Roberto Barbieri And Barbara Cavalazzi

Dipartimento di Scienze della Terra e Geologico-Ambientali, Université di Bologna, Via Zamboni 67, I-40126 Bologna, Italy

Abstract The recent detection of methane in the martian atmosphere has stimulated a debate on its source, including speculations on a possible biological origin as in the Earth's atmosphere, where methane is present as a trace gas and is mostly produced by life. Large amounts of methane seepage flows from the subsurface are documented on Earth since the lower Paleozoic by the formation of authigenic carbonate deposits. Methane-derived carbonates also precipitate in the modern continental slopes throughout the world with a great variety in size and shape, and document a still active methane advection from deep sources. The interest of seep carbonates in an astrobiological perspective relies on their relationship with microbiological communities that inhabit the methane seep ecosystems and establish the base of their food chain. They also might represent terrestrial analogues for martian environments and possible models for microbial life on other planets.

1. Introduction

Exciting new discoveries in terrestrial extreme environments are widening the physicochemical limits of life on Earth, and therefore enabling an understanding of the potential spectra of conditions in which life can be present. The expanding limits of the environments of life on the edge may also help to answer the key question of how to recognize life, if life were ever to be met somewhere outside of our planet. A recent remarkable finding that documents the ability of life to survive in seemingly hostile conditions, involving both complex animal biota and microorganisms, is given by the dense beds of living clams and bacterial mats found in 2005 in a deep-sea site off the Antarctic Peninsula (Domack et al., 2005a). In this site, which is permanently covered by more than 10,000 years old superficial ice shelves (Domack et al., 2005b), a chemosynthetic-interpreted ecosystem sustained by low temperature fluid flow (cold seepage) is the first ever recorded from the Antarctic.

Methane seeps, as well as hydrothermal vents, are of great interest as extreme environments because the macroinvertebrates living there have developed efficient mutualistic partnerships with specific microbial consortia adapting to a range of conditions in which biochemical processes are largely driven by archaea and bacteria (Levin, 2005). Metazoa-microbe mutualisms would, therefore, be a successful strategy for further development along with new possibilities for life under extreme physical and chemical stresses (Hickman, 2003). On Earth, chemo-synthetic generated (non-hydrothermal) geologic bodies have been known at least since the Silurian Period (Barbieri et al., 2004) and can preserve significant parts of ecosystems that are generated by hydrogen sulfide and hydrocarbons, especially methane. The enormous amounts of methane delivered to the atmosphere every year largely have geological sources (Kvenvolden and Rogers, 2005), including seeps, volcanic activity, and gas hydrates. It is believed that some periodic destabilization of natural gas hydrates throughout geological time, with episodic CH4 release, may have influenced the Earth's climate (Kennett et al., 2003) and the distribution of seep ecosystems (Van Dover et al., 2006). At least some of this methane should have been originated from the activity of methanogenic archaea (methanogenesis), which have a high adaptability at extreme environments, including the conditions present on early Earth. Inorganically produced methane, such as that which is formed through serpentinization reactions related to hydrothermal processes, was recently found to sustain unique ecosystems. In the Lost City hydrothermal field (Kelley et al., 2001), near the Mid-Atlantic Ridge, for example, elevated (relative to seawater) methane concentrations support methane-consuming and methane-producing archaean populations (Kelley et al., 2005).

The record of methane, one of the major gas components at cold seeps, in the atmospheres of solar system bodies, including Europa, Titan, and especially Mars (Formisano et al., 2004; Krasnopolsky et al., 2004; Mumma et al., 2005), has revived interest in this biogenic tracer. Methane abounds in the solar system, however, its detection from small and localized spots, such as those recently reported from Mars and Titan, agrees with the presence of consortia of methanogenic bacteria similar to the ones described on Earth in cold seep ecosystems and based on methane for their biogeochemical processes. New insights into methane-dominated environments may help us to understand primordial life on Earth, and by analogy, in other parts of the solar system.

The likelihood that life, if present on Mars, is microbial, along with the expression of earlier wet periods that might have left some fossil records, have enhanced astrobiological interest in cold seep ecosystems, thanks to the fossiliza-tion potential of their microbe-mineral interactions. The focus of the present paper is to discuss these astrobiological perspectives and their controversies in light of the latest data from the ongoing European Space Agency (ESA) and National Aeronautics and Space Administration (NASA) missions to Mars, Titan, and Europa.

