Biomolecules from Fossilized Hot Spring Sinters: Implications for the Search for Life on Mars

Abstract

Hot spring environments are commonly dominated by silica sinters that precipitate by the rapid cooling of silica-saturated fluids and the activity of microbial communities. However, the potential for preservation of organic traces of life in silica sinters back through time is not well understood. This is important for the exploration of early life on Earth and possibly Mars. Most previous studies have focused on physical preservation in samples <900 years old, with only a few focused on organic biomarkers. In this study, we investigate the organic geochemistry of hot spring samples from El Tatio, Chile and the Taupo Volcanic Zone, with ages varying from modern to ∼9.4 ka. Results show that all samples contain opaline silica and contain hydrocarbons that are indicative of a cyanobacterial origin. A ∼3 ka recrystallized, quartz-bearing sample also contains traces of cyanobacterial biomarkers. No aromatic compounds were detected in a ∼9.4 ka opal-A sample or in a modern sinter breccia sample. All other samples contain naphthalene, with one sample also containing other polyaromatic hydrocarbons. These aromatic hydrocarbons have a thermally mature distribution that is perhaps reflective of geothermal fluids migrating from deep, rather than surface, reservoirs. These data show that hot spring sinters can preserve biomolecules from the local microbial community, and that crystallinity rather than age may be the determining factor in their preservation. This research provides support for the exploration for biomolecules in opaline silica deposits on Mars.

1. Introduction

Biosignatures are distinctive suites of durable textural, mineralogical, and chemical indicators of life (Bock and Goode, 1996; Farmer, 1999, 2000; Farmer and Des Marais, 1999; Jones et al., 2001a; Jones and Renaut, 2003; Philippot et al., 2007; Glikson et al., 2008; Preston et al., 2008; Van Kranendonk et al., 2008; Campbell et al., 2015a, 2015b; Westall et al., 2015a, 2015b; Morag et al., 2016; Djokic et al., 2017). The search for biosignatures on Mars has been guided by our knowledge of preservational pathways on Earth (Walter and Davies, 1999). For macroscopic fossils, microfossils, and many types of textural biosignatures, silica is the best preserving mineral, effectively entombing organisms and their constructed edifices within the fine matrix of various silica phase minerals (e.g., opal-A, opal-CT/C, microcrystalline quartz or chert: Walter and Des Marais, 1993; Guido et al., 2010; Brasier et al., 2011; Campbell et al., 2015b; Tarhan et al., 2016). For example, the preservation of ancient life signatures in Archean rocks from the Pilbara Craton of Australia is overwhelming in cherts (e.g., Sugitani et al., 2009, 2010, 2013) or in diagenetically silicified carbonates (e.g., Hofmann et al., 1999). Carbonates from throughout the geological record, on the other hand, typically do not preserve microfossils unless silicified early in diagenesis (Guido and Campbell, 2012). This is because of the high crystallization energy of carbonate, which has been reported to cause the destruction of prokaryotic cell-sized fossils, as well as organic matter readily becomes remineralized to carbonate through diagenesis (e.g., Altermann and Kazmierczak, 2003).

Siliceous hot spring deposits, or sinters, precipitate due to the rapid cooling and evaporation of silica-saturated fluids, as well as from biomediation (e.g., Kaur et al., 2008). As with Archean cherts, it has been well documented that young (i.e., Phanerozoic) sinters preserve not only textural biosignatures but also microfossils (e.g., Campbell et al., 2001, 2015a; Jones and Renaut, 2001a; Konhauser et al., 2001; Ruff and Farmer, 2016). To date, however, most studies on sinter have focused on textural preservation, with only a small proportion having evaluated the preservation of organic geochemical biomolecules from the microbial communities that inhabited the silicifying hot spring waters (e.g., Siljeström et al., 2017; Sanchez-Garcia et al., 2019). Even fewer studies have prospected for fossilized biomolecules encased in well-preserved mineral deposits (i.e., those with opaline silica: Kaur et al., 2008, 2011; Gibson et al., 2014; Campbell et al., 2015a). To date, the oldest identified biomolecules in sinters are 900 years old (Kaur et al., 2008; Hays et al., 2017).

1.1. Astrobiological implication for siliceous hot spring sinters

Siliceous hot spring sinters are promising targets in early life studies and in the search for life on Mars. When silica first precipitates to build up a sinter deposit, it comprises noncrystalline (amorphous) opal-A. As sinter undergoes diagenesis, opal-A transforms to paracrystalline opal-CT, followed by opal-C, and finally to microcrystalline quartz, or microquartz (Herdianita et al., 2000). Although age can sometimes be used as an estimate of the crystallinity, these silica stages are not always spatially or temporally uniform. The degree of crystallinity among sinter deposits can depend on other factors such as variable fluid components and the degree of fluid mobilization (Campbell et al., 2001).

Considering this, the presence of opaline silica observed on Mars suggests that minimal diagenesis/recrystallization has occurred, for at least some inferred hydrothermal deposits, such as Columbia Hills (Squyres et al., 2008; Ruff et al., 2011). H₂O-poor opaline silica also has been detected at Nili Patera on Mars, where Skok et al. (2010) suggested that the presence, distribution, and chemical composition of this silica on a mound immediately adjacent to a volcanic center indicates a hydrothermal origin.

Since modern to ancient (∼3.5 Ga) terrestrial hot spring systems on Earth that display varying degrees of crystallization preserve signs of microbial life (e.g., Ruff and Farmer, 2016; Djokic et al., 2017, 2020; Ruff et al., 2019), the well-preserved martian hydrothermal deposits become promising astrobiological targets. Hot springs have also been suggested as candidate environments for the origin of life on Earth (Damer and Deamer, 2015; Deamer and Georgiou, 2015; Van Kranendonk et al., 2017). If life originated in a terrestrial hot spring setting, there are implications for the search for life beyond Earth.

NASA's Mars life exploration strategy, which includes a requirement to “follow the water,” is reflected by the Mars Science Laboratory (Grotzinger et al., 2014), which has focused its efforts on determining habitable environments by investigating fluvial and lacustrine settings in Gale crater. These environments will continue to be studied with the Mars2020 mission in Jezero crater (announced by NASA, 2018). So far, results from Gale crater have revealed the presence of organic molecules, but without definitive proof that any of these compounds have a biological origin (Freissinet et al., 2015; Eigenbrode et al., 2018).

In addition, laboratory simulation experiments (Royle et al., 2018) show that chlorinated hydrocarbons detected in Gale crater likely became chlorinated during analysis, and that these compounds have a low likelihood of survival under martian conditions. Further, there is no information on the preservation of organic molecules in silica from Mars, and, indeed, this topic is not well studied, even on Earth.

Research into the preservation of fossilized biomolecules from microbial cell membranes has primarily concentrated on data from the opaline sinter terrace of Champagne Pool in the Taupo Volcanic Zone (TVZ), New Zealand (Kaur et al., 2008; Gibson et al., 2014), which occupies a 900-year-old hydrothermal explosion crater (Lloyd, 1959). However, these data do not necessarily reflect other hydrothermal systems, because the primary controls on lipid preservation in hydrothermal sinters have been suggested to be thermal alteration, high temperatures, and variable pH values of the hot spring waters, which vary from pool to pool (Pancost et al., 2006). This highlights the need for not only cross-locational studies but also ones that span a range of ages, pH, and silica mineral phase crystallinity.

Here, we investigate preserved biomolecules in samples of siliceous hot spring sinters from El Tatio, Chile (Fernandez-Turiel et al., 2005), and from the TVZ, New Zealand (Houghton et al., 1995). Samples analyzed here span an age range from actively forming, to fossil deposits (∼9.4 ka), and from rocks that preserve primary opal-A to those that are recrystallized to microcrystalline quartz. This study examines the potential for sinters to preserve biomolecules of their entombed microbial community over time, and it provides an additional context for the exploration of biosignatures in hot spring deposits on Mars.

2. Sample Acquisition

2.1. El Tatio, Chile

Three modern opal-A sinter samples were collected from the El Tatio hydrothermal field in the high Andes of northern Chile (22°20′S, 68°01′W), which experiences high evaporation and low precipitation rates at an elevation of ∼4300 m at the edge of the Atacama Desert (e.g., Nicolau et al., 2014). All samples were collected with permission issued in 2017 by the presidents of the indigenous communities of Caspana (Jilberto Anza) and Toconce (Abel Bartolo), which oversee El Tatio.

Sample ET2-1 (22°20′43.71″S 68°00′43.97″W) is a nodular sinter with poorly developed digitate structures collected from a discharge channel with green and nearly black biofilms (Fig. 1A, D). Its location was ∼7 m downstream of a ∼1-m-diameter spring mound discharging water with a temperature of ∼77°C and near neutral pH, although cooled to <40°C at the position of the sample.

FIG. 1.

Sample locations at El Tatio, Chile. (A) ET2-1, including adjacent spring mound. (B) ET3-2, including the geyser pool source. (C) ET4-4, showing the rock sampled and surrounding damp ground. (D) Photograph of the sample ET2-1. (E) Photograph of the sample ET3-2. (F) Photograph of the sample ET4-4. Scale bar is 1 cm. Color images are available online.

