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A Terrestrial Hot Spring Setting for the Origin of Life? Darwin’s Warm Little Pond revisited

Pilbara, Western Australia

This is the first holistic, integrated, multinational study ever proposed to investigate the possibility of a terrestrial hot spring field as a setting for the origin of life. The Project is unique in applying an actualistic geological control on an origin of life setting by using the 3.5 Ga Dresser Formation (Pilbara region of Western Australia) – informed by analogues with active hot spring fields – as a guide to constraining the components of an “origins” setting. This Project’s novel approach is to use leading world experts in four fields of research to pursue an actualistic approach to understanding a hot spring “origins” setting through integration of field and analytical work in ancient and modern analogues with detailed, in situ, analyses of hot spring materials, and experimental procedures. Further novelty is provided by the proposed measurements of the chemical and biological aspects of hot spring mixing zones and their use to guide the experimental framework for organic chemistry. The Project is also unique in attempting to integrate whole rock chemistry with the metal budget and transport mechanisms of biologically important trace metals in the ancient Dresser system. This project is funded from the Australian Research Council (DP180103204) and will run from 2018 until 2021.

AIMS AND BACKGROUND 

This Project aims to test the proposal that a terrestrial hot spring field could have been the setting for the origin of life, in preference over the currently favoured site at deep sea vents. This will be achieved through a world-first, integrated, and multi-disciplinary study of the rocks, fluids, and molecules that together make up ancient to modern hot spring systems, and experiments on prebiotic organic chemistry using early Earth materials.

Understanding the origin of life is one of the grand challenges for modern science and gets to the very root of who we are, how we got here, and whether life may exist elsewhere in the solar system. However, knowledge about the origin of life remains elusive due to its complexity, as even the most simple prokaryote is an incredible construct of integrated parts that must have developed in an environment with the capacity for complex chemical interactions. 

Currently, the favoured environment for the origin of life is in a deep sea setting, at either “black” (~400°C, acidic, with sulfide minerals), or “white” (~120°C, alkaline, with carbonate minerals) hydrothermal vents, known as “smokers”. Deep sea vents initially garnered interest as an environment for the origin of life because they contained thriving animal communities supported entirely by chemotrophic micro-organisms1. Deep sea vents continue to be of interest because they have the sharp thermal gradients required to generate complex geochemistry, studies of microbial phylogenies showed that the most primitive microbes were hyperthermophilic, and some vents have the potential for organic polymerisation (the process whereby simple organic molecules are made more complex)2-5

However, deep sea vents – black or white – may not be a suitable environment for the origin of life because:
1) wetting-drying cycles are the most efficient way to polymerise complex organic molecules6,7
2) the K+/Na+ ratios of the interior of all cells are similar to fresh, not marine, waters 8;
3) global oceans are uniform, homogeneous chemical reservoirs that lack the ability to concentrate key elements, such as boron (B) and zinc (Zn), which are critical catalysts for polymerisation8,9; and
4) more recent phylogenetic studies have shown that the most primitive microbes are mesothermophiles10.

These issues have prompted several researchers to suggest that life could have originated on exposed land, in environments ranging from tidal flats, to rivers, or hot springs8,9,11. However, only terrestrial hot springs uniquely satisfy all of the issues identified above 8, 11-13, as they undergo multiple wetting-drying cycles on a daily basis (e.g., Old Faithful geyser at Yellowstone National Park, USA), are composed of fresh water, are known to concentrate elements important for prebiotic chemistry, and contain temperature gradients in the range of mesothermophiles14.
   Furthermore, terrestrial hot springs have the capability for orders-of-magnitude greater complexity than their deep sea counterparts, arising from additional water-air, and rock-air interactions, yet they have the same capacity as deep sea vents for generating complexity via hot water-rock interactions. More importantly, hot spring fields typically contain up to a hundred separate pools, each with potentially different pH, chemistry, temperature, and activity level (still, bubbling, convecting, splashing, fountaining), and all having the ability to exchange materials and energy via wind, splashing, and/or subterranean plumbing networks. Such spatial and thermo-chemical complexity generates “innovation pools” in which the complexity of the field as a whole greatly exceeds that in any single spring (Fig. 1). 
 

