Clues to Life in the Mines of Murgul

pyrite
Pyrite, a form of iron sulfide (FeS2) also known as "Fool’s Gold."
Image Credit: University of Wisconsin-Madison, Dept. of Geology and Geophysics

The Mine of Murgul sounds like an ominous place in "The Lord of the Rings," a dark cavern filled with menacing orcs and trolls. But, in fact, this copper mine in Turkey may help shed light on life’s origin.

The mine contains pyrite, a form of iron sulfide (FeS2) also known as "Fool’s Gold." This iron sulfide mineral may have acted as a template for the early chemical reactions that led to amino acids, proteins, and other building blocks of life.

Pyrite has been the focus of theories regarding the origin of life since 1988, when a German patent lawyer named Gunter Wächtershäuser suggested that pyrite may have acted as a catalyst for the chemistry of living cells. In Wächtershäuser’s scenario, chemical reactions occurred on positively charged pyrite located at hydrothermal vents. These chemical reactions eventually led to the generation of oily compounds called lipids. The lipids formed a bubble around the prebiotic system, and this bubble "cell" then drifted free of the surface on which it was generated.

Although the right combination of chemicals and energy for life’s origin could have been present at hydrothermal vents, skeptics say that such a hot environment would have endangered the formation of delicate proteins and RNA strands.

Another possible birthplace may be at the interface between land and sea. Charles Darwin thought that life could have originated "in some warm little pond, with all sorts of ammonia and phosphoric salts, light, heat, electricity, etc. present." John Desmond Bernal expanded on this idea, suggesting that life could have begun in tidal regions, where molecules faced alternating wet and dry periods. The wet period would dissolve chemicals and allow them to react with each other, while the dry periods would allow the chemicals to condense, spurring further reactions.

hydrothermal_vent
Although the right combination of chemicals and energy for life’s origin could have been present at hydrothermal vents, skeptics say that such a hot environment would have endangered the formation of delicate proteins and RNA strands.
Image Credit: University of Victoria, Canada

Yet the danger of ultraviolet (UV) radiation from the sun prompted others to suggest that an ever-present layer of water would be necessary for protection. Matthew Edwards of the University of Toronto thinks shallow ocean waters were more likely sites for life’s origin than evaporative pools. His model for the origin of life requires ocean waters at least a few meters deep.

"Wetting-drying is important in prebiotic ‘soup’ models, since it is hard to get dissolved charged molecules like amino acids to combine otherwise," says Edwards. "In my model, amino acids are formed in situ in a developing metabolic complex. The basic ingredients are just simple substrates like carbon dioxide or carbon monoxide."

Carbon dioxide and carbon monoxide were major components of the Earth’s atmosphere before the rise of oxygen-producing photosynthesis. In Edward’s model, these ingredients, along with energy from the sun, induced prebiotic chemical reactions on submerged pyrite.

When pyrite absorbs sunlight, a weak electrical current is generated. In the Earth’s early anoxic environment, this effect would have been further enhanced. This photoelectric quality could have led to carbon and nitrogen fixation. A primitive metabolism would then have developed around these fixation sites. Edwards says this process would have been very fast, occurring in a few weeks or less.

The inspiration for his model came from Helmut Tributsch and colleagues at the Hahn-Meitner Institüt in Berlin, who were looking at pyrite for solar cell research. After Edwards told them about the evolutionary aspect of their work, they tested natural pyrite samples from 13 different ore sites.

Not all pyrite is created equal, and the chemical properties and crystal structures of the mineral determine how well the pyrite reacts to light. Pyrite samples from the Murgul mine in Turkey showed the best evidence of photocurrent voltage, perhaps indicating the type of pyrite most likely to play a role in life’s origin.

cysteine
Helmut Tributsch and colleagues determined that the amino acid cysteine (above) would have played a vital role in life’s origin, because cysteine is able to provide the chemical energy of pyrite in a form that can be utilized by primitive organisms.
Image Credit: Molecular Expressions, National High Magnetic Field Laboratory

The Tributsch study also determined that the amino acid cysteine would have played a vital role in life’s origin, because cysteine is able to provide the chemical energy of pyrite in a form that can be utilized by primitive organisms. Acidithiobacillus ferrooxidan, for instance, uses cysteine to dissolve pyrite in order to acquire iron and sulfur.

"This chemical energy may have already been relevant during the early stage of biological evolution," they write.

In addition to Acidithiobacillus, other microorganisms have evolved to extract chemical energy from pyrite. Leptospirillum ferrooxidans, for instance, induces electrochemical corrosion on pyrite to recover iron. Although these organisms do not use light-driven reactions, the use of pyrite in such primitive metabolisms may indicate a relationship that stretches far back in time.

These bacteria use pyrite in a process called chemosynthesis – or the production of food from chemicals. The earliest forms of life are thought to have been chemosynthetic. But the development of photosynthesis – the production of food from sunlight – was not far behind, and even may have emerged at the same time as chemosynthesis.