2. Modern and Fossil Methane Seep Ecosystems

The ecosystems sustained by methane-rich fluids (see the recent review by Levin, 2005) have diverse biota that produce enormous biomasses (Sibuet and Olu, 1998; Olu-Le Roy et al., 2004) and have been recognized from relatively shallow marine, down to hadal environments (Fujikura et al., 1999). Macroinvertebrate chemosymbiotic groups at cold (methane) seeps include mussels, clams, vestimentifera, gastropods, polichaetes, and nematodes as distinctive faunal components, which are partially shared with hydrothermal vent communities at different taxonomic levels (Van Dover et al., 2006). Some of these communities have a symbiotic relationship with methane-consuming and sulfide-oxidizing bacteria, whereas other parts obtain their nutrition from the direct utilization of the microbial biomass. The food web is, therefore, based on these chemoautotrophic primary producers. Methanotrophs belonging to specific archaeal clusters (ANME-1, ANME-2, and ANME-3) and the sulfate-reducing bacteria Desulfovibrio and Desulfococcus-Desulfosarcina clusters have been extracted from different anoxic environments associated with gas hydrates (Hinrichs et al., 1999; Meyerdierks et al., 2005; Treude et al., 2005; Zhang et al., 2005). Moreover, large communities of sulfide-oxidizing, filamentous bacteria - including Beggiatoa, which is amongst the largest of the prokaryotes (Jannasch et al., 1989), Thioploca, Thiothrix, and Arcobacter - typify the seep ecosystems, where they indicate areas of active gas seeping. Mats produced by the thiotrophic bacteria Beggiatoa, in particular, represent an interface separating oxic and anoxic environments at cold seeps. The authigenic carbonates, which make up most of the seep deposits (Ritger et al., 1987), only precipitate within anoxic environments (e.g., beneath the Beggiatoa mats), where the oversaturation of Ca2+ and CO32- ions is largely determined by bacterial-induced kinetic constraints. The hydrothermal-generated carbonate bodies of the Lost City hydrothermal field (Kelley et al., 2001) are similar to methane seeps in many respects. In particular, they host macro- and microorganisms, which consume or generate methane in their metabolic processes (Kelley et al., 2005).

In ancient methane seeps the shelled megafaunal component represents a readily discernible diagnostic feature and include chemosymbiotic bivalves belonging to lucinids, bathymodiolids, thyasirids, vesicomyids, and solemyids that develop dense, low-diversity fossil assemblages. Lucinidae, which engage in a well known symbiosis with chemoautotrophic bacteria (Schweimanns and Felbeck, 1985; Fisher, 1990), have a large fossil record for this strategy of life, which makes this group remarkable from a geological perspective. The oldest known lucinid with morphological features that are similar to recent members of this group is Ilionia prisca, a Silurian species for which a bacteria-symbiotic feeding strategy is hypothesized (Liljedahl, 1992). The worldwide abundance of hydrocarbon seeps in the geologic record (Campbell, 2006) represents a useful condition for studying chemosymbiotic relationships through time; however, this is limited by the substantial changes that occurred throughout the Phanerozoic to the macroinvertebrate component of the seep fauna, especially for bivalve and brachiopod groups (Little et al., 2002).

These changes, and the consequent reduced phylogenetic relationships between modern and ancient macroinvertebrates, make it rather difficult to have a pale-oecological analysis that is based on a uniformitarian approach (Campbell and Bottjer, 1995; Barbieri et al., 2004). Additionally, it is unclear as to whether the seeming resistance to the extinction of the seep macrofauna (Tunnicliffe, 1992; Kiel and Little, 2006) is a genuine feature or is rather dependent on the incompleteness of the fossil record. Unlike most of the modern and fossil seep ecosystems, some of them lack the typical (and diagnostic) macroinvertebrate assemblages. For example the Miocene-aged deposits of Santa Cruz, California (Aiello et al., 2001) consist of low magnesium calcite with associated foraminif-eral and diatom tests. The activity of methanotrophs (as anaerobic methane oxi-dizers) and sulfate-reducing bacteria seems to be, therefore, the common factor that is shared by modern and fossil cold seep environments. High alkalinity conditions promoted by the biogeochemical processes of these microbial communities lead to the formation of calcium carbonate deposits (Ritger et al., 1987), the geological expression of the cold seep environments, past and present. The precipitation of a variety of limestone thin crusts, just beneath the seafloor surface, up to several meters-high limestone bodies (chemoherms and chimneys) packed with seep megafaunas, depends on the intensity and persistence of the seepage (Teichert et al., 2005; Campbell, 2006).