                                           
Figure 1: Schematic diagram showing how variation and interaction between hot springs with different chemical properties (different colours) can lead to greater fitness of prebiotic molecules within innovation pools. Inspired by Rachel Whitaker from the University of Illinois



It has been suggested that life may have required a trillion interactions to get started, and that this required one half, to one billion, years to complete. However, a terrestrial hot spring field - via its average 100 thermo-chemically distinct pools, each exchanging materials and energy - would permit a trillion interactions in as little as 10 million years! This suggests that, perhaps, life on Earth could have started rapidly after the end of the Late Heavy Meteorite Bombardment at 3.85 Ga, as indicated by the recent discovery of 3.7 Ga stromatolites in Greenland15. By inference, life may have commenced on planetary bodies with a much shorter active geological history than Earth, such as Mars, thus significantly increasing the odds of finding signs of past life on our nearest neighbour. Indeed, a terrestrial hot spring origin makes Mars a prime target, as hot spring deposits have been found there by remote sensing and previous rover analysis16,17.


The Objectives for this Project are to:

1. Develop a systems-approach understanding of the oldest in habited hot spring setting on Earth - the 3.5 billion-year-old Dresser Formation - including controls on fluid flow, mechanisms that concentrate elements, causes for variations in element concentrations, and relationship of life signatures to available elements.
2. Obtain a detailed understanding of the chemistry and chemical energetics of active hot spring systems, focussing on the products and microbial diversity of zones of mixing between thermo-chemically distinct hot springs as a guide to better understanding the ancient Dresser system.
3. Conduct experimental research on prebiotic organic chemistry using actual materials from the Dresser Formation and fluid chemistries from modern hot springs, to determine whether complexity in prebiotic organic chemistry can be achieved by mixing components from thermo-chemically distinct hot springs.

4. Combine 1-3 above to produce a holistic model for a terrestrial origin of life setting.
5. Use the information to guide exploration for the search for life on Mars.


A glimpse of the past: the 3.5 Ga Dresser Formation

The ~3.5 billion-year-old (Ga) Dresser Formation in the Pilbara Craton, Western Australia, contains the oldest, most convincing, evidence of life on Earth in the form of fossil stromatolites, fractionated S and C isotopes, and putative microbial remains18-23. The formation is exceptionally well-preserved, exhibiting low strain and low-grade metamorphism (prehnite-pumpellyite to lower greenschist facies). The lower, fossiliferous, sedimentary unit is ~4-60 m thick and well-exposed for ~14 km along strike. It consists of grey-and-white layered chert with subordinate volcaniclastic sandstone, jasplitic chert, bedded carbonate, and diverse stromatolites20. Underlying, hydrothermally altered, komatiitic metabasalts are transected by a dense network of syn-depositional silica (microquartz)±barite± pyrite±organic matter-bearing hydrothermal veins that disperse into, but not through, the lower sedimentary unit24,25.

Originally, Dresser Formation stromatolites were interpreted to have been deposited in a quiet, shallow marine lagoon, similar to Shark Bay, Western Australia18. However, new findings have demonstrated a volcanic caldera environment affected by volcanic eruptions, faulting, and hydrothermal fluid circulation24-26. More importantly, recent discoveries by our group show that at least some of this ancient life flourished in the fresh water of a hot spring field on an exposed land surface27. This is based on the presence of thin (≤40 cm) units of stratiform geyserite, black-and-white, thinly laminated (2-30 µm-thick), siliceous rocks with alternating anatase (low-temperature polymorph of TiO2) and kaolinite+illite-rich layers (Fig. 2a). Geyserite is a siliceous deposit precipitated from hot (> 75-100 °C), silica-rich fluids around spring vents on exposed land surfaces28. The mineralogy is common in Recent to Jurassic geothermal fields28: kaolinite+illite derived from advanced argillic (steam-heated acid-sulfate) alteration (<120 °C) in high-sulfidation epithermal systems29, including in the Dresser Formation 30; anatase precipitation occurs in near neutral alkali-chloride thermal springs31. Units of siliceous sinter with terracettes and packed fragmental breccia typical of hot spring fields have also been found in the Dresser27, as have the mineralised remnants of the hot spring pools themselves in the form of ovoid (5-20 m diameter) masses of coarsely crystalline, hydrothermal barite (BaSO4) + pyrite (FeS2) that immediately underlying two of the geyserite localities27.


