trapped volcanic clast in the middle. b) Note fine filament (< 1 µm in thickness) embedded in a thick coating of EPS. c-d) TEM micrographs of the calcified 10 µm thick biofilm. The STEM micrograph on the left of Fig. c shows a granular texture due to the precipitation of nanocrystallites of aragonite within the degraded kerogen matrix. Domains of thiophene molecules are dotted in the right HRTEM micrograph d. e) Optical micrograph of delicately preserved packet of phototrophic biofilms within pure hydrothermal silica. Note the pull-apart deformation caused by syngenetic infiltration of the hydrothermal fluids. Micrograph 8 mm long. F. Westall - Early life 93 94 Bollettino della Società Paleontologica Italiana, 55 (2), 2016

Fig. 10 - Large spherical and spindle-shaped carbonaceous structures from Mid Archaean cherts, Pilbara Craton, Western Australia. After Sugitani et al. (2010). Figures a-h show different shapes and sizes of the spindle features with corresponding details. appear to have complex wall structures. Interpreted as the Because of the importance of chemotrophy with remains of planktonic microorganisms, the complexity respect to extraterrestrial life, I will describe the of morphologies exhibited by these features suggests chemotrophic biosignatures in some detail. The 3.33 Ga that they may represent different life cycle stages, as Josefsdal Chert in the Barberton Greenstone Belt presents known from cyanobacteria, including reproductive cells, a fine example of chemotrophic colonisation in the vicinity vegetative cells or endospores. There is no known affinity of hydrothermal activity (Westall et al., 2015a, b) - and is with modern photautotrophs, however, and the affiliation also an example of the challenges involved in the study of these carbonaceous structures, if they indeed represent of such traces. Volcanic clasts in these shallow water the remains of microorganisms, remains enigmatic. sediments are invariably coated to some extent by a very Certainly the carbonaceous matter of which they are made thin layer of carbon, even in the oligotrophic settings has elemental and carbon isotope signatures indicative away from venting. Knowing the early oceans contained of biogenic carbon. Javaux et al. (2010) also noted the dissolved carbon (Lyons et al., 2014), as they do today, it presence of large, spherical (~100 µm) carbonaceous is likely that a thin “conditioning film” of organic carbon cell-like structures in deep water sediments of the 3.2 formed around the particles as they settled down through Ga Fig Tree Group in the Barberton Greenstone Belt. the water column. But detrital grains originating from Their affinities are also uncertain but they may represent mafic and ultramafic lithologies are ideal substrates for planktonic cells. lithoautotrophs, i.e. microbes obtaining their energy from oxidation/reduction reactions of elements occurring in Chemotrophic biosignatures the minerals exposed at the surfaces of the clasts (e.g., The signatures of chemotrophic microorganisms are Stevens & McKinley, 1995; Parkes et al., 2014). So how is particularly difficult to identify and study, mainly because it possible to distinguish between an abiotic conditioning of the small size and simple structures of the chemotrophs. layer and colonisation of a particle by micro-organisms? Although macroscopic chemotrophic mats have been Wacey et al. (2011) used detailed in situ sulphur isotope observed around hydrothermal vents in modern oceans analysis (δ34S and δ32S) of micron-sized pyrite crystals (e.g., Corliss et al., 1979; Sievert & Vetriani, 2012), these associated with carbonaceous matter coating a 3.4 Ga structures are formed by anaerobic sulphur reducing quartz sandstone from the Strelley Pool Chert in the bacteria (SRBs) that require vast amounts of sulphate Pilbara to demonstrate microbial reprocessing of organic (SO4). Sulphate in the anoxic early Archaean oceans carbon through both sulphate reduction and sulphur was a rare nutrient and its limited availability could not disproportionation. The association of a carbon coating on have supported significant SRB activity and huge mat the quartz crystals, however, is rather strange since quartz development as in the modern oceans. Nevertheless, as we offers no nutrition for lithoautotrophic microorganisms - will see below, hydrothermal fluids in the Early Archaean there are no elements that can be oxidised or reduced to oceans locally supported a sufficient chemotroph provide energy in quartz. development to the extent that mats up to the centimetre In the Josefsdal Chert example, apart from the fine scale could develop. carbon coating that is generalised around the volcanic F. Westall - Early life 95 clasts, clasts deposited in the vicinity of hydrothermal activity are characterised by thick, irregular coats