Scientists untangle interactions between the Earth's early life forms and the environment over 500 million years

The atmosphere, the ocean and life on Earth interacted over the past 500-plus million years in ways that improved conditions for early organisms to thrive. Now, an interdisciplinary team of scientists has produced a perspective article of this co-evolutionary history published in multidisciplinary open-access journal National Science Review.

"One of our tasks was to summarize the most important discoveries about carbon dioxide and oxygen in the atmosphere and ocean over the past 500 million years," says Syracuse University geochemistry professor Zunli Lu, lead author on the paper. "We reviewed how those physical changes affected the evolution of life in the ocean. But it's a two-way street. The evolution of life also impacted the chemical environment. It is not a trivial task to understand how to build a habitable Earth over long time scales"

The team from Syracuse University, Oxford University and Stanford University explored the intricate feedbacks among ancient life forms, including plants and animals, and the chemical environment in the current Phanerozoic Eon, which began approximately 540 million years ago.

At the start of the Phanerozoic, carbon dioxide levels in the atmosphere were high, and oxygen levels were low. Such a condition would be difficult for many modern organisms to thrive. But ocean algae changed that. They absorbed carbon dioxide from the atmosphere, locked it into organic matter and produced oxygen through photosynthesis.

The ability of animals to live in an ocean environment was affected by oxygen levels. Lu is studying where and when ocean oxygen levels may have risen or fallen during the Phanerozoic using geochemical proxies and model simulations. Co-author Jonathan Payne, professor of Earth and planetary sciences at Stanford University, compares an ancient animal's estimated metabolic requirements to places where it survived or disappeared in the fossil record.

As photosynthetic algae removed atmospheric carbon into sedimentary rocks to lower carbon dioxide and raise oxygen levels, the algae's enzymes became less efficient in fixing carbon. Therefore, algae had to figure out more complicated ways of doing photosynthesis at lower carbon dioxide and higher oxygen levels. It accomplished this by creating internal compartments for photosynthesis with control over the chemistry.

"For algae, it is changes in the environmental ratio of O2/CO2 that seems to be key to driving improved photosynthetic efficiency," says co-author Rosalind Rickaby, who is a professor of geology at Oxford. "What is really intriguing is that these improvements in photosynthetic efficiency may have expanded the chemical envelope of habitability for many forms of life."

Ancient photosynthesizers had to adapt to changes in the physical environment that they themselves had created, notes Lu. "The first part of the history of the Phanerozoic is increasing habitability for life, and then the second part is adaptation."

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A blueprint for life forms on Mars?

Microbes taken from surface sediment near Lost Hammer Spring, Canada, about 900 km south of the North Pole, could provide a blueprint for the kind of life forms that may once have existed, or may still exist, on Mars.

The extremely salty, very cold, and almost oxygen-free environment under the permafrost of Lost Hammer Spring in Canada's High Arctic is the one that most closely resembles certain areas on Mars. So, if you want to learn more about the kinds of life forms that could once have existed -- or may still exist -- on Mars, this is a good place to look. After much searching under extremely difficult conditions, McGill University researchers have found microbes that have never been identified before. Moreover, by using state-of-the-art genomic techniques, they have gained insight into their metabolisms. In a recent paper in ISME, the scientists demonstrate, for the first time, that microbial communities found living in Canada's High Arctic, in conditions analogous to those on Mars, can survive by eating and breathing simple inorganic compounds of a kind that have been detected on Mars (such as methane, sulfide, sulfate, carbon monoxide, and carbon dioxide). This discovery is so compelling that samples of the Lost Hammer surface sediments were selected by the European Space Agency to test the life detection capabilities of the instruments they plan to use on the next ExoMars Mission.

Developing a blueprint for life on Mars

Lost Hammer Spring, in Nunavut in Canada's High Arctic, is one of the coldest and saltiest terrestrial springs discovered to date. The water which travels up through 600 metres of permafrost to the surface is extremely salty (~24% salinity), perennially at sub-zero temperatures (~ -- 5 °C) and contains almost no oxygen (<1ppm dissolved oxygen). The very high salt concentrations keep the Lost Hammer spring from freezing, thus maintaining a liquid water habitat even at sub-zero temperatures. These conditions are analogous to those found in certain areas on Mars, where widespread salt deposits and possible cold salt springs have been observed. And while earlier studies have found evidence of microbes in this kind of Mars-like environment -- this is one of a very few studies to find microbes alive and active

To gain insight into the kind of life forms that could exist on Mars, a McGill University research team, led by Lyle Whyte of the Department of Natural Resource Sciences, has used state-of-the-art genomic tools and single cell microbiology methods to identify and characterize a novel, and more importantly, an active microbial community in this unique spring. Finding the microbes and then sequencing their DNA and mRNA was no easy task.