The newly discovered Dresser hot spring deposits are in close stratigraphic affinity with stromatolites and also contain a suite of newly identified biosignatures27. These include the unmistakable remnants of bubbles trapped between layers of geyserite and now filled by inward-radiating crystal splays of anatase and other hydrothermal minerals (Fig. 2b, c). These bubbles were trapped in what must have been microbial exopolymeric substance (EPS), identical to what is found on the mid-apron of active hot springs (Fig. 2d). Vertically aligned quartz crystals (230 µm-high) that wrap around the curved hinge of the convex ridges within the sinter terracettes are identical to recrystallised palisade fabric formed through silicification of microbial filaments on mid- to distal-apron hot spring terraces28. These textures are also similar to the internal structures of recently documented siliceous hot spring nodules from Chile that are macroscopically identical to opaline silica nodules found on Mars17. Beds with digitate, ferruginous microstromatolites also occur within the siliceous sinter (Fig. 2e).


                       
Figure 2: 3.5 Ga Dresser Formation hot spring deposits and biosignatures27. A) Geyserite, showing fine black (anatase)-and-white (kaolinite-illite) laminae (1 mm);  B) Circular bubble remnants in layers between geyserite, filled by hydrothermal barite (B) and quartz (Qz) (90µm). Red box = part C; C) Inward radiating anatase crystals (22µm); D) Oxygen bubbles in modern exopolymeric substance (EPS), New Zealand (2 mm). E) Microdigitate stromatolites in sinter (1 cm).



What makes the Dresser hot springs so important in terms of understanding the origin of life is the discovery that they concentrated many key elements of prebiotic chemistry, including B, Zn, P, S, C, O, and N (Fig. 3). 
For example, boron was discovered as multiple tourmaline crystals within a centimetre-thick crust of finely layered ferruginous rocks draped over rounded cobbles characteristic of river deposits. Although boron can be concentrated through evaporation of sea, or lake, water, δ11B results (avg. = -13.5‰) from Dresser tourmalines identified a non-marine, evaporative setting, identical to active boron-enriched hot springs from India14. Dresser hot springs also concentrated zinc (Zn, in hydrothermal veins) and manganese (Mn, in evaporative caldera lake deposits), important inorganic components in the cytoplasm from all three branches of life20. Phosphorous is concentrated in apatite in the hydrothermal veins33. Abundant H, as methane, and organic matter, are also present in the veins22,23, whereas C-bearing carbonates are widespread and abundant in Dresser footwall basalts, both as direct seawater precipitates and as hydrothermal alteration products. The ions K+ and Na2+ were concentrated in the system by hydrothermal alteration of basalt and captured in clays (paragonite, kaolinite, illite)25 that are important for organic molecule polymerisation. Clay synthesis was generated by late-stage steam-heated acid sulfate alteration, which occurs when the water table drops from waning hydrothermal activity29. Thus, could it be that Charles Darwin was right, that microbial life originated in “…some warm little pond…” as he proposed 145 years ago? Was it possible that life on Earth started on land and then adapted to the oceans12?


                                             
Figure 3: The key ingredients for life in an ancient hot spring13. Meteorites and hydrothermal fluids deliver simple organics and other elements (e.g., Au, PGEs) to the surface. Coeval volcanoes add S and other volatiles to the atmosphere. Hydrothermal fluids concentrate elements (e.g., Fe, Zn, B, P) through alteration. A/W, R/A, and W/R refer to Air/Water, Rock/Air and Water/Rock reactive interfaces.




Modern Hot Springs as a guide to interpreting past conditions

Ancient hot spring deposits are plagued by the effects of fluid alteration and metamorphism, such that the original chemistries of fluids that initially precipitated the deposits can be hard to identify. However, we can use modern hot springs as a guide to interpreting the Dresser Formation because of the characteristic facies of the modern examples. 
   Modern terrestrial hot spring deposits (sinters) develop as chemical precipitates from thermal waters that originate as mainly meteoric waters - in some cases supplanted with minor connate, magmatic or metamorphic components - which convectively circulate above and around magmatic intrusions34-36. Heated fluids may boil in the subsurface as they rise and depressurize, causing steam separation that results in surface discharges of hot springs and geysers (liquid-dominated) or fumaroles and steaming ground (steam-dominated)35,36. 