of carbon, at times up to 25-30 µm thick (Westall et al., 2015a, b) (Fig. 11a). What is striking about these coats is their apparently spiky vertical formation. While abiotic conditioning coats form angstrom-thin, surface conformable layers around objects in seawater, microbial colonies develop in a haphazard manner on the surfaces of particles. In situ analysis of δ13C of heavily carbon- coated clasts documents average values of ~ -31‰ (new data), consistent with microbial fractionation, while bulk analyses of dark, carbon-rich layers have slightly heavier values of ~ -27.6‰ (Westall et al., 2011a), probably indicative of a mixed biogenic signatures, as well as admixed abiotic carbon of various origins (Westall et al., 2015b). Concentrations of the hydrothermal tracer elements, Fe, Ni, Cu, and As, directly measured on the carbon-coated clasts, as well as rare earth element indications of an Eu anomaly, confirm the field indications of deposition of these sediments close to hydrothermal vents and, thus the importance of hydrothermal activity for the development of significant biomass. Hydrothermal fluids are an important source of nutrients, such as H2, CH4, and other small carbon molecules (Shock et al., 1998), that are essential for chemotrophs (both lithoautotrophs as well as organotrophs). Given the thick, organic encrustation of the volcanic clasts, it can also be assumed that the initial lithoautotrophic colonisers were themselves subsequently colonized by organotrophs that oxidised the carbon produced by dead colonies of the former. Fig. 11 - Early Archaean volcanic clasts colonised by chemotrophic Further documentation of probable communities. a) Optical microscope view of a volcanic clast in chemolithoautotrophic colonisation of volcanic clasts cross section (now thoroughly silicified) showing an up to 30 µm comes from in situ observation of silicified, < 1 µm-sized, thick, irregular carbonaceous coating interpreted as the remains of carbonaceous coccoidal bacteriomorphs, occurring in chemotrophic organisms. This clast (300 µm long) comes from a 2 hydrothermally-influenced facies in the 3.33 Ga Josefsdal Chert, colony formations up to several hundreds of µm in size, Barberton (Westall et al., 2015b). b) Scanning electron microscope directly on the surfaces of altered volcanic clasts in the view of a monolayer of bimodal coccoidal structures (~0.8 and 3.45 Ga Kitty’s Gap Chert, Pilbara (Fig. 11b), a volcanic 0.5 µm diameter) at the edge of a volcanic clast (now replaced sediment deposited in a littoral environment similar to by muscovite and silica that can be seen in the background. After that of the Josefsdal Chert (Westall et al., 2006b, 2011b, Westall et al., 2011a). These features are interpreted as silicifed 2015b; Foucher et al., 2010). These colonies consist of two chemotrophs and the light veil coating them as EPS. size classes of coccoids, interpreted as representing two different species. The individual cell-like structures are coated with a thin film-like coating possibly representing careful re-evaluation by Westall et al. (2015a) found that an EPS. Detailed evaluation of such features in individual abiotic explanation for the totality of observations was not 1mm thick layers of sediment documented different tenable and that the Kitty’s Gap Chert coccoidal features stages of degradation before silicification, as well as were best explained by microbial formation. Nevertheless, the presence of sedimented fragments of phototrophic this kind of discussion is useful because it demonstrates the biofilms. Bulk, carbon isotopic analysis of the individual difficulties in interpreting simple microbial structures and layers showed values varying around -27.7 to -25.9‰ the care needed in their interpretation. Obviously, more (Westall et al., 2006b, 2011b). Apart from the direct detailed in situ geochemical studies, such as in situ carbon attachment of the coccoidal colonies on the surfaces of isotope analysis or study of the molecular and elementary individual volcanic clasts, observation of small corrosion composition of the features would greatly help. Given the tunnels filled with a film-like substance, similar to EPS, extremely small size of these interpreted microfossils, reinforces the interpretation of the coccoidal colonies these kinds of studies are technologically challenging. as chemolithotrophs who obtained their energy from However, such methods need to be developed in view of oxidation/reduction reactions on the surfaces of volcanic investigations on rocks containing potential traces of life particles (Foucher et al., 2010). from Mars since, if life appeared on the red planet, it is Coccoidal microbial morphologies are, however, more likely to have been primitive chemotroph-like life notoriously easily confused with abiotic spherical