Sample ET3-2 (22°20′32.74″S 68°00′46.90″W) is also a nodular sinter with poorly developed digitate structures that came from a dry, but recently flowing, discharge channel with no apparent biofilm (Fig. 1B, E). Temperature and pH were measured at the source, a geyser pool ∼5 m from the sampling location, with ∼85°C water (boiling point at the elevation of the location) and near neutral pH.

Sample ET4-4 (22°19′56.51″S 68°00′41.93″W) is a sinter breccia located ∼10 m downstream of an active geyser producing shallow discharge flows at near neutral pH (Fig. 1C, F). The sample was broken off from a larger piece of loose sinter breccia (∼30-cm-long dimension) resting on damp regolith.

2.2. The TVZ, New Zealand

The TVZ is a 60-km-wide by ∼300-km-long rifted arc basin, in North Island, New Zealand (Wilson and Rowland, 2016). It is the largest and most active rhyolitic magmatic system on Earth, and it is accompanied by more than 20 large hydrothermal fields (Houghton et al., 1995). Four samples from the TVZ were analyzed. All samples were collected with permission from the landowners and/or the New Zealand Department of Conservation.

First, a modern conical tufted, opal-A sinter (Tokaanu) was collected from the Hipua-Waihi field, ∼50 km SW of Taupo. This field consists of ∼5000 m³ of sinter deposited over 6000 years (Soto et al., 2019). Conical tufted samples are found in the mid-apron, where temperatures were between 45°C and 65°C (Fig. 2).

FIG. 2.

Schematic cross-section of a near-neutral pH, alkali chloride, Si-bearing hot spring. The connected sinter morphologies and temperature gradients are shown. Figure modified from Campbell et al. (2015b).

Second, a Subrecent sample from Te Puia is an opal-A sinter with distinct microbial palisade texture (e.g., Campbell et al., 2015a) and is from a part of the terrace with a pH 8.5–9.15 (Jones et al., 2001b). Palisade textures occur when fine filaments are densely packed in vertical pillar structures (Campbell et al., 2015b). Palisade textures are typically formed from photosynthetic cyanobacteria, which are associated with the low-temperature environments in the distal apron (Fig. 2; Campbell et al., 2015b).

Third, a ∼9.4 ka sample of packed fragmental opal-A sinter was collected from Mangatete, which is a fossil hydrothermal field of ∼2 km² area located in the Taupo Fault Belt (Drake et al., 2014). Packed fragmental sinter (PFS) textures are known from the Jurassic in Patagonia, and even the Paleoarchean of Australia (Djokic et al., 2020). Modern PFS constitutes a porous sinter matrix with stacked, broken sheets of irregular, angular, mostly highly tabular, silicified microbial fragments, and which has been interpreted to form where fast flowing, warm (50°C), alkali-chloride thermal streams break up silicified microbial mats (Guido and Campbell, 2011; Drake et al., 2014).

Finally, a ∼3.5 ka sample comes from a sinter buttress in the Te Kopia hydrothermal field (38°24′S 176°13′). It is composed of microcrystalline quartz and contains microbial sinters that have a streamer fabric and microbial palisade fabric (Martin et al., 2000), both of which are observed from channels and in the distal sinter apron at temperatures of <40°C (Fig. 2; Campbell et al., 2015a).

3. Methods

3.1. Sample preparation

The samples in this study, except the one from Te Puia, were broken off from outcrop by use of a geological hammer and placed in sealed plastic bags until analysis. The Te Puia sample was obtained from historical collections stored in rock trays in the University of Auckland petrological collection.

A mixture of dichloromethane (DCM, Honeywell) and methanol (MeOH, Honeywell) (9:1 v/v) was used to extract surficial contaminants before crushing, as these samples were not collected cleanly (e.g., George et al., 2007, 2008; Sherman et al., 2007). The samples were placed in beakers and covered with a mixture of DCM and MeOH (9:1 v/v). The beaker was sonicated for two cycles of 10 min and rested for 5 min in between. This outside rinse solution was reduced by a rotary evaporator until less than 2 mL remained and was then transferred by pipette into a 2-mL vial. The vial was spiked with three compounds as internal standards by adding 1 mL of a DCM solution (solution-1) containing about 117 ng each of anthracene-d10 (98 atom%D, Isotec), p-terphenyl-d14 (98 atom %D, Isotec), and tetracosane-d50 (98 atom %D, Isotec).

The outside rinse was then checked to ensure there were minimal contaminants by gas chromatography-mass spectrometry (GC-MS). Once the chromatograms obtained from the GC-MS were checked, the samples were cut with a diamond blade and crushed with a tungsten carbide ring mill crusher. Before cutting and crushing, a blank was performed on both the saw and the crusher. The outer 3–5 mm of the sample was cut off and not extracted, so as to minimize contamination from sample collection. These external offcuts from the samples were made into thin sections. Petrographic examination of thin sections was undertaken with a Nikon Eclipse Ci POL microscope in plain polarized light, with magnifications from 2× to 50× zoom at the University of New South Wales (UNSW).

3.2. Solvent extraction, fractionation, and derivatization

The rock powder was solvent extracted by using a mixture of DCM and MeOH (9:1 v/v) and sonication for 10 min, resting for 5 min, and sonication for a further 10 min (e.g., Hoshino and George, 2015; Hoshino et al., 2015). Between each sonication, the solution was stirred and left to resettle for 5 min. The solvent solution was then decanted into a round bottom flask, and the process was repeated twice more for each sample. The second and third solvent mixtures were added to the first for each sample.

Before rotary evaporation, a blank was performed and the machine was confirmed to be free of contamination. The collected solvent mixtures were reduced by rotary evaporation to ∼40 mL. The samples were centrifuged at 2000 rpm for 10 min to remove fine rock particles, and then the solution was decanted into a round bottom flask. If, after centrifugation, there were still fine particles suspended in the mixture, the mixture was filtered through silica gel (silica gel 60, 0.063–0.200 mm), which was activated at 120°C for >4 h before use.

The samples were fractionated on small scale silica columns in pipettes, using a mixture of hexane and DCM (4:1) to elute an apolar fraction. The apolar fraction was further fractionated into aliphatic and aromatic hydrocarbons by using hexane and the 4:1 solution. The hydrocarbon fractions were spiked with the internal standard solution-1, further evaporated by hot plate and nitrogen blow down, pipetted into a 100-μL vial insert, and finally analyzed by the GC-MS.

3.3. Gas chromatography-mass spectroscopy

The samples were analyzed by GC-MS using a two-dimensional gas chromatograph (Agilent 7890A) operating in one dimension, coupled to a Pegasus time-of-flight-mass spectrometer (GC × GC-ToFMS). The interface was held at 310°C, and the MS source temperature was 280°C. Fractions were injected (1 μL) in a split/splitless injector operating at 310°C in splitless mode onto a J&W DB5MS column (60 m × 0.25 mm i.d., 0.25 mm film thickness) coated with modified 5% phenyl 95% methyl silicone, with 1.5 mL/min He carrier gas flow. The GC column oven temperature was programmed from 40°C (hold for 2 min) to 310°C at 4°C/min and held for 40.5 min.

Aliphatic and aromatic fractions of an international external standard (North Sea Oil) were run by using the same program to aid component assignment. Peak areas were integrated with LECO Chromatof software, and they were quantified relative to the peak areas of the internal standards. This quantification was based on ng/g of rock (after French et al., 2015; Hoshino and George, 2015; Aharonovich and George, 2016). The limit of detection for n-alkanes was 0.5 ng/g, and for aromatic hydrocarbons it was 0.02 ng/g.

4. Results

4.1. Petrography

Thin-section petrographic analysis of sample ET2-1 from El Tatio reveals a polymict clastic sediment, containing fine-grained (up to 300 μm) clasts in an opal-A matrix (Fig. 3A). Some sand-sized clasts are themselves an aggregate of fine-grained clastic material, including angular volcanic glass shards, mica grains (biotite and white micas), and angular quartz and feldspar mineral fragments. These aggregate clasts are rimmed by uneven layers of opal (i.e., point a on Fig. 3A). Other parts of the sample contain multiple, thin, opaline silica rinds that coat bundles of aligned, clear, completely silicified microbial filaments. The opaline silica rind coats, and abuts against, a matrix of opaline silica packed with diatoms (point b on Fig. 3B) and individual sand grains. Well-preserved microbial filaments with orange pigment (point c on Fig. 3B) appear to cut across the boundary between textural domains within the sample, suggesting that these less well-oriented orange filaments grew after those incorporated within the coated grains.

FIG. 3.