3. Microbial Evidences at Methane Seep Ecosystems

The presence and role of microorganisms in seep habitats are documented by various types of microbial mats, in which sulfide-oxidizing bacteria grow at or just below the water-sediment interface, and host a variety of faunal groups (Robinson et al., 2004). Beggiatoa, for example, that develop dense and thick mats, can be visually recognized because they are white (colorless) or have yellow-orange pigmentation (Prince et al., 1988; Levin, 2005). Other thiotrophic communities with higher diversity (including Thioploca and Thiomargarita) exhibit a gray color (Lichtschlag et al., 2006). The patchy distribution of these mats in a seep habitat is largely dependent on the extent and duration of the reduced fluid (H2S) emissions.

The source of carbon in a seep ecosystem is strongly imprinted in the carbon isotopic composition of the tissues of invertebrate and microbial communities, and the authigenic carbonates. The rather negative 513C excursions measured on both biological and geological components (Campbell et al., 2002) of seep environments come from the microbial oxidation of hydrocarbons (oil and methane), which are the main carbon source. On average, biogenic methane is more depleted in 513C than thermogenic methane, and can reach extremely negative 513C values: less than -100%c (PDB) (Schoell, 1988). 513C values as low as -69%c, as measured in Cenozoic high Mg-calcite (Campbell et al., 2002), represent a permanent signature in the geological record and are a useful diagnostic feature for documenting methane seep activity.

The microbial community structure and activity at methane seep sites is complex and is not only limited to the seafloor. Methanotrophs are also distributed in the overlying water column, as is the case in the Black Sea, where archaea and bacteria have been detected in both anoxic and oxic waters above seep sites (Durisch-Kaiser et al., 2005). Archaeal and bacterial communities are also found to occur consistently in deep marine sediments that are associated with methane hydrates (Inagaki et al., 2006). The recent record of microbial CH4, from fluid inclusions detected in the low-temperature hydrothermal silica of the early Archean-aged Dresser Formation in the Pilbara Craton, Western Australia (Ueno et al., 2006), is the oldest evidence of the activity of methanogenic microbes at an early (and probably Mars-like) stage of the evolution the Earth's atmosphere.j

Methanotrophic symbiont-bearing macroinvertebrates, such as certain living mussels (Childress et al., 1986), or other taxa with methanotrophic food sources, such as certain polychaete species (Fisher et al., 2000), are strongly depleted 513C. The strongest depletions (values around -110%e), however, have been measured in lipid biomarkers as archaeol, the most common ether lipid in archaea, hydroxyarchaeol, and crocetane, derived from methanotrophic archaea and other microbial consortia (Hinrichs et al., 1999; Treude et al., 2005). Conversely, in the Gulf of Mexico, the isotopic compositions of lipid biomarkers typifying sulfur-oxidizing bacteria (Beggiatoa) associated with gas hydrates (Zhang et al., 2005), and of bulk Beggiatoa mats (Sassen et al., 1993), are slightly less than -30%c, and indicate that they used carbon from a non-methane origin. In methane seeps of the Californian continental margin, however, lower values (around -50%e) from Beggiatoa mats have been measured (Orphan et al., 2001).

4. Microbial-Induced Fossils, Fabrics and Minerals of Seep Deposits

Primary among the geobiological interactions involved in the preservation of fossils (Bottjer, 2005) are those performed by microbes in a wealth of environmental conditions, whereby they promote mineral dissolution and diagenesis, and authi-genic mineral precipitation (Ehrlich, 1998). Microbiologically induced mineralization, whether passively or actively promoted, have profoundly influenced the composition of the lithosphere and the fossil record as a whole. Although still underestimated, the mineral by-products of the interaction between microorganisms and physico-chemical environments (in the sense given by Lowenstam, 1981) have provided the Earth's surface with the most common type of fossils: microbes and microbial-derived structures.