features forms than phototrophs (Westall et al., 2015b). (Westall & Cavalazzi, 2011), as we saw above with the Another study by Kiyokawa et al. (2006, 2012) example from the Martian meteorite (McKay et al., 1996; documented the presence of chemotrophic activity, Gibson et al., 2001). The in situ observations from the including methanogenesis, on the basis of bulk carbon Kitty’s Gap Chert have been challenged (Wacey, 2014) but isotope analysis in hydrothermal sediments deposited in an 96 Bollettino della Società Paleontologica Italiana, 55 (2), 2016 island arc setting in the 3.2-3.1 Ga Dixon Island Formation in Westall et al., 2015b). In a solution of silica (or any off the NW coast of Australia (in the Pilbara Craton). other dissolved species), the microbial structures serve The carbon-rich sediments exhibit a partially layered as templates for passive fixation of silica to functional and partially clotted fabric, very similar to those of the groups (carboxyls, phosphoryls, hydroxyls) in the organic hydrothermal carbonaceous cherts of the Josefsdal Chert, surfaces, whether microbial cells themselves or their although their environment of formation is interpreted to EPS, the more functional groups, the better the silica be deep water. Identification of environment of deposition encrustation (Westall, 1997). In an anaerobic environment, of these ancient cherts is often not evident because of the such as that on the early Earth, the organic matter high degree of silicification (the rocks consist sometimes comprising the silicified organism remains entrapped of > 99% silica), which makes observation of sedimentary within the structure, degrading to mature kerogen with structures difficult. However, from the published data, the geological time (and metamorphism). Apart from natural sedimentary structures appear to be similar to those of the degradation, the degree of preservation of the organic Josefsdal Chert and, therefore, the depth of deposition carbon within the early Archaean fossilised microbial may be shallow as the one there interpreted (Kiyokawa features is good enough to enable study its elemental, et al., 2006, 2012). molecular, and isotopic compositions in situ (Westall et al., 2011a, 2015a, b). Note that not all microbial forms inhabiting a particular PRESERVATION AND ANALYSIS environment are preserved. Experimentation shows that OF BIOSIGNATURES IN THE species that are very similar to each other may react very EARLY ARCHAEAN CHERTS differently to the silicification process. Orange et al. (2009) showed that of two hyperthermophilic methanogens, One of the remarkable aspects of biosignatures in the Pyrococcus abyssi and Methanocaldococcus janischii, Early Archaean cherts is often their exquisite degree of the former fossilised well with good cellular preservation preservation. This was due to the very rapid silicification whereas the cells of the latter lysed while their associated of the organisms, usually as they were living, because EPS fossilised very well. Cation bridging, for instance the early oceans were saturated in silica compared to with iron (Fe), facilitates attachment of silica to today’s oceans. The silica originated from dissolution and Methanocaldococcus janischii cells, thus aiding their alteration of the largely volcanic rocks and sediments, preservation (Orange et al., 2011). Given the commonality as well as high input into the oceans from hydrothermal of mafic and ultramafic lithologies on the early Earth, fluids. As noted above, hydrothermal activity on the Early and the anoxic conditions, Fe was common in seawater Archaean Earth was prevalent (Hofmann & Harris, 2008; and may have acted as the cation bridge of silicification. Westall et al., 2015b). There is some debate in the literature Other factors also influence the degree of preservation as to whether silicification of not only the microbial of microbial structures. Microbial colonies and biofilms features but also the sediments and tops of lava flows was are delicate features. Thus, biofilms formed on coarse- due simply to silica saturated seawater (e.g., Lowe, 1999; grained sediments are morphologically less well preserved Tice & Lowe, 2006; Ledevin et al., 2014) or to mainly than those formed on finer grained or hydrothermal hydrothermal input (Hofmann & Harris, 2008). The fact sediments (Westall et al., 2015a). After silicification of is that both situations existed and played a role in rapid the delicate microbial structures, it is also necessary for silicification. In the Josefsdal Chert, we see: the sediments to be rapidly cemented in order to protect the delicate features and this was the situation with the 1. facies of alternating black and white chert Early Archaean cherts. consisting of > 99% SiO2 in which the sedimentary In terms of preservation, silica is an ideal