Thin-section photomicrographs of analyzed samples, in plane polarized light. (A) Sample ET2-1, showing an opaline silica-coated grain that comprises a variety of sand grains including angular volcanic glass shards, mica grains, and quartz and feldspar, in a silty matrix. Coatings of opaline silica are present (a). Scale bar is 50 μm. (B) Sample ET2-1, consisting of a horseshoe-shaped bulb, rimmed by vertically oriented, silicified microbial filaments (a) within a diatomaceous opaline silica matrix (b), and with younger, pigmented filaments (c). Scale bar is 50 μm. (C) Sample ET3-2, showing a palisade fabric of vertically oriented, orange microbial filaments (a), and digitate columnar stromatolites (b) with fine-scale, overlying laminae. Scale bar is 200 μm. (D) Close-up view of the palisade fabric of orange, microbial filaments from Sample ET3-2. Scale bar is 100 μm. (E) Sample ET4-4, showing a coated grain cored by aligned microbial filaments (a) and rimmed by opaline silica (b). Scale bar is 500 μm. (F) Sample from Mangatete, which is strongly recrystallized but retains the outline and rind of a degraded oncoid (a). Scale bar is 500 μm. Color images are available online.

Sample ET3-2 from El Tatio contains mottled opaline silica layers with microbial palisade texture comprising bright orange cyanobacterial filaments aligned vertically along bedding planes (point a in Fig. 3C, D). Microbial palisade layers are overlain by digitate columnar microstromatolites that are characterized by dark opaline silica in the lower parts of the columns (point b in Fig. 3C), and by fine-scale laminations in the upper parts of the columns.

Sample ET4-4 from El Tatio contains densely packed and poorly sorted oncoids that are 250–500 μm in diameter, which form by wetting and drying cycles of mid-temperature thermal spring discharge on the mid- to distal sinter apron (c.f. Jones and Renaut, 1997; Guido and Campbell, 2011). These show concentric laminations with both angular and rounded nuclei. Some of the oncoids are discoidal, whereas others have lobate edges. Some elongated oncoids have cores composed of aligned microbial filaments that are coated by a series of very thin opaline silica coatings (point b on Fig. 3E). These rinds include a granular, mottled lamina coated by an irregular, dark brown rim, and then by a lighter lamina with detrital infill, which is again coated by a thin dark rind.

The Mangatete sample has a mottled, gray, siliceous matrix with layered, broken, silicified microbial sheets that contain flat lamination throughout, as well as sub-rounded to lobate oncoids (point a on Fig. 3F). The rock matrix is recrystallized to a fine-grained, mottled, silicified patchwork incorporating volcaniclastic silt and sand grains. The embedded oncoids constitute a series of concentric coatings that are preserved despite recrystallization.

The Te Kopia sample is a sinter of fine-grained opaline silica in which no distinctive textures were visible in thin sections. Thin sections were not made for the samples from Te Puia and Tokaanu, as there was insufficient material after organic geochemical analysis.

4.2. Organic geochemistry

4.2.1. n-Alkanes

A series of n-alkanes were detected in all samples (Fig. 4; Supplementary Table S1). The two modern digitate samples from El Tatio (ET2-1 and ET3-2) have bimodal n-alkane distributions. The first mode is from n-C₁₃ to n-C₂₀, with strong enrichments of n-C₁₅ relative to n-C₁₄ and n-C₁₆, and n-C₁₇ relative to n-C₁₆ and n-C₁₈. The second mode is from n-C₂₀ to n-C₃₀, with a very strong odd-over-even carbon number predominance. In ET2-1, the maximum is at n-C₃₀; whereas in ET3-2, the maximum is at n-C₁₇. El Tatio sinter breccia (ET4-4) has n-alkanes ranging from n-C₁₅ to n-C₃₂. This sample has similar n-C₁₅ and n-C₁₇ enrichments relative to the neighboring alkanes, a maximum at n-C₂₇, and a strong odd-over-even carbon number predominance. Carbon preference indices (CPI_22–32) for all three El Tatio samples are 1.5–1.8 (Table 1).

FIG. 4.

Amount (ng/g sample) and distribution of n-alkanes in all samples from this study. Procedural blanks yielded no n-alkanes, except a very small amount of the C₁₀ n-alkane. Color images are available online.

Table 1.

Weights of Samples and Aliphatic Hydrocarbon Ratios for the Samples from El Tatio (Chile) and the Taupo Volcanic Zone, New Zealand

Sample	Weight of powder after crushing (g)	n-C₁₇/((n-C₁₆ + n-C₁₈)/2)	CPI_22-32	Pr/Ph	Pr/n-C₁₇	Ph/n-C₁₈
ET2-1	25.8	10.5	1.54	0.98	0.03	0.25
ET3-2	22.4	7.7	1.81	nd	0.17	nd
ET4-4	25.5	3.3	1.46	0.71	0.07	0.24
Tokaanu	5.6	7.8	1.1	0.98	0.03	0.17
Te Puia	50.1	16.3	1.3	0.90	0.08	0.89
Te Kopia	43.0	5.0	1.0	nd	nd	nd
Mangatete	74.7	2.0	0.9	0.38	0.06	0.14

Pr = pristane, Ph = phytane, CPI_22–32 = carbon preference index of n-alkanes: (2 × (C₂₃ + C₂₅ + C₂₇ + C₂₉ + C₃₁))/(C₂₂ + 2 × C₂₄ + 2 × C₂₆ + 2 × C₂₈ + 2 × C₃₀ + C₃₂).

nd = not detected.

The four New Zealand samples have similar bimodal n-alkane distributions as those from El Tatio, with n-alkanes ranging from n-C₁₀ to between n-C₃₃ and n-C₃₇. In the fossilized Mangatete and Te Kopia sinter samples, n-C₁₃ was not detected, and n-C₁₂ was not detected in the Te Puia sample. Te Puia has a strong odd-over-even predominance similar to the El Tatio samples, whereas the ∼9.4 ka Mangatete sample has a slight even-over-odd predominance (Table 1). Both the modern Tokaanuu and the ∼3.5 ka Te Kopia samples have CPI_22–32 near unity. The two modern samples (Tokaanu and Te Puia) have maxima at n-C₁₇, whereas the maximum in the ∼9.4 ka Mangatete sample is n-C₂₇, and in the ∼3.5 ka Te Kopia sample it is n-C₂₈. The Te Kopia sample is a recrystallized, microcrystalline sample with the lowest total abundance of n-alkanes among all samples (Fig. 1). In contrast, the older ∼9.4 ka Mangatete sample that preserves opal-A has an intermediate abundance of n-alkanes relative to the other samples (Fig. 4).

All samples are enriched in n-C₁₇ compared with neighboring n-alkanes, as measured by the 17/(16 + 18) n-alkane parameter (Table 1; Hoshino and George, 2015), although the strength of that enrichment varies between samples. This n-C₁₇ enrichment is strongest in the digitate structures from El Tatio, and in the modern samples from New Zealand (Te Puia and Tokaanu) (Table 1).

The isoprenoids, pristane (Pr) and phytane (Ph) were detected in all samples except Te Kopia, and phytane was not detected in ET3-2. All samples have Pr/Ph ratios of <1.1, with the ∼9.4 ka recrystallized Mangatete sample having the lowest ratio (0.4; Table 1).

4.2.2. Methylalkanes

Monomethylalkanes (MMAs) were detected in all samples. ET3-2 has MMAs from C₁₂ to C₃₂ (Fig. 5), whereas ET4-4 and ET2-1 have MMAs from C₁₃ to C₃₂. MMAs are present in the Tokaanu sample from C₁₃ to C₃₃, in Te Puia from C₁₄ to C₃₂, in Mangatete from C₁₆ to C₃₁, and in Te Kopia from C₂₃ to C₃₂. For all samples that were found to contain methylheptadecanes (MHeD), it is the mid-chain MMAs (especially including 6-MHeD and 5-MHeD) that are more predominant than 2-MHeD and 3-MHeD (Fig. 5).

FIG. 5.

Partial m/z 57 mass chromatogram of sample ET3-2, showing the n-alkane range from C₁₂ to C₃₅, with zoomed-in segments for monomethylalkanes, including the MHeD, and the C₂₆–C₂₉ MPC, MHC, MHeC, and MOC. Numbers in the insets refer to methyl positions on the methylalkanes. DMHeD = dimethylheptadecane; MHC = methylhexacosanes; MHeC = methylheptacosane; MHeD = methylheptadecanes; MPC = methylpentacosanes; MPD = methylpentadecane; MOC = methyloctacosanes. Color images are available online.

The distribution of MHeDs varies between the samples (Fig. 6). The sample ET3-2 is dominated by 5-MHeD with abundant 6-MHeD, whereas the Mangatete sample contains 6-MHeD as the most abundant, followed by 5-MHeD and the peak due to the co-eluting mid-chain isomers 7-, 8-, and 9-MeHeD.

FIG. 6.

Histogram of mono MHeD distribution in all samples from this study. Abundance is relative to n-C₁₇ (100). Color images are available online.