Hot water-rock interactions create chloride-rich, saline geothermal reservoirs (up to 400 °C) that are driven to the surface where they are expelled as near-neutral pH, alkali chloride solutions that precipitate relatively thick (decimetres to 10’s of metres) siliceous sinter35,37-39. The rising thermal fluids may mix with shallow groundwater to produce common acid-sulfate and/or bicarbonate springs35,36. In particular, oxidation of H2S in steam-heated groundwater may exit to the surface in the vapour phase, or condense in perched water tables, to form acid-sulfate springs and acid lakes that precipitate native sulfur and hydrothermal alteration minerals (e.g., kaolinite)35,40. Geothermal fluids are generally classified into chloride, sulfate, and bicarbonate waters by dominant anion36,39, although mixed anionic composition types are also known (e.g., acid-sulfate-chloride41). 

Typically, Modern springs precipitate opaline silica on biotic and abiotic surfaces to build up a broad sinter apron that displays various textures indicative of proximal vent to distal discharge-apron facies28,39 controlled by evaporative cooling in channels, pools and terraces (100°C to ~35°C)42,43. For example, geyserite is a type of sinter formed exclusively in and around the peripheries of vent-related (75-100°C) geyser and spouter mounds, formed by splashing and surging of hot, silica-rich water in the presence or absence of microbial activity28,44. Thick microbial mat textures are commonly preserved at lower temperatures away from the vent28,45
 
Importantly, modern hot spring fields are complex and may contain hundreds of pools, each with a slightly different chemistry (pH, Eh, temperature, amount and types of ions in solution, etc.), and with interactions between different fluid compositions46. In some locations, mixing of acid-sulfate and chloride waters will deposit thin siliceous sinters (few cm-thick) with distinctive textures and biotas47. Condensation of CO2 in groundwater around the peripheries of geothermal fields may generate neutral to alkaline bicarbonate springs with travertine mounds, cones, and terraces a few cm to 10’s of m thick37,48,49. In areas of low topographic relief, both acid and alkaline springs may form in close proximity and mix components37,44. Overall, the thickness and extent of sinter or travertine deposits are affected by volume and duration of fluid flow, fluid composition, tectonics, volcanism, host rock geology, and climate38,50-54
In complex fields, each pool becomes its own unique experiment in chemical and energetics terms49. Energetic complexity is rich in such fields, driven by three highly reactive interfaces (water-rock, water-air, and rock-air) and temperature gradients away from hot spring vents (Fig. 3).

Prebiotic organic chemistry

Many experimental tests of prebiotic chemistry have been conducted, starting with the famous Miller-Urey experiments in the 1950’s that created complex organic molecules from simple compounds using simulated lightning and inferred early Earth atmospheric conditions55,56. More recently, experiments using amino acids, nucleobases, phosphate, glycerol and a long chain fatty acid with 14 carbons were mixed directly into the centre of an acidic hot spring in Kamchatka11. Within seconds, this produced a white froth around the edges of the spring that later microscopic examination revealed was composed of vast numbers of tiny membranous compartments, each filled with compounds of the original organic soup (Fig. 4). This simple observation led to a new insight into the process by which life could have begun: if the vesicles and their contents dried out around the edges of the puddle, could polymers be synthesised and captured in the membranous vesicles? 

Further experiments under laboratory conditions mixed mononucleotides with lipids. When subject to wetting-drying cycles under the acidic conditions and high temperatures of the Kamchatka spring, this mixture produced polymers ranging from ten to over a hundred nucleotides in length57 that X-ray diffraction conclusively demonstrated were organised into structures that clearly had the potential to form short strands of nucleic acids. These reactions provide a compelling insight into how terrestrial hot springs can produce conditions important to prebiotic chemistry. 

Experimentation is now focused on what might happen when a prebiotic hydrothermal pool undergoes cycles of wetting and drying? Damer et al.12 suggest that tiny cargos of polymers encapsulated within lipid membranes would experience Darwinian selection because each drying cycle would cause lipid membranes of the vesicles to fuse, and entrapped polymers to become re-synthesized, more complex, and more concentrated. On re-wetting, the lipid membranes would re-encapsulate more concentrated - and longer chain - polymers, each of which would represent a new experimental configuration. The most robust systems of encapsulated polymers would survive and undergo further complexification.


                                              

Figure 4: Image of a lipid-mononucleotide mixture stained with a dye that strongly interacts with nucleic acids, after being put through four wet-dry cycles. The image shows that some (but not all) of the vesicles have captured the nucleic acids synthesized during the wet-dry cycles, forming protocells. The vesicles are in the size range of typical cells, around 10-20 µm in diameter. Photograph by David Deamer.