medium for structures are almost, although not entirely, invisible; a number of reasons. It has a very small crystalline matrix 2. facies where the chert (90-96% SiO2) consists of that can reproduce fine-scale detail. This can be seen in visibly layered sedimentary structures; and the replication of the nanometre-scale reticulate structure 3. facies of purely hydrothermal silica, all facies of the kerogen making up the 3D-preserved microbial containing microbial features (Westall et al., 2015a). biofilm in the Josefsdal Chert in which even nanometre- sized crystallites of aragonite are preserved (Westall et In all likelihood, there was a delicate interplay between al., 2006a, 2011a). Silica is also particularly impervious the degree of hydrothermal influence on the seawater and and resistant and is less subject to dissolution than other pore water compositions of these shallow water interface minerals, such as carbonate. Indeed, the silicified Early sediments, albeit with a preponderance of hydrothermal Archaean sediments form resistant ridges. For these input. reasons, the microbial biosignatures of the Early Archaean Experimental fossilisation of microbes using silica cherts are particularly well-preserved. can inform us about how microbial silicification occurs However, the heavy silicification of the Early Archaean (e.g., Westall, 1997; Toporski et al., 2002; Orange et sediments also causes analytical problems. The rocks al., 2009, 2011). In order to be fossilised, encapsulation are very hard; fresh fracture surfaces consist of quartz and impregnation by the mineralising solutions needs to crystals and it is rare to observe fossil features on a be fast (Fig. 12). Microbes and microbial communities freshly prepared surface. While study of the carbonaceous generally have a relatively short life span of days to microbial biosignatures in thin section is essential for weeks. The individual microbial features described from context information, at the same time as providing other the Early Archaean cherts range from extremely well essential morphological and compositional information, preserved to, at times, partially degraded (see discussion much detailed information can also be obtained from F. Westall - Early life 97

Fig. 12 - Experimentally silicified, early Earth and early Mars analogue microorganism, Pyrococcus abyssi (after Orange et al., 2009). a) Unsilicified microorganism; b-c) SEM micrographs after 24 hours in silica; d) EDS spectrum showing presence of Si in the mineral precipitate; e-g) TEM micrographs showing delicate encapsulation of P. abyssii cells in a silica crust. scanning electron microscope study of the morphological they are not revealed. As noted above, the individual cells features revealed through delicate acid etching of the rock comprising colonies and biofilms are tiny, < 1µm in size, fracture surfaces or thin section surfaces. The procedure is, and thus not visible individually in this section. On the other however, arduous and often frustratingly unsuccessful - too hand, the colonies encrusting volcanic grains, where well- much etching and the biosignatures are lost, too little and developed, can be seen in this section, as are the biofilms. 98 Bollettino della Società Paleontologica Italiana, 55 (2), 2016

For more detailed analyses, such as the elemental, described above. Average in situ δ13C values within molecular or isotopic composition of the organic matter the biofilm range from -29.2 to -31.5‰, consistent from the microfossils, two approaches are commonly with microbial fractionation. However, although these used. Bulk analysis of organic carbon, i.e. its isotopic values were obtained in situ in a 10 µm thick biofilm, and molecular composition (e.g., Derenne et al., 2008; nevertheless, they are likely to represent a mixed Tice, 2009), obtained from dissolution of the fossil- signature. Phototrophic biofilms and mats are complex containing rock, can provide very accurate measurements. communities in which phototrophs and heterotrophs co- However, what is eventually measured is a mixture of exist, the latter degrading the primary biomass produced preserved organic carbon from all the carbonaceous by the former, as documented by evidence of the activity remains in the rock, whether microbial or abiotic. Study of sulphate reducing bacteria (heterotrophs) found in this of modern microbial communities using either traditional 3D biofilm in the form of carbonate precipitation and observational methods or the more sophisticated gene enhanced sulphur concentrations (up to 1%) (Westall et analysis techniques available document a huge array al., 2011b). of species within one micro-ecosystem. Thus, the bulk analyses are just that, a general analysis that rarely reflects the variable species composition of a microbial community. PERSPECTIVES: MICROBIAL PALAEONTOLOGY Given the small sizes and low biomass of the anaerobic AND THE APPEARANCE OF LIFE ELSEWHERE microbial colonies in the Early Archaean cherts, and IN THE SOLAR SYSTEM hence the low carbon concentrations associated with individual features, in situ analysis of individual features It was noted above that extreme environmental is challenging. The 3D-preserved biofilm in the Josefsdal conditions characterised the early Earth and were the scene Chert is just such a case where the structure was sufficiently for the emergence of life on Earth. These conditions were large and the carbon content sufficiently high as to allow very likely similar to those of early Venus, probably also detailed in situ investigations (Westall et al., 2006a, 2011a, an ocean planet before the CO2 atmosphere and proximity 2015a). Here it was possible to take ultrathin sections to the Sun induced a “runaway greenhouse effect” that (90 nm to 3 µm) through the ~10µm thick biofilm for made the surface of the planet inhospitable (Kasting, high-resolution transmission and scanning and electron 1988), and before the global volcanic resurfacing event microscope observation and elemental analysis. Detailed that occurred about 500 million years ago (Strom et al., elemental analyses were made using NanoSIMS for the 1994). distribution of the bioessential elements, C, N, and S, Mars in its early history was also habitable - but in synchrotron µ-XRF analysis and PIXE (proton-induced a slightly different manner. While the Earth has always X-ray spectroscopy) for the trace-element composition, been an ocean planet, Mars was always a land-locked and synchrotron NEXAFS (S at the k-edge) and ToF- planet with aqueous basins of various sizes distributed in SIMs (Time-of Flight secondary ion spectroscopy) for different locations and at different times, a situation that molecular studies. The necessity for sophisticated, high- is termed “punctuated habitability” (Westall et al., 2015a) resolution techniques is due to the very high degree of (Fig. 13). This scenario has a number of consequences silicification - while preserving the biosignatures perfectly for potential life. In the first place, Mars had the same in the original state in which they were silicified, i.e. either ingredients of life as the early Earth, i.e. the combination while living or already partially degraded - which also of liquid water and carbon molecules in contact with hot considerably dilutes any organo-geochemical signatures. rock in an anaerobic environment. Of critical importance Thus, elemental concentrations that were originally at the for the emergence of life is the length of time that these trace level, are now even lower, hence necessitating high ingredients could coexist. As noted above, it is not known energy techniques to detect them. how long it took for the first cells to appear on Earth, In light of the above discussion regarding bulk carbon hundreds of thousands of years or a couple of million isotope measurements, it is interesting to evaluate in situ years? For life to have emerged on Mars, the impact crater measurements made on the 3D phototrophic biofilm lakes or northern ocean (if it existed) needed to have been

Fig. 13 - Changes in the habitability of Mars with time (after Westall et al., 2015a): Stage 1: before the planet became habitable. Stage 2: beginnings of habitability during the preNoachian-Noachian (4.4-4.2 Ga) with life emerging (red star) in two different locations. Stage 3: Late Noachian (~3.8 Ga) with life emerging in yet another location while a potentially habitable lake remains uninhabited because viable cells cannot reach it; life has reached the subsurface aquifer (black dots) through fractures in the crust. Stage 4: Hesperion/Amazonian (< 3.6 Ga), the surface of Mars is uninhabitable due to degraded environmental conditions but there are still viable cells (red dots) in subsurface aquifers. Stage 5: Hesperion/Amazonian (< 3.6 Ga), a particularly large impact causes crustal fractures to reach an aquifer containing viable cells (red dots), which can briefly colonise a surficial crater lake. F. Westall - Early life 99