The most abundant MHeD peak in the ET2-1, ET4-4, and Te Puia samples is due to the mid-chain isomers, followed by 6-MHeD (Fig. 6). In the sample from Tokaanu, the most abundant is 3-MHeD, and for all other MMAs, the 2- and 3-MMAs are more predominant than the mid-chain isomers. In ET3-2 and ET2-1, the mid-chain methylpentadecanes (MPD) are also more predominant than 2-MPD and 3-MPD. In Tepuia, the mid-chain MMAs are more predominant than the 2- and 3-MMAs for the methylhexadecanes, MHeDs, and methyloctadecanes.

There is a strong increase in the relative abundance for the MMAs between C₂₄–C₃₀ for ET4-4, C₂₄–C₃₂ for Tokaanu, C₂₄–C₃₁ for Mangatete, and C₂₅–C₃₀ for Te Kopia. Two unidentified compounds that are tentatively assigned as dimethylheptadecanes (DMHeDs) have a base peak at m/z 57 and an m/z 268 molecular ion (labeled DMHeD? in Fig. 5). A third DMHeD was identified as 5,12-DMHeD, based on retention time and spectral comparison with the spectrum published in the work of Shiea et al. (1990).

4.2.3. Aromatic hydrocarbons

No aromatic compounds were detected in samples ET4-4 or Mangatete, but naphthalene is present in all other samples. The methylnaphthalene (MN) isomers 2-MN and 1-MN are present in both ET2-1 and ET3-2, whereas Tokaanu contains a suite of MN, ethylnaphthalenes, dimethylnaphthalenes, and trimethylnaphthalenes (Fig. 7; Table 2). Fluorene and the 2-, 3-, 1-, and 4-methylfluorene (MF) isomers were detected in both Tokaanu and El Tatio sample ET3-2, with the 2-MF/1-MF ratio of Tokaanu = 1.49, and ET3-2 = 0.49. These samples were the only ones that contained phenanthrene and the four methylphenanthrene (MP) isomers (Fig. 8). Anthracene, 1-MA, and biphenyl were also detected in the Tokaanu sample. The methylnaphthalene ratio for Tokannu (1.21) is much higher than that of ET3-2 (0.76; Table 2). Tokaanu has an ethylnaphthalene ratio of 1.32, a dimethylnaphthalene ratio-1 of 2.8, a trimethylnaphthalene ratio-1 (TNR-1) of 0.67, and a trimethylnaphthalene ratio-2 (TNR-2) of 0.96 (Table 2).

FIG. 7.

Partial m/z 128, 142, 156, and 170 mass chromatograms of the Tokaanu sample. Abundance of each chromatogram relative to naphthalene is shown. DMN = dimethylnaphthalene; EN = ethylnaphthalene; MN = methylnaphthalene; TMN = trimethylnaphthalene.

FIG. 8.

Partial m/z 178 to 192 mass chromatograms of the Tokaanu sample, showing phenanthrene, anthracene, and their methyl derivatives. MA = methylanthracene; MP = methylphenanthrene.

Table 2.

Aromatic Hydrocarbon Ratios for Samples from El Tatio (Chile) and the Taupo Volcanic Zone, New Zealand

Sample	MNR	ENR	DNR-1	TNR-1	TNR-2	MPI	Rc (%) from MPI	MPR
ET3-2	0.76	nd	nd	nd	nd	0.70	0.82	1.42
Tokaanu	1.21	1.32	2.84	0.67	0.96	0.55	0.73	1.32

MNR = methylnaphthalene ratio (2-MN/1-MN); ENR = ethylnaphthalene ratio (2-EN/1-EN); DNR-1 = dimethylnaphthalene ratio ([2,6-DMN + 2,7-DMN])/1,5-DMN); TNR-1 = trimethylnaphthalene ratio-1 (2,3,6-TMN/[1,4,6- + 1,3,5-TMN]); TNR-2 = trimethylnaphthalene ratio-2 ([2,3,6- + 1,3,7-TMN]/[1,4,6- + 1,3,5- + 1,3,6-TMN]); MPI = methylphenanthrene index (1.5 × (3-MP + 2-MP)/(P + 9-MP + 1MP)). Rc = calculated reflectance; MPR = methylphenanthrene ratio (2-MP/1-MP). nd = not detected.

The amount of phenanthrene relative to MPs increases with increasing degree of thermal alteration, and there is also preferential preservation of the β-substituted isomers 3-MP and 2-MP (Radke et al., 1982). Phenanthrene is >5 times more abundant than the MPs (Fig. 8), >8 times for Tokaanu, and almost 6 times for ET3-2. The methylphenanthrene ratio (MPR) for the ET3-2 and Tokaanu samples is 1.42 and 1.32, respectively (Table 2). As a result, the methylphenanthrene index (MPI) was used to derive calculated reflectance (Rc) by using the lower maturity calibration (Rc = (0.6 × MPI) +0.4) (Radke et al., 1982). Rc values are 0.82 for ET3-2 and 0.73 for Tokaanu, showing that both samples have a thermal maturity in the middle of the oil window (Table 2: see Section 5).

5. Discussion

5.1. Depositional environments

All samples have Pr/Ph ratios of <1.1. Values <1.0 are indicative of hypersaline and evaporative conditions (Clark and Philp, 1989), which are common in hydrothermal fluids of alkali chloride composition. Low Pr/Ph values in the El Tatio samples are likely related to the presence of saline waters associated with evaporites (Fernandez-Turiel et al., 2005). The Pr/Ph ratio is higher in ET2-1, which is from a flowing thermal stream, but lower in ET4-4, where the sinter breccia was exposed to moisture but no fluid outflows.

Tokaanu hosts chloride-rich springs (Soto et al., 2019), as does Te Puia (formerly Whakarewarewa, Lloyd, 1975). The Pr/Ph ratios of 0.98 and 0.90 for these two samples, respectively, are consistent with these environments.

Mangatete, however, has a much lower Pr/Ph ratio than the other samples (0.38). Low Pr/Ph ratios have been associated with high sulfur content (Peters et al., 1995), and low values of Pr/Ph (0.4) have also been associated with green and purple sulfur bacteria (Bhattacharya et al., 2017).

5.2. Organic matter inputs

5.2.1. Bacterial input

The high values of the 17/(16 + 18) n-alkane parameter indicate the presence of cyanobacteria in all samples. However, the Mangatete sample differs slightly from other samples studied here in its n-alkane distribution, which appears more similar to the distribution in the green sulfur bacteria Chlorobidium sp. (Shiea et al., 1991). The possibility of a green sulfur bacteria source is supported by the fact that it was necessary to remove elemental sulfur from the Mangatete sample, and because of the low Pr/Ph ratio from this sample, as discussed next.

In the samples studied here, except Te Kopia, we report the presence of mid-chain MMAs, which are the direct products of cyanobacteria (Schirmer et al., 2010). Cyanobacteria are the only microorganisms known to produce mid-chain MMAs, and they are found in most species of cyanobacteria (Shiea et al., 1990; Schirmer et al., 2010; Hoshino and George, 2015).

The most commonly reported organic components derived from cyanobacteria are the 7- and 8-methylalkanes, which have been previously reported as significant components of hot spring cyanobacterial mats (Robinson and Eglinton, 1990; Shiea et al., 1990). Indeed, Robinson and Eglinton (1990) noted that hydrocarbons present in mats in varied environments globally have a varied carbon number range and distribution of mid-chain branched alkanes, but that the composition of the microbial population and environmental effects (e.g., water temperature) may govern the distribution of mid-chain branched alkanes in specific mats.

In modern cyanobacterial monomethylalkane synthesis, 6-MHeD is not a major product (Coates et al., 2014), although some cyanobacterial species (such as Fischerella—a streamer-fabric-producing cyanobacterium found in hot spring environments) produce more 6- and 5-methylalkanes than the 7+-methyl isomers (Coates et al., 2014; He et al., 2015). This trend is similar to the results reported here from two of our samples (Mangatete and ET3-2). In addition, Hoshino et al. (2015) reported 6-MHeD having a higher abundance than 7-MHeD in endolithic bacteria found on the surface of 2.7 Ga stromatolites from limestones in the Pilbara Craton, Western Australia, which they suggested could be related to relative thermal stabilities of the hydrocarbons. Alternatively, wild cyanobacteria may have produced different branched alkanes than their laboratory-cultured counterparts, or perhaps Hoshino et al. (2015) discovered cyanobacteria that had not yet been identified. In the samples from our study, the outer slices were removed, so endolithic cyanobacteria living on the outside of the samples cannot be a source here.

5.2.2. Algal and terrigenous input

The El Tatio samples all have pronounced odd-over-even carbon number predominance (CPI >1) in the long chain n-alkanes. This signature, especially for C₂₇, C₂₉ and C₃₁, is commonly associated with the waxes of vascular plants (Eglinton and Hamilton, 1967). In contrast, the TVZ samples have a CPI near 1.0, which may reflect an algal signal, or a source from sulfate-reducing bacteria. Some of the latter are known to produce long-chain n-alkanes ranging from n-C₂₅ to n-C₃₅ (Ladygina et al., 2006; Melendez et al., 2013). This difference in microbial community composition could explain the differing signals obtained from the TVZ versus the El Tatio samples, where no sulfur is present in the studied materials.