The preservation potential of cold seep ecosystems throughout the geologic record is mostly determined by authigenic carbonate precipitation induced by microbes in anoxic conditions. The resulting complex carbonates contain accumulations of clams, tube worms, brachiopods, and other seep-related megafaunal components, and can also store microbial remains and other products of these

Giant Beggiatoa
Figure 1. Reflected light micrograph of a polished surface. Large filaments interpreted as giant Beggiatoa embedded in a microsparite groundmass from Miocene-aged seep carbonates, northern Italy. Average diameter of the filaments is 90-100 |m.

chemosynthetic ecosystems. A compelling example is the extraordinarily well-preserved mats of giant Beggiatoa-type filaments from Miocene-aged seep carbonates of northern Italy (Fig. 1). The preservation of these unique filamentous microbes relies on early, microbially-mediated diagenetic events that produced aragonite cement fringes around the giant filaments (Barbieri et al., 2001; Peckmann et al., 2004; Barbieri and Cavalazzi, 2005).

The groundmass of seep deposits, however, generally consists of authigenic micrite and microcrystalline calcite forming crusts, mounds, and chimneys that are strongly depleted in 513C. This authigenic micrite may often consist of microbial clotted fabrics (Peckmann et al., 1999, 2001). Other carbonate (high-Mg calcite, aragonite, and dolomite) textures are variously interpreted as the product of microbial activity, they include botryoids, peloids, rhomboids, spheroids, dumbbell-shaped structures in the hollow cores of minerals (Terzi et al., 1994; Savard et al., 1996; Cavagna et al., 1999; Peckmann et al., 1999, 2001; Aharon, 2000; Peckmann and Thiel, 2004; Barbieri and Cavalazzi, 2005). Early diagenesis is often related to the above textures. Radial fibrous, sparry and scalenoedral cements, which are typical early diagenetic products in the development of a seep-carbonate body, have been interpreted as products of microbial processes. Because of their early precipitation, these cements can also favor the preservation of delicate microbial morphologies (Fig. 1).

Morphologies interpreted as mineralized biofilms have been described in Cenozoic seep deposits, and include the coating of the dolomitic matrix (Peckmann et al., 1999) and membranous structures incorporating mineral and clastic grains (Shapiro, 2004; Barbieri and Cavalazzi, 2005). Their negative 513C values further enable an interpretation as biofilms produced by methanotrophic bacteria.

Stromatolite morphologies may be present in fossil (Kelly et al., 1995) and modern seep (Greinert et al., 2002) ecosystems. Submillimeter-scale microcolum-nar buildups have been described as microstromatolites in the laminated infill of veins crosscutting the Devonian mounds of Hamar Laghdad (Anti-Atlas, Morocco), where 513C values suggest relationships with hydrocarbon-rich fluids (Cavalazzi et al., 2007).

Apart from the case of the giant Beggiatoa mentioned above, preserved bacterial cells and colonies are comparatively rare in seep deposits. Bacteriomorphs as cocci, rods, and filaments are limited to rock portions in which early carbonate (or other mineral) precipitation has allowed their preservation. Cocci and rods have been described in a Pliocene seep of northern Apennine (Cavalazzi and Barbieri, 2006) and in the Cretaceous Tepee Buttes, Colorado (Fig. 2) (Shapiro, 2004), whereas intertwined and closely packed filamentous structures make up well-developed microbial mats in the Devonian mounds of Anti-Atlas, Morocco (Fig. 3) (Cavalazzi, 2007; Cavalazzi et al., 2007).

Bacterial clusters are often coated by amorphous membranes, which are interpreted as EPS (extracellular polymeric substances). The EPS are more frequently recovered as fossils than cells by themselves. The higher fossilization potential of EPS biofilms results from their abundance (cell colonies are usually embedded in protective biofilms that greatly stabilize the microbial environments) and a better resistance to degradation than single cells. The high affinity of EPS for calcium (and other) ions should also favor mineralization, and consequently, calcium carbonate precipitation (Altermann et al., 2006).

Together with generic biofilm textures, more architecturally complex structures have been described from fossil seeps. In the Silurian hematite-rich carbonate

Fossil Microbe Silice
Figure 2. Scanning electron microscope (SEM) image of fossilized sheaths containing calcite crystals in the centers from Cretaceous seep carbonates, Colorado. (Image reprinted with permission from Shapiro, 2004.)

Figure 3. Transmitted light micrographs from a pétrographie thin section of laminated carbonate infilling veins cutting a Devonian-aged paleoseep, Anti-Atlas, Morocco. (A) Stromatolitic fabric with thin interlayers made up of intertwined filaments. Scale bar: 5 mm. (B) Details of filaments with an average diameter of 3-5 |m. Scale bar: 30 |m. (Images reprinted with permission from Cavalazzi et al., 2007.)