Fig. 14 - Water plumes rising up from fractures in the icy crust of Saturn’s moon Enceladus (credit NASA). large enough to have sustained liquid water in contact with having infiltrated fractures in the crust could have been hot rock, i.e. hydrothermal systems in continuation and for explosively transported in crustal fragments into another up to perhaps a couple of million years. At a minimum, habitable environment through impact transfer, especially the craters needed to have dimensions of at least 100 km during the pre-Noachian and Noachian when large impacts and probably more. During the habitable Pre-Noachian were more frequent. and Noachian periods of Mars (4.5 to ~3.8 Ga), there may The implication of this punctuated habitability is that have been many craters with these conditions and life Mars never had the kind of continuous habitability that could have appeared in more than one place and at more the Earth had and, thus, the possibilities for Martian life to than one time. Once cellular life appeared and flourished, evolve were limited. It is therefore unlikely that Martian it could have survived as the habitable conditions of life could have evolved much beyond the chemotrophic an individual crater slowly disappeared. Friedmann & life style before habitable conditions at the surface of the Koriem (1989) first suggested the possibility that Martian planet degraded to the extent that the surface of the planet life forms could have survived in endolithic habitats, as was no longer habitable (~3.8-3.6 Ga). As seen above, in desert environments on Earth, such as the Dry Valleys the study of primitive chemotrophic biosignatures is of Antarctica. Knowing that life can exist in the most particularly arduous and, even on Earth where extremely extreme environments on Earth today - and that early sophisticated technology is available, still subject to life emerged in an extreme environment - it is likely that controversy. On the other hand, the crust of Mars has not early Martian life forms managed to colonise all possible been destroyed by tectonic forces and, if life emerged habitable niches, from lake bed floors and fissures and on the red planet, it is possible that the precious trace of fractures beneath them, to emerged, protected cracks in the passage from inert substances to living cells is still rocks and evaporite deposits in littoral environments. preserved, somewhere, on its surface. While specific conditions are needed for life to emerge, There are further implications with respect to the once established, flourishing life can rapidly colonise search for traces of life on Mars. The present NASA even ephemerally habitable environments - if viable cells mission, Mars Science Laboratory, and the future can reach the environment. This is an important point. missions ExoMars 2020 of Europe/Russia and Mars On a water covered world, viable cells can always be 2020 of NASA, all aim at searching for biosignatures - transported from one habitat to another by ocean currents. of course, taking into account the all-important context This is not the case on a land-locked world. As noted by information. However, the instrumentation developed Cockell et al. (2012), this means that certain locations for space missions, while highly miniaturized and as on Mars could theoretically have been habitable but not efficient as possible, is limited. No electronic microscopes, inhabited because no viable organism could reach the NanoSIMS or synchrotrons can be sent to Mars. It is location. Various means of cell transport can be envisaged, not even possible to study the rocks in thin section in such as through aquifers in the subsurface. Wind-blown transmitted light, a simple method of observation that transport is not an option because of damage from is the basis of all microbial palaeontology observations. ionising radiation (Norman et al., 2014). Microorganisms Primitive, anaerobic chemotrophic life forms do not leave 100 Bollettino della Società Paleontologica Italiana, 55 (2), 2016 macroscopic signatures, such as MISS or stromatolites. of course astrobiology (which is almost everything). I have been They will therefore be difficult to observe in situ with favoured by inspiration and support from many people. Claude space instrumentation. The ExoMars rover has Raman, Monty first introduced me to geobiology, and while in Italy I was infrared (IR) spectrometers, and laser desorption-gas lucky to have the support of Elisabetta Guerzoni, Laurita Boni, Paola Giordani, Roberto Barbieri, and Gian Gabriele Ori. At the chromatography-mass spectrometry (GC-MS) that should Johnson Space Center, David Mckay and Everett Gibson accepted be able to detect the presence of organic molecules, my “devil’s advocate” stance on the traces of life in the meteorite although the experience with the SAM (Sample Analysis ALH84001. I also enjoyed fierce battles with Robert Folk over the at Mars) spectrometer on Curiosity has shown just how existence or not of “nanobacteria” (the battle is still ongoing, both of difficult this can be (Freissinet et al., 2015). The Mars us being very stubborn). I am happy to acknowledge my colleagues 2020 rover will also have a Raman spectrometer and “in (astrobiological) crime” Barbara Cavalazzi and Annalisa Ferretti. will also be able to take samples with the aim of caching André Brack took a momentous step in asking me to take over his them for future sample return to Earth. It is evident that prebiotic and