It takes an unusual life form to survive in difficult conditions

"It took a couple of years of working with the sediment before we were able to successfully detect active microbial communities," explains Elisse Magnuson, a PhD student in Whyte's lab, and the first author on the paper. "The saltiness of the environment interferes with both the extraction and the sequencing of the microbes, so when we were able to find evidence of active microbial communities, it was a very satisfying experience."

The team isolated and sequenced DNA from the spring community, allowing them to reconstruct genomes from approximately 110 microorganisms, most of which have never been seen before. These genomes have allowed the team to determine how such creatures survive and thrive in this unique extreme environment, acted as blueprints for potential life forms in similar environments. Through mRNA sequencing, the team were able to identify active genes in the genomes and essentially identify some very unusual microbes actively metabolizing in the extreme spring environment.

No need for organic material to support life

"The microbes we found and described at Lost Hammer Spring are surprising, because, unlike other microorganisms, they don't depend on organic material or oxygen to live," adds Whyte. "Instead, they survive by eating and breathing simple inorganic compounds such as methane, sulfides, sulfate, carbon monoxide and carbon dioxide, all of which are found on Mars. They can also fix carbon dioxide and nitrogen gasses from the atmosphere, all of which makes them highly adapted to both surviving and thriving in very extreme environments on Earth and beyond."

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Living in an anoxic world: Microbes using arsenic are a link to early life

 Much of life on planet Earth today relies on oxygen to exist, but before oxygen was present on our blue planet, lifeforms likely used arsenic instead. These findings are detailed in research published today in Communications Earth and Environment.

A key component of the oxygen cycle is where plants and some types of bacteria essentially take sunlight, water and CO2 and convert them to carbohydrates and oxygen which are then cycled and used by other organisms that breathe oxygen. This oxygen serves as a vehicle for electrons, gaining and donating electrons as it powers through the metabolic processes. However, for half of the time life has existed on Earth, there was no oxygen present and for the first 1.5 billion years we really do not know how these systems worked, says lead author of the study and UConn Professor of Marine Sciences and Geosciences Pieter Visscher.

Light-driven, photosynthetic organisms appear in the fossil record as layered carbonate rocks called stromatolites dating to around 3.7 billion years ago, says Visscher. Stromatolite mats are deposited over the eons by microbial ecosystems, with each layer holding clues about life at that time. There are contemporary examples of microbes that photosynthesize in the absence of oxygen using a variety of elements to complete the process, however it is not clear how this happened in the earliest life forms.

Theories as to how life's processes functioned in the absence of oxygen have mostly relied on hydrogen, sulfur, or iron as the elements that ferried electrons around to fulfill the metabolic needs of organisms.

Visscher explains these theories are contested, for example photosynthesis is possible with iron but researchers do not find evidence of that in the fossil record before oxygen appeared some 2.4 billion years ago. Hydrogen is mentioned yet the energetics and competition for hydrogen between different microbes shows it is highly unfeasible.

Arsenic is another theoretical possibility, and evidence for that was found in 2008. Visscher says the link with arsenic was strengthened in 2014 when he and colleagues found evidence of arsenic-based photosynthesis in deep time. To further support their theory, the researchers needed to find a modern analog to study the biogeochemistry and element cycling.

Finding an analog to the conditions on early Earth is a challenge for a number of reasons, besides the fact that oxygen is abundant on modern earth. For instance, the evidence shows early microbes captured atmospheric carbon and produced organic matter at a time when volcanic eruptions were frequent, UV light was intense in the absence of the ozone layer, and oceans were essentially a toxic soup.