In addition, the high-molecular-weight methylalkanes do not have the same mid-chain predominance in the TVZ samples (Fig. 2), but they rather have 2- and 3-methyl isomers as the predominant input. This signal has been observed in lichen (consisting of an alga and a fungus; Huang et al., 2012), although the source of the compounds remains poorly defined (Huang et al., 2011). Samples with a weak even-over-odd carbon number predominance sometimes also produce these high-molecular-weight methylalkanes, and this signal has been associated with algal organic matter, if the thermal maturity is not high (Cheng et al., 2018), which is not the case for any of the samples studied here (Section 5.3).

5.3. Thermal maturity

The mostly low Ph/n-C₁₈ ratios of 0.14–0.89 are consistent with a thermal maturity in the oil window, as are the low Pr/n-C₁₇ ratios (0.03–0.17) (Table 1; Ten Haven et al., 1987; Aharonovich and George, 2016). The MPI value, which changes with thermal maturity (Radke et al., 1982; Radke, 1988), is 0.55 for Tokaanu, and 0.70 for ET3-2 (Table 2), placing these samples in the early oil window (Rc of 0.73% and 0.82%). The MPR is in agreement that ET3-2 (1.42) has a higher thermal maturity than Tokaanu (1.32). The alkylnaphthalene data and the smooth n-alkane distribution (CPI_22–32 near unity) for Tokaanu are also consistent thermal maturities within the oil window (Table 2).

These data, indicative of temperatures typical in petroleum systems, are unusual for recent sediment/rock samples that have not been buried. The Tokaanu sample comes from the mid-slope of the hot spring sinter apron, an area that is generally a mid-temperature environment (60–45°C; Campbell et al., 2015a), so it seems unlikely that the temperatures indicated by the thermal maturity values are related to the surface-temperature gradient. Rather, several boreholes in Tokaanu show that the surface hydrothermal fluids originate from higher temperatures in the subsurface throughout the field, some of which are higher than 130°C (Soto et al., 2019). The Tokaanu sinter comes from the dissolution of Si-bearing minerals at high temperatures beneath the hydrothermal field (Soto et al., 2019). Thus, these aromatic hydrocarbons with a thermally mature distribution may be reflective of organic matter sourced from subsurface hydrothermal fluids migrating from deeper immature source rocks that have been hydrothermally altered, rather than from the in situ material preserved within the samples. The presence of a significant amount of anthracene, and a small amount of 2-methylanthracene, is consistent with hydrothermal alteration of immature organic matter (e.g., Kawka and Simoneit, 1990; Leif and Simoneit, 1995).

This may also be the case for the ET3-2 sample, which has a slightly higher maturity than Tokaanu based on the alkylphenanthrene distributions. The waters at El Tatio have been interpreted to be heated by the Laguna Colorado ignimbrite caldera complex (Zandt et al., 2003). The primary aquifer has a temperature of 265°C at a depth of 800 m, whereas the surface waters discharged at El Tatio have a temperature of ∼86°C (which is the boiling point at the El Tatio hydrothermal field; Lahsen and Trujillo, 1975). However, this does not explain why these two samples are the only ones studied that have these aromatic compounds. Analysis of further samples is required to ascertain why this is the case.

5.4. Biomarker preservation in hot springs

The fossilized opal-A sample from Mangatete has comparable abundances and a similar compound range to the modern opal-A-bearing samples, even though it is 9.4 ka. However, the younger, ∼3.5 ka, fossilized microcrystalline quartz sample from Te Kopia has fewer, and lower abundance, compounds. It, thus, would appear that the degree of hydrocarbon preservation is, at least in part, related to sample crystallinity arising from the degree of diagenesis. The pristine opal-A sinters preserve more hydrocarbons than samples affected by a greater degree of diagenesis. The reason for this is that, typically, the density of silica minerals increases as diagenesis proceeds (Lynne and Campbell, 2004), resulting in occlusion of porosity and expelling of interstitial organic compounds. During deposition, opal-A encrusts or replaces microbes, and it then continues to precipitate as a cement framework. This process continues as long as the silica saturated waters are flowing, and it can reduce porosity by up to half (Jones and Renaut, 2003). As pore fluids continue to evolve during burial, hydrocarbons may migrate and be carried out of the host rock to imprint a hydrocarbon signature on the mineralogically maturing sinter deposit. In some of our samples, high-temperature signals, such as the alklylnaphthalenes, appear to be overprinting the primary biogenic signal. In these samples, we can detect the low maturity signal due to the cyanobacteria, and the signal from the high maturity migrating fluid.

5.5. Life on Mars

The results from this study have implications for the search for life on Mars. Currently, the search for fossil organics on Mars is focused on lacustrine-deltaic sediments and the regolith. However, this study shows that other strong candidates in the search for biomolecules would be the opal-A deposits at Columbia Hills identified by the Miniature Thermal Emission Spectrometer (Mini-TES; Squyres et al., 2008), hydrothermal silica at Nili Patera identified by the Compact Reconnaissance Imaging Spectrometer for Mars (CRISM; Skok et al., 2010), or perhaps among the high-Si minerals identified by the Chemistry and Camera (ChemCam) instrument, and the Chemistry and Mineralogy (CheMin) instrument in Gale crater (Morris et al., 2016; Frydenvang et al., 2017).

The results presented here are biased by the overwhelming prevalence of photosynthesizers on Earth today and in the recent past (e.g., Hays et al., 2017; Michalski et al., 2018). Although the types of organics we may detect on Mars could be radically different than the cyanobacterial and plant signatures discovered here, hot springs remain some of the most ancient analogs for life on Earth (e.g., Djokic et al., 2017), and thus they provide a window to when Earth and Mars would have been the most similar. Given that silica is known to be an exceptional preserver of microfossils and other biosignatures (e.g., Knoll, 1985; Trewin, 1996), and can act as a potential shield to UV radiation (Phoenix et al., 2002), it becomes a very attractive beacon by which to guide the search for life on Mars, whether or not photosynthesizers existed there. At Columbia Hills, the presence of nodular opaline silica with digitate structures, similar to those from El Tatio sinter known to have been microbially mediated (Ruff and Farmer, 2016; Ruff et al., 2019), provide exciting opportunities to investigate whether life may have ever existed on Mars (Westall et al., 2015a; Cady et al., 2018).

6. Conclusions

Three modern opal-A sinter samples from El Tatio, two modern opal-A sinter samples from the TVZ in New Zealand, a ∼3.4 ka microcrystalline quartz sinter sample from Te Kopia in the TVZ, and a ∼9 ka opal-A sinter sample from Mangatete in the TVZ were investigated for their potential biomolecular preservation state. All samples contain biomarker distributions that are consistent with the presence of cyanobacteria. The samples collectively have Pr/Ph ratios that are reflective of evaporative conditions, consistent with the sinter apron environments from which they were collected. Thermal maturity parameters indicate the presence of organic compounds in the oil window, derived from temperatures higher than those present in the surface environment, suggesting a contribution of organic components from fluids that have undergone convective circulation in the subsurface and, thus, are not solely from microbial remnants indigenous to the rock sample. Overall, hydrocarbon preservation in these samples appears to be affected more by crystallinity—reflecting degree of diagenesis—than by age. These findings are favorable for the search for traces of ancient life in opaline silica deposits on Mars.

Footnotes

Acknowledgments

B.L.T. acknowledges helpful discussions with Bryan Drake and Ayrton Hamilton about sinter aprons. B.L.T. would like to acknowledge and pay her respects to the Bedegal people (UNSW) and the Darug Nation (Macquarie University), the traditional custodians of the land on which this research took place. The authors thank the communities of Caspana and Toconce, Chile for allowing fieldwork and sample collection at El Tatio. Thanks are due to Diego Guido for providing an updated sinter facies-temperature gradient diagram.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

B.L.T. was supported by an Australian Government Research Training Program Scholarship. Funding for this project comes from an Australian Research Council Discovery Grant to M.J.V.K., and samples were collected during research conducted by K.A.C. supported by a Royal Society of New Zealand Marsden grant.

Supplementary Material

Supplementary Table S1

Abbreviations Used

References

Aharonovich

and George

S.C.

(2016) A possible shale gas prospect? First results of the organic composition and thermal maturity of the Carboniferous Namoi Formation, northern NSW, Australia. Aust J Earth Sci, 63:771–780.

Altermann

and Kazmierczak

(2003) Archean microfossils: a reappraisal of early life on Earth. Res Microbiol, 154:611–617.

Bhattacharya

, Dutta

, and Summons

R.E.

(2017) A distinctive biomarker assemblage in an Infracambrian oil and source rock from western India: molecular signatures of eukaryotic sterols and prokaryotic carotenoids. Precambrian Res, 290:101–112.

Bock

G.R.

and Goode

J.A.

, eds. (1996) Evolution of Hydrothermal Ecosystems on Earth (and Mars?). Ciba Foundation Symposium 202. Wiley, Chichester, United. Kingdom.