By receiving energy from the Sun, pyrite could have set the stage for the origin of photosynthesis. It is perhaps no coincidence that many of the enzymes in modern photosynthetic organisms are metal proteins with iron-sulfur clusters.

Tracking Down Photosynthesis

purple_bacteria
Purple bacteria use energy from the sun but extract electrons from substances other than water, and therefore release no oxygen. Most species are strict anaerobes and live in the sediment of ponds and lakes.
Credit: Digital Films For Cells

A modern-day photosynthetic cell harnesses light energy by using two kinds of proteins. Photosystem I protein molecules use sunlight to convert carbon dioxide into carbon and oxygen, producing food in the form of carbohydrates. Photosystem II protein molecules use light to split water into hydrogen and oxygen for plant respiration.

Some early organisms used Photosystem I, while others used Photosystem II. The earliest, non-oxygen producing photosynthetic organism is thought to be purple bacteria, which relies on Photosystem I for energy. Studies suggest that modern photosynthesis developed as a result of gene transfer, where genes are swapped between different organisms. This allowed the Photosystems to come together, creating the oxygen-producing photosynthesis we are familiar with today.

The Photosystem proteins developed at least 2.7 billion years ago, and possibly even earlier. A recent study by Danish researchers Minik Rosing and Robert Frei suggests oxygen-producing photosynthesis – which needs both Photosystems in order to work – already could have been in place as early as 3.7 billion years ago. Life is thought to have originated 3.8 billion years ago, soon after the Earth stopped being bombarded by the many meteorites that still cluttered the early solar system.

Photosynthesis could have developed at hydrothermal vents, but it only would have been able to work at the low infrared light levels generated from the vent heat. Green sulfur bacteria living off infrared light have been found living at the vents, but it is possible that rather than originating there, these bacteria migrated downwards from the ocean surface and adapted to the infrared light conditions. It seems most likely that photosynthesis developed in a region that had regular access to the sun’s light.

Shining a Light on Life

isua_rocks
Scientists Minik Rosing and Robert Frei claim to have found the oldest evidence of photosynthesis – the most important chemical reaction on Earth – in 3.7-billion-year-old seafloor sediments in Isua, Greenland.
Credit: BBC News

The early Earth did not have an ozone layer, so UV radiation from the sun would have been 100 times today’s levels. While the delicate molecules of life’s beginning would have deteriorated under this light intensity, Edwards’s model avoids this problem because his pyrite is submerged, with water acting as a protective barrier against UV.

But even if the molecules on the pyrite were periodically exposed to UV, Tributsch says it still may not have been a problem. Molecules within 10 nanometers from the surface of pyrite are protected against UV radiation (10 nanometers is about five times the dimension of a typical organic molecule).

When a molecule absorbs UV radiation, electrons become excited for a short time. The extra energy of the excited electrons can damage the molecule. But if the excitation happens within approximately 10 nanometers of a material like pyrite, the pyrite will absorb the extra energy and release it as heat. This diffuses the energy and averts any potential damage.

Tributsch suggests that chlorophyll, the light-sensitive pigment that drives modern photosynthesis, may have originated within this 10-nanometer protected region on pyrite. The chlorophyll would have become photochemically active when pushed outside this region. By remaining in contact with the still-protected organic layer, chlorophyll could have started to provide energy to primitive cells.

But could this process have happened in a tidal region? In Edwards’ model, there would appear to be nothing to stop waves from washing away chemicals reacting on the submerged pyrite, and diffusing them out into the open ocean.

gandalf
Lord of the Rings Gandalf the Great in Moria.
Credit: TheOneRing.net

Yet Edwards says that the molecules were at first anchored directly to the mineral surface, and a "boundary layer" would have protected the molecules bound to the pyrite. "In any situation where a liquid or gas flows by a solid body, the speed of the flow falls off progressively the closer you get to the body," he says. The boundary layer is the space where the speed of flow drops to zero.

"In the origins of life situation, the point is that even under quite wavy conditions, the boundary layer would have protected the developing biomolecules from being washed away," says Edwards.

If lipids were generated, these also would have prevented the molecules from washing away. "Hydrophobic molecules would have preferentially adhered to the mineral surface rather than diffused away," says Edwards. "Think of how hard it is to clean up submerged rocks after an oil spill."

Tributsch adds that when modern bacteria interact with metal sulfides, slimy organic biofilms cover the sulfide surface. He says these films, which are not easily dissolved by water, form through molecular interactions between organic molecules. Chemicals bound within these films diffuse very slowly into water, yet inorganic nutrients such as phosphate can penetrate the films.

"Such an organic film may be imagined as a reaction phase, confining chemicals and supporting organic evolution on pyrite," says Tributsch.

While many scientists favor hydrothermal vents as the location for life’s origin, the work of Tributsch and Edwards suggests life also could have originated closer to the ocean’s surface. Could the clues found in the Mines of Murgul point to a final answer? Perhaps only Gandalf would know for sure.