origins of life group at the CNRS in Orléans, thus in situ identification of biosignatures on Mars with space opening up my horizons challengingly. The possibility of working with the ExoMars mission is allowing me to dream of other instrumentation will be very difficult and so sample worlds and other life, aided and abetted by many close friends and return is a must. The biosignatures in the Early Archaean colleagues, especially Jorge Vago the project scientist of ExoMars, rocks and the techniques used to study them provide my research group in Orléans (Frédéric Foucher, Frédéric Gaboyer, us with a good idea as to what might be found in the Avinash Dass, Keyron Hickman-Lewis, Axelle Hubert, Marylène returned Martian rocks and how to identify any potential Bertrand, Annie Chabin), and CNRS friends and colleagues Philippe biosignatures. Martin and Pascale Gautret. Finally, where would we be without the Mars could still possibly host extant life in the support of the French Space Agency (CNES) and our astrobiological subsurface, but deep drilling to search for extant life thematic leader, Michel Viso. And many, many others have had a forms is not possible in the immediate future. However, lasting input into my research. other satellites in the Solar System could host extant life in oceans beneath their icy crusts, such as Enceladus (e.g., REFERENCES McKay et al., 2014) around Saturn and Europa (e.g., Hand & Carlson, 2015) around Jupiter (Fig. 14). Indeed, there Allwood A.C., Walter M.R., Burch I.W. & Kamberc Balz S. (2007). are a number of missions planned to explore the surface 3.43 billion-year-old stromatolite reef from the Pilbara Craton of Europa in the next decade. All that could be observed of Western Australia: Ecosystem-scale insights to early life on is the icy surface upon which possible salty deposits from Earth. 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C., Foucher F., Toporski J., Jauss A., Thiel V., Southam G., Westall F., Foucher F., Cavalazzi B., de Vries S.T., Nijman W., MacLean L., Wirick S., Hofmann A., Meibom A., Robert F. Pearson V., Watson J., Verchovsky A., Wright I., Rouzaud J.N., & Défarge C. (2011b). Implications of in situ calcification for Marchesini D. & Anne S. (2011a). Early life on Earth and Mars: photosynthesis in a 3.3 Ga-old microbial biofilm from the a case study from 3.5 Ga-old rocks from the Pilbara, Australia. Barberton Greenstone Belt, South Africa. Earth and Planetary Planetary Space Science, 59: 1093-1106. Science Letters, 310:∼ 468-479. Zahnle K., Schaefer∼ L. & Fegley B. (2010). Earth’s earliest Westall F., de Ronde C.E.J., Southam G., Grassineau N., Colas M., atmospheres. In Deamer D. & Szostak J.W. (eds): Additional Cockell C.S. & Lammer H. (2006a). Implications of a 3.472– Perspectives on The Origins of Life. Cold Spring Harb Perspect 3.333 Gyr-old subaerial microbial mat from the Barberton Biol 2010;2:a004895. Greenstone Belt, South Africa for the UV environmental Zahnle K.J. & Catling D.C. (2016). Waiting for oxygen. Geological conditions on the early Earth. Philosophical Transactions of Society of America Special Paper, 504: 37-48. the Royal Society B, 361: 1857-1875. Westall F., de Vries S.T., Nijman W., Rouchon V., Orberger B., Pearson V., Watson J., Verchovsky A., Wright I., Rouzaud J.- N., Marchesini D. & Anne S. (2006b). The 3.466 Ga Kitty’s Gap Chert, an Early Archean microbial ecosystem. Geological Society of America Special Paper, 405: 105-131. Westall F., Foucher F., Bost N., Bertrand M., Loizeau D., Vago J.L., Kminek G., Gaboyer F., Campbell K.A., Bréhéret J.-G., Manuscript received 15 July 2016 Gautret P. & Cockell C.S. (2015a). Biosignatures on Mars: Revised manuscript accepted 28 August 2016 What, Where, and How? Implications for the Search for Martian Published online 30 September 2016 Life. Astrobiology, 15: 998-1029. Editor Barbara Cavalazzi

Frances Westall is a geologist now working in the very broad discipline of astrobiology, the study of the origins of life and its destiny in the Universe. After a PhD in marine geology at the University of Cape Town in South Africa, she worked in various research institutes around the world: the Alfred Wegener Institute for Polar and Marine Research in Bremehaven in Germany, the University of Nantes in France, the University of Bologna in Italy, the Johnson Space Center and Lunar and Planetary Institute in Houston, USA and, for the last 15 years, she is Director of Research at the CNRS-Orléans in France where she heads the astrobiology group. Her research interests and activities cover study of the earliest traces of life on Earth and the geological environment in which they lived, the artifical fossilisation of bacteria, the search for life on Mars, especially with the ESA/Russian ExoMars 2020 mission, and prebiotic chemistry and the origin of life.