Brasier

M.D.

, Antcliffe

J.B.

, and Callow

R.H.

(2011) Evolutionary trends in remarkable fossil preservation across the Ediacaran–Cambrian transition and the impact of metazoan mixing. In Taphonomy, edited by Allison

P.A.

and Bottjer

D.J.

, Springer, Dordrecht, pp 519–567.

Cady

S.L.

, Skok

J.R.

, Gulick

V.G.

, Berger

J.A.

, and Hinman

N.W.

(2018) Siliceous hot spring deposits: why they remain key astrobiological targets. In From Habitability to Life on Mars, edited by N.A. Cabrol and E.A. Grin, Elsevier, Amsterdam, Netherlands.

Campbell

K.A.

, Sannazzaro

, Rodgers

, Herdianita

, and Browne

(2001) Sedimentary facies and mineralogy of the late Pleistocene Umukuri silica sinter, Taupo Volcanic Zone, New Zealand. J Sediment Res, 71:727–746.

Campbell

K.A.

, Guido

D.M.

, Gautret

, Foucher

, Ramboz

, and Westall

(2015a) Geyserite in siliceous hot-spring sinter: window on Earth's hottest terrestrial environment and its extreme life. Earth Sci Rev, 148:44–64.

Campbell

K.A.

, Lynne

B.Y.

, Handley

K.M.

, Jordan

, Farmer

J.D.

, Guido

D.M.

, Foucher

, Turner

, and Perry

R.S.

(2015b) Tracing biosignature preservation of geothermally silicified microbial textures into the geological record. Astrobiology, 15:858–882.

10.

Cheng

, Zhang

, Huang

, and Zhang

(2018) The contribution of bacteria to organic matter in coal-measure source rocks. Acta Geochim, 38:1–12.

11.

Clark

J.P.

and Philp

R.P.

(1989) Geochemical characterization of evaporite and carbonate depositional environments and correlation of associated crude oils in the Black Creek Basin, Alberta. Bull Can Petrol Geol, 37:401–416.

12.

Coates

, Podell

, Korobeynikov

, Lapidus

, Pevzner

, Sherman

, Allen

, Gerwick

, and Gerwick

(2014) Characterization of cyanobacterial hydrocarbon composition and distribution of biosynthetic pathways. PLoS One, 9:e85140.

13.

Damer

and Deamer

(2015) Coupled phases and combinatorial selection in fluctuating hydrothermal pools: a scenario to guide experimental approaches to the origin of cellular life. Life, 5:872–887.

14.

Deamer

D.W.

and Georgiou

C.D.

(2015) Hydrothermal conditions and the origin of cellular life. Astrobiology, 15:1091–1095.

15.

Djokic

, Van Kranendonk

M.J.

, Campbell

K.A.

, Walter

M.R.

, and Ward

C.R.

(2017) Earliest signs of life on land preserved in ca. 3.5 Ga hot spring deposits. Nat Commun , 8:15263.

16.

Djokic

, Campbell

K.A.

, Van Kranendonk

M.J.

, Havig

, Walter

M.R.

, and Guido

D.M.

(2020) A reconstructed subaerial hot spring field in the (∼3.5 billion-year-old) Dresser Formation, Pilbara Craton, Western Australia. Astrobiology, 20:000-000.

17.

Drake

B.D.

, Campbell

K.A.

, Rowland

J.V.

, Guido

D.M.

, Browne

P.R.

, and Rae

(2014) Evolution of a dynamic paleo-hydrothermal system at Mangatete, Taupo Volcanic Zone, New Zealand. J Volcanol Geotherm Res, 282:19–35.

18.

Eglinton

and Hamilton

R.J.

(1967) Leaf epicuticular waxes. Science, 156:1322–1335.

19.

Eigenbrode

J.L.

, Summons

R.E.

, Steele

, Freissinet

, Millan

, Navarro-González

, Sutter

, McAdam

A.C.

, Franz

H.B.

, Glavin

D.P.

, and Archer

P.D.

(2018) Organic matter preserved in 3-billion-year-old mudstones at Gale Crater, Mars. Science, 360:1096–1101.

20.

Farmer

J.D.

(1999) Taphonomic modes in microbial fossilization In Size Limits of Very Small Microorganisms, Proceedings of a Workshop. Space Studies Board, Commission on Physical Sciences, Mathematics & Applications. National Research Council. National Academy Press, Washington, DC.

21.

Farmer

J.D.

(2000) Hydrothermal systems: doorways to early biosphere evolution. GSA Today, 10:1–9.

22.

Farmer

J.D.

and Des Marais

D.J.

(1999) Exploring for a record of ancient martian life. J Geophys Res Planets, 104:26977–26995.

23.

Fernandez-Turiel

, Garcia-Valles

, Gimeno-Torrente

, Saavedra-Alonso

. and Martinez-Manent

(2005) The hot spring and geyser sinters of El Tatio, Northern Chile. Sediment Geol, 180:125–147.

24.

Freissinet

, Glavin

D.P.

, Mahaffy

P.R.

, Miller

K.E.

, Eigenbrode

J.L.

, Summons

R.E.

, Brunner

A.E.

, Buch

, Szopa

, Archer

P.D.

, and Franz

H.B.

(2015) Organic molecules in the Sheepbed Mudstone, Gale Crater, Mars. J Geophys Res Planets, 120:495–514.

25.

French

K.L.

, Hallmann

, Hope

J.M.

, Schoon

P.L.

, Zumberge

J.A.

, Hoshino

, Peters

C.A.

, George

S.C.

, Love

G.D.

, Brocks

J.J.

, and Buick

(2015) Reappraisal of hydrocarbon biomarkers in Archean rocks. Proc Natl Acad Sci U S A, 112:5915–5920.

26.

Frydenvang

, Gasda

P.J.

, Hurowitz

J. A.

, Grotzinger

J.P.

, Wiens

R.C.

, Newsom

H.E.

, Edgett

K.S.

, Watkins

, Bridges

J.C.

, Maurice

, Fisk

M.R.

, Johnson

J.R.

, Rapin

, Stein

, Clegg

S.M.

, Schwenzer

S.P.

, Bedford

, Edwards

, Mangold

, Cousin

, Anderson

, Payre

, Vaniman

, Blake

, Lanza

N.L.

, Gupta

, Van Beek

J.K.

, Sautter

, Meslin

P.-Y.

, Rice

, Milliken

, Gellert

, Thompson

, Clark

B.C.

, Sumner

D.Y.

, Fraeman

A.A.

, Kinch

K.M.

, Madsen

M.B.

, Mitofranov

, Jun

, Calef

F.J.

, and Vasavada

A.R.

(2017) Diagenetic silica enrichment and late-stage groundwater activity in Gale crater, Mars. Geophys Res Lett, 44:4716–4724.

27.

George

S.C.

, Volk

, and Ahmed

(2007) Geochemical analysis techniques and geological applications of oil-bearing fluid inclusions, with some Australian case studies. J Petrol Sci Eng, 57:119–138.

28.

George

S.C.

, Volk

, Dutkiewicz

, Ridley

, and Buick

(2008) Preservation of hydrocarbons and biomarkers in oil trapped inside fluid inclusions for >2 billion years. Geochim Cosmochim Acta, 72:844–870.

29.

Gibson

R.A.

, Sherry

, Kaur

, Pancost

R.D.

, and Talbot

H.M.

(2014) Bacteriohopanepolyols preserved in silica sinters from Champagne Pool (New Zealand) indicate a declining temperature gradient over the lifetime of the vent. Org Geochem, 69:61–69.

30.

Glikson

, Duck

L.J.

, Golding

S.D.

, Hofmann

, Bolhar

, Webb

, Baiano

J.C.

, and Sly

L.I.

(2008) Microbial remains in some earliest Earth rocks: comparison with a potential modern analogue. Precambrian Res, 164:187–200.

31.

Grotzinger

J.P.

, Sumner

D.Y.

, Kah

L.C.

, Stack

, Gupta

, Edgar

, Rubin

, Lewis

, Schieber

, Mangold

, Milliken

, Conrad

P.G.

, DesMarais

, Farmer

, Siebach

, Calef III

, Hurowitz

, McLennan

S.M.

, McLennan

S.M.

, Ming

, Vaniman

, Crisp

, Vasavada

, Edgett

K.S.

, Malin

, Blake

, Gellert

, Mahaffy

, Wiens

R.C.

, Maurice

, Grant

J.A.

, Wilson

, Anderson

R.C.

, Beegle

, Arvidson

, Hallet

, Sletten

R.S.

, Rice

, Bell III

, Griffes

, Ehlmann

, Anderson

R.B.

, Bristow

T.F.

, Dietrich

W.E.

, Dromart

, Eigenbrode

, Fraeman

, Hardgrove

, Herkenhoff

, Jandura

, Kocurek

, Lee

, Leshin

L.A.