Figure 3. Transmitted light micrographs from a pétrographie thin section of laminated carbonate infilling veins cutting a Devonian-aged paleoseep, Anti-Atlas, Morocco. (A) Stromatolitic fabric with thin interlayers made up of intertwined filaments. Scale bar: 5 mm. (B) Details of filaments with an average diameter of 3-5 |m. Scale bar: 30 |m. (Images reprinted with permission from Cavalazzi et al., 2007.)

deposits near Khenifra, Morocco, packed with the remnants of the most ancient-known seep derived ecosystem (Barbieri et al., 2004), early mineral (hematite) replacement let to the preservation of complex, three dimensional structures (Fig. 4) that are interpreted as the product of Beggiatoa-like mats. Morphological analogues of these microbially induced alveolar textures have been described from Pliocene-aged, seep carbonate accumulations (Barbieri and Cavalazzi, 2005), and other fossil settings, such as the Carboniferous-aged Panther Seep Formation in New Mexico (Chafetz et al., 1993), and the stromatolites of the Miocene-aged Monterey Formation in California (Williams, 1984). The modern analogues include microbial mats of modern lagoons (cyanobacteria) (Bauld et al., 1993; Sprachta et al., 2001), and deep marine settings (sulfide-oxidizing chemotrophic Beggiatoa) (Williams and Reimers, 1983). Because of their recurrence through time in microbially derived systems that were developed in different environmental settings, along

Figure 4. Three dimensional alveolar structures of inferred microbial origin from Silurian seep carbonates, central Morocco. The frame is made up of hematite and the infill is calcium carbonate. (A) Transmitted light micrograph. Scale bar: 10 |m. (B) Scanning electron microscope (SEM) image of HCl-etched rock surface. Scale bar: 10 |im. (Image B reprinted with permission from Barbieri et al., 2004.)

Figure 4. Three dimensional alveolar structures of inferred microbial origin from Silurian seep carbonates, central Morocco. The frame is made up of hematite and the infill is calcium carbonate. (A) Transmitted light micrograph. Scale bar: 10 |m. (B) Scanning electron microscope (SEM) image of HCl-etched rock surface. Scale bar: 10 |im. (Image B reprinted with permission from Barbieri et al., 2004.)

with their fossilization potential, these alveolar morphologies deserve a remarkable amount of interest.

Useful tracers for documenting the relationships between methane seeps and microbes in the geologic record are lipid biomarkers (chemofossils). In fossil seeps these complex organic compounds include 513C-depleted archaeal isoprenoids, hopanoids, and non-isoprenoidal lipids (Peckmann and Thiel, 2004) derived from contributions by various microbiotic sources.

Sulfide minerals, especially authigenic pyrite, are distributed within microfractures and intergranular spaces (Cavagna et al., 1999), scattered in seep-carbonates and locally forming pyrite rims across the length of corroded surfaces (Peckmann et al., 2001; Campbell et al., 2002). Pyrite occurs as grains, rods, palisade-like, regular framboids (from a few micrometers to several tens of microns), concentric layers, and represents a precipitation product related to the metabolism of sulfate reducing bacteria in anoxic seep sediments (Cavagna et al., 1999; Peckmann et al., 2001; Peckmann and Thiel, 2004; Sassen et al., 2004; Chen et al., 2006). Other iron sulfides, such as the ferromagnetic greigite, accumulate by anaerobic magne-totactic bacteria in methane-derived carbonates and associated microbial ecosystems (Reitner et al., 2005).

Barite, arranged in banded or layered, porous deposits, is another important, although rare, seep-related authigenic mineral. It occurs as a concretion, mound, and chimney (Koski and Hein, 2003), and represents a useful record for documenting past and present seep activity. The amount of barite precipitation depends on the seepage intensity, on the available sulfate and barium, and on biogeochemical processes governed by the microbial oxidation of methane (Aloisi et al., 2004).

Bio-induced iron minerals, such as hematite, may provide a characteristic reddish pigmentation in the micritic seep deposits (Barbieri et al. 2004) as a possible consequence of the mineral dispersion of this Fe oxide, previously accumulated via intracellular biomineralization, by bacterial cell lysis.

5. Astrobiological Perspectives

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