, Leveille

, Limonadi

, Maki

, McCloskey

, Meyer

, Minitti

, Newsom

, Oehler

, Okon

, Palucis

, Parker

, Rowland

, Schmidt

, Squyres

, Steele

, Stolper

, Summons

, Treiman

, Williams

, Yingst

, and MSL Science

Team.

(2014) A habitable fluvio-lacustrine environment at Yellowknife Bay, Gale Crater, Mars. Science, 343:1242777.

32.

Guido

D.M.

and Campbell

K.A.

(2011) Jurassic hot spring deposits of the Deseado Massif (Patagonia, Argentina): characteristics and controls on regional distribution. J Volcanol Geotherm Res, 203:35–47.

33.

Guido

D.M.

and Campbell

K.A.

(2012) Diverse subaerial and sublacustrine hot spring settings of the Cerro Negro epithermal system (Jurassic, Deseado Massif), Patagonia, Argentina. J Volcanol Geotherm Res, 229:1–12.

34.

Guido

D.M.

, Channing

, Campbell

K.A.

, and Zamuner

(2010) Jurassic geothermal landscapes and fossil ecosystems at San Agustín, Patagonia, Argentina. J Geol Soc, 167:11–20.

35.

Hays

L.E.

, Graham

H.V.

, Des Marais

D.J.

, Hausrath

E.M.

, Horgan

, McCollom

T.M.

, Parenteau

M.N.

, Potter-McIntyre

S.L.

, Williams

A.J.

, and Lynch

K.L.

(2017) Biosignature preservation and detection in Mars analog environments. Astrobiology, 17:363–400.

36.

, Simoneit

B.R.

, Jara

, and Jaffé

(2015) Occurrence and distribution of monomethylalkanes in the freshwater wetland ecosystem of the Florida Everglades. Chemosphere, 119:258–266.

37.

Herdianita

, Browne

, Rodgers

, and Campbell

(2000) Mineralogical and textural changes accompanying ageing of silica sinter. Miner Deposita, 35:48–62.

38.

Hofmann

H.J.

, Grey

, Hickman

A.H.

, and Thorpe

(1999) Origin of 3.45 Ga coniform stromatolites in the Warrawoona Group, Western Australia. Geol Soc Am Bull, 111:1256–1262.

39.

Hoshino

and George

S.C.

(2015) Cyanobacterial inhabitation on Archean rock surfaces in the Pilbara Craton, Western Australia. Astrobiology, 15:559–574.

40.

Hoshino

, Flannery

D.T.

, Walter

M.R.

, and George

S.C.

(2015) Hydrocarbons preserved in a ∼2.7 Ga outcrop sample from the Fortescue Group, Pilbara Craton, Western Australia. Geobiology, 13:99–111.

41.

Houghton

, Wilson

, McWilliams

, Lanphere

, Weaver

, Briggs

, and Pringle

(1995) Chronology and dynamics of a large silicic magmatic system: Central Taupo Volcanic Zone, New Zealand. Geology, 23:13–16.

42.

Huang

, Meyers

P.A.

, Wu

, Jia

, and Xie

(2011) Significance of long chain iso and anteiso monomethyl alkanes in the Lamiaceae (mint family). Organic Geochem, 42:156–165.

43.

Huang

, Xue

, and Guo

(2012) Long chain n-alkanes and their carbon isotopes in lichen species from western Hubei Province: implication for geological records. Front Earth Sci, 6:95–100.

44.

Jones

and Renaut

R.W.

(1997) Formation of silica oncoids around geysers and hot springs at El Tatio, northern Chile. Sedimentology, 44:287–304.

45.

Jones

and Renaut

R.W.

(2003) Hot spring and geyser sinters: the integrated product of precipitation, replacement, and deposition. Can J Earth Sci, 40:1549–1569.

46.

Jones

, Renaut

R.W.

, and Rosen

M.R.

(2001a) Taphonomy of silicified filamentous microbes in modern geothermal sinters—implications for identification. Palaios, 16:580–592.

47.

Jones

, Rosen

M.R.

, and Renaut

R.W.

(2001b) “Geyser Eggs” from Te Whakarewarewatangaoteopetauaawahiao, North Island, New Zealand. J Sediment Res, 71:190–204.

48.

Kaur

, Mountain

B.W.

, and Pancost

R.D.

(2008) Microbial membrane lipids in active and inactive sinters from Champagne Pool, New Zealand: elucidating past geothermal chemistry and microbiology. Org Geochem, 39:1024–1028.

49.

Kaur

, Mountain

B.W.

, Hopmans

E.C.

, and Pancost

R.D.

(2011) Preservation of microbial lipids in geothermal sinters. Astrobiology, 11:259–274.

50.

Kawka

O.E.

and Simoneit

B.R.T.

(1990) Polycyclic aromatic hydrocarbons in hydrothermal petroleums from the Guaymas Basin spreading center. Appl Geochem, 5:17–27.

51.

Knoll

A.H.

(1985) Exceptional preservation of photosynthetic organisms in silicified carbonates and silicified peats. Philos Trans R Soc Lond B Biol Sci, 311:111–122.

52.

Konhauser

K.O.

, Phoenix

V.R.

, Bottrell

S.H.

, Adams

D.G.

, and Head

I.M.

(2001) Microbial–silica interactions in Icelandic hot spring sinter: possible analogues for some Precambrian siliceous stromatolites. Sedimentology, 48:415–433.

53.

Ladygina

, Dedyukhina

E.G.

, and Vainshtein

M.B.

(2006) A review on microbial synthesis of hydrocarbons. Process Biochem, 41:1001–1014.

54.

Lahsen

and Trujillo

(1975) El Tatio geothermal field. In Proceedings of the Second United Nations Symposium on the Development and Use of Geothermal Resources, San Francisco, CA, 1:170–177.

55.

Leif

R.N.

and Simoneit

B.R.T.

(1995) Confined-pyrolysis as an experimental method for hydrothermal organic synthesis. Orig Life Evol Biosph, 25:417–429.

56.

Lloyd

E.F.

(1959) The hot springs and hydrothermal eruptions of Waiotapu. N Zeal J Geol Geophys, 2:141–176.

57.

Lloyd

E.F.

(1975) Geology of Whakarewarewa Hot Springs: New Zealand Department of Scientific and Industrial Research, Information Series No. 111. Wellington, AR Shearer, Government. Printer.

58.

Lynne

B.Y.

and Campbell

K.A.

(2004) Morphologic and mineralogic transitions from opal-A to opal-CT in low-temperature siliceous sinter diagenesis, Taupo Volcanic Zone, New Zealand. J Sediment Res, 74:561–579.

59.

Martin

, Mildenhall

D.C.

, Browne

P.R.

, and Rodgers

K.A.

(2000) The age and significance of in-situ sinter at the Te Kopia thermal area, Taupo Volcanic Zone, New Zealand. Geothermics, 29:367–375.

60.

Melendez

, Grice

, Trinajstic

, Ladjavardi

, Greenwood

, and Thompson

(2013) Biomarkers reveal the role of photic zone euxinia in exceptional fossil preservation: an organic geochemical perspective. Geology, 41:123–126.

61.

Michalski

J.R.

, Onstott

T.C.

, Mojzsis

S.J.

, Mustard

, Chan

Q.H.

, Niles

P.B.

, and Johnson

S.S.

(2018) The Martian subsurface as a potential window into the origin of life. Nat Geosci, 11:21–27.

62.

Morag

, Williford

K.H.

, Kitajima

, Philippot

, Van Kranendonk

M.J.

, Lepot

, Thomazo

, and Valley

J.W.

(2016) Microstructure-specific carbon isotopic signatures of organic matter from ∼3.5 Ga cherts of the Pilbara Craton support a biologic origin. Precambrian Res, 275:429–449.

63.

Morris

R.V.

, Vaniman

D.T.

, Blake

D.F.

, Gellert

, Chipera

S.J.

, Rampe

E.B.

, Ming

D.W.

, Morrison

S.M.

, Downs

R.T.

, Treiman

A.H.

, and Yen

A.S.

(2016) Silicic volcanism on Mars evidenced by tridymite in high-SiO₂ sedimentary rock at Gale crater. Proc Natl Acad Sci U S A, 113:7071–7076.

64.

NASA. (2018) NASA announces landing site for Mars 2020 Rover. Available online at https://www.nasa.gov/press-release/nasa-announces-landing-site-for-mars-2020-rover (accessed December 10, 2018 ).

65.

Nicolau

, Reich

, and Lynne

(2014) Physico-chemical and environmental controls on siliceous sinter formation at the high-altitude El Tatio geothermal field, Chile. J Volcanol Geotherm Res, 282:60–76.

66.

Pancost

, Pressley

, Coleman

, Talbot

, Kelly

, Farrimond

, Schouten

, Benning

, and Mountain

(2006) Composition and implications of diverse lipids in New Zealand geothermal sinters. Geobiology, 4:71–92.

67.

Peters

K.E.

, Clark

M.E.

, Gupta

U.D.

, McCaffrey

M.A.

, and Lee

C.Y.

(1995) Recognition of an Infracambrian source rock based on biomarkers in the Baghewala-1 oil, India. AAPG Bull, 79:1481–1493.

68.

Philippot

, Van Zuilen

, Lepot

, Thomazo

, Farquhar

, and Van Kranendonk

M.J.

(2007) Early Archaean microorganisms preferred elemental sulfur, not sulfate. Science, 317:1534–1537.

69.

Phoenix

V.R.

, Konhauser

K.O.

, Adams

D.G.

, and Bottrell

S.H.

(2002) Role of biomineralization as an ultraviolet shield: Implications for Archean life. Geology, 29:823–826.

70.

Preston

L.J.

, Benedix

G.K.

, Genge

M.J.

, and Sephton

M.A.

(2008) A multidisciplinary study of silica sinter deposits with applications to silica identification and detection of fossil life on Mars. Icarus, 198:331–350.

71.

Radke

(1988) Application of aromatic compounds as maturity indicators in source rocks and crude oils. Marine Petrol Geol, 5:224–236.

72.

Radke

, Welte

D.H.

, and Willsch

(1982) Geochemical study on a well in the Western Canada Basin: relation of the aromatic distribution pattern to maturity of organic matter. Geochim Cosmochim Acta, 46:1–10.

73.

Robinson

and Eglinton

(1990) Lipid chemistry of Icelandic hot spring microbial mats. Org Geochem, 15:291–298.

74.

Royle

S.H.

, Tan

, Kounaves

S.P.

, and Sephton

M.A.

(2018) Survivability of 1-chloronapthalene during simulated early diagenesis: implications for chlorinated hydrocarbon detection on Mars. J Geophys Res Planets, 123:2790–2802.

75.

Ruff

S.W.

and Farmer

J.D.

(2016) Silica deposits on Mars with features resembling hot spring biosignatures at El Tatio in Chile. Nat Commun, 7:13554.

76.

Ruff

S.W.

, Farmer

J.D.

, Calvin

W.M.

, Herkenhoff

K.E.

, Johnson

J.R.

, Morris

R.V.

, Rice

M.S.

, Arvidson

R.E.

, Bell

J.F.

, Christensen

P.R.

, and Squyres

S.W.

(2011) Characteristics, distribution, origin, and significance of opaline silica observed by the Spirit rover in Gusev Crater, Mars. J Geophys Res Planets, 116:1–48.

77.

Ruff

S.W.

, Campbell

K.A.

, Van Kranendonk

M.J.

, Rice

M.S.

, and Farmer

J.D.

(2019) The case for hot spring silica sinter in Gusev crater, Mars. Astrobiology, 19:1–25.

78.

Sanchez-Garcia

, Fernandez-Martinez

M.A.

, García-Villadangos

, Blanco

, Cady

S.L.

, Hinman

, Bowden

M.E.

, Pointing

S.B.

, Lee

K.C.

, Warren-Rhodes

K. L

, acap-Bugler

, Cabrol

N.A.

, Parro

, and Carrizo

(2019) Microbial biomarker transition in high-altitude Sinter Mounds from El Tatio (Chile) through different stages of hydrothermal activity. Front Microbiol, 9:1–19.

79.

Schirmer

, Rude

M.A.

, Li

, Popova

, and del Cardayre

S.B.

(2010) Microbial biosynthesis of alkanes. Science, 329:559–562.

80.

Sherman

L.S.

, Waldbauer

J.R.

, and Summons

R.E.

(2007) Improved methods for isolating and validating indigenous biomarkers in Precambrian rocks. Org Geochem, 38:1987–2000.

81.

Shiea

, Brassell

S.C.

, and Ward

D.M.

(1990) Mid-chain branched mono-and dimethyl alkanes in hot spring cyanobacterial mats: a direct biogenic source for branched alkanes in ancient sediments?. Org Geochem, 15:223–231.

82.

Shiea

, Brassell

S.C.

, and Ward

D.M.

(1991) Comparative analysis of extractable lipids in hot spring microbial mats and their component photosynthetic bacteria. Org Geochem, 17:309–319.

83.

Siljeström

, Parenteau

M.N.

, Jahnke

L.L.

, and Cady

S.L.

(2017) A comparative ToF-SIMS and GC-MS analysis of phototrophic communities collected from an alkaline silica-depositing hot spring. Org Geochem, 109:14–30.

84.

Skok

J.R.

, Mustard

J.F.

, Ehlmann

B.L.

, Milliken

R.E.

, and Murchie

S.L.

(2010) Silica deposits in the Nili Patera caldera on the Syrtis Major volcanic complex on Mars. Nat Geosci, 3:838–841.

85.

Soto

M.F.

, Hochstein

M.P.

, Campbell

, and Keys

(2019) Sporadic and waning hot spring activity in the Tokaanu Domain, Hipaua-Waihi-Tokaanu geothermal field, Taupo Volcanic Zone, New Zealand. Geothermics, 77:288–303.

86.

Squyres

S.W.

, Arvidson

R.E.

, Ruff

, Gellert

, Morris

R.V.

, Ming

D.W.

, Crumpler

, Farmer

J.D.

, Marais

D.J.D.

, Yen

, McLennan

S.M.

, Calvin

, Bell

J.F.

, Clark

B.C.

, Wang

, McCoy

T.J.

, Schmidt

M.E.

, and de Souza Jr

P.A.

(2008) Detection of silica-rich deposits on Mars. Science, 320:1063–1067.

87.

Sugitani

, Grey

, Nagaoka

, Mimura

, and Walter

M.R.

(2009) Taxonomy and biogenicity of Archaean spheroidal microfossils (ca. 3.0 Ga) from the Mount Goldsworthy–Mount Grant area in the northeastern Pilbara Craton, Western Australia. Precambrian Res , 173:50–59.

88.

Sugitani

, Lepot

, Nagaoka

, Mimura

, Van Kranendonk

, Oehler

D.Z.

, and Walter

M.R.

(2010) Biogenicity of morphologically diverse carbonaceous microstructures from the ca. 3400 Ma Strelley Pool Formation, in the Pilbara Craton, Western Australia. Astrobiology , 10:899–920.

89.

Sugitani

, Mimura

, Nagaoka

, Lepot

, and Takeuchi

(2013) Microfossil assemblage from the 3400 Ma Strelley Pool Formation in the Pilbara Craton, Western Australia: results form a new locality. Precambrian Res, 226:59–74.

90.

Tarhan

L.G.

, Hood

A.V.

, Droser

M.L.

, Gehling

J.G.

, and Briggs

D.E.

(2016) Exceptional preservation of soft-bodied Ediacara Biota promoted by silica-rich oceans. Geology, 44:951–954.

91.

Ten Haven

H.L.

, De Leeuw

J.W.

, Rullkötter

, and Damsté

J.S.

(1987) Restricted utility of the pristane/phytane ratio as a palaeoenvironmental indicator. Nature, 330:641–643.

92.

Trewin

N.H.

(1996) The Rhynie Chert: an early Devonian ecosystem preserved by hydrothermal activity. In: Evolution of Hydrothermal Ecosystems on Earth (and Mars?). Proceedings of the Ciba Foundation Symposium 202, edited by G.R. Bock, and G.A. Goode, J. Wiley, Chichester, pp. 131–149.

93.

Van Kranendonk

M.J.

, Philippot

, Lepot

, Bodorkos

, and Pirajno

(2008) Geological setting of Earth's oldest fossils in the c. 3.5 Ga Dresser Formation, Pilbara Craton, Western Australia. Precambrian Res , 167:93–124.

94.

Van Kranendonk

M.J.

, Deamer

D.W.

, and Djokic

(2017) Life springs. Sci Am, 317:28–35.

95.

Walter

and Davies

P.C.W.

(1999) The Search for Life on Mars. Perseus Books, Cambridge, MA.

96.

Walter

M.R.

and Des Marais

D.J.

(1993) Preservation of biological information in thermal spring deposits: developing a strategy for the search for fossil life on Mars. Icarus, 101:129–143.

97.

Westall

, Foucher

, Bost

, Loiseau

, Vago

, Kminek

, Gaboyer

, Campbell

K.A.

, Bréheret

J.G.

, and Gautret

(2015a) Biosignatures on Mars: What, where, how?. Astrobiology, 15:998–1029.

98.

Westall

, Campbell

K.A.

, Bréhéret

J.G.

, Foucher

, Gautret

, Hubert

, Sorieul

, Grassineau

, and Guido

D.M.

(2015b) Archean (3.33 Ga) microbe-sediment systems were diverse and flourished in a hydrothermal context. Geology, 43:615–618.

99.

Wilson

C.J.

and Rowland

J.V.

(2016) The volcanic, magmatic and tectonic setting of the Taupo Volcanic Zone, New Zealand, reviewed from a geothermal perspective. Geothermics, 59:168–187.

100.

Zandt

, Leidig

, Chmielowski

, Baumont

, and Yuan

(2003) Seismic detection and characterization of the Altiplano-Puna magma body, central Andes. Pure Appl Geophys, 160:789–807.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.02 MB