Another challenging aspect of working within the fossil record, especially those as ancient as some stromatolites, is that there are few left due to the cycling of rock as continents move and time marches on. However, a breakthrough happened when the team discovered an active microbial mat, currently existing in the harsh conditions in Laguna La Brava in the Atacama Desert in Chile.

The mats have not been studied previously but present an otherworldly set of conditions, like those of early Earth. The mats are in a unique environment which leaves them in a permanent oxygen-free state at high altitude where they are exposed to wild, daily temperature swings, and high UV conditions. The mats serve as powerful and informative tools for truly understanding life in the conditions of early Earth.

Visscher explains, "We started working in Chile, where I found a blood red river. The red sediments are made up by anoxogenic photosynthetic bacteria. The water is very high in arsenic as well. The water that flows over the mats contains hydrogen sulfide that is volcanic in origin and it flows very rapidly over these mats. There is absolutely no oxygen."

The team also showed that the mats were making carbonate deposits and creating a new generation of stromatolites. The carbonate materials also showed evidence for arsenic cycling -- that arsenic is serving as a vehicle for electrons -- proving that the microbes are actively metabolizing arsenic much like oxygen in modern systems. Visscher says that these findings, along with the fossil evidence gives a strong indication of what was seen on early earth.

"Arsenic-based life has been a question in terms of does it have biological role or is it just a toxic compound?" says Visscher. That question appears to be answered, "I have been working with microbial mats for about 35 years or so. This is the only system on Earth where I could find a microbial mat that worked absolutely in the absence of oxygen."

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Tracking records of the oldest life forms on Earth

Rocks with banded iron formations and biosignatures - 1,900 million years old, Michigan, US (top left), 2,700 million years old, Ontario, Canada (bottom left) and 2,500 million years old, Karijini National Park, Western Australia (right).

The discovery provides a new characteristic 'biosignature' to track the remains of ancient life preserved in rocks which are significantly altered over billions of years and could help identify life elsewhere in the Solar System.

The research, published in two papers -- one in the Journal of the Geological Society and another in Earth and Planetary Science Letters -- solves the longstanding problem of how scientists can track records of life on Earth in highly metamorphosed rocks more than 3,700 million years old, with organic material often turning into the carbon-based mineral graphite.

In the first study, published in Earth and Planetary Science Letters, the team analysed ten rock samples of banded iron formations (BIF) from Canada, India, China, Finland, USA and Greenland spanning over 2,000 million years of history.

They argue that carbon preserved in graphite-like crystals -'graphitic carbon'- located alongside minerals such as apatite, which our teeth and bones are made of, and carbonate, are the biosignatures of the oldest life forms on Earth.

"Life on Earth is all carbon-based and over time, it decomposes into different substances, such as carbonate, apatite and oil. These become trapped in layers of sedimentary rock and eventually the oil becomes graphite during subsequent metamorphism in the crust," explained Dr Dominic Papineau (UCL Earth Sciences, Center for Planetary Sciences and the London Centre for Nanotechnology).

"Our discovery is important as it is hotly debated whether the association of graphite with apatite is indicative of a biological origin of the carbon found in ancient rocks. We now have multiple strands of evidence that these mineral associations are biological in banded iron formations. This has huge implications for how we determine the origin of carbon in samples of extra-terrestrial rocks returned from elsewhere in the Solar System."

The team investigated the composition of BIF rocks as they are almost always of Precambrian age (4,600 million years old to 541 million years old) and record information about the oldest environments on Earth.

For this, they analysed the composition of rocks ranging from 1,800 million years old to more than 3,800 million years old using a range of methods involving photons, electrons, and ions to characterise the composition of graphite and other minerals of potential biogenic origin.

"Previously, it was assumed that finding apatite and graphite together in ancient rocks was a rare occurrence but this study shows that it is commonplace in BIF across a range of rock metamorphic grades," said team member Dr Matthew Dodd (UCL Earth Sciences and the London Centre for Nanotechnology).

The apatite and graphite minerals are thought to have two possible origins: mineralised products of decayed biological organic matter, which includes the breakdown of molecules in oil at high temperatures, or formation through non-biological reactions which are relevant to the chemistry of how life arose from non-living matter.

By showing evidence for the widespread occurrence of graphitic carbon in apatite and carbonate in BIF along with its carbon-isotope composition, the researchers conclude that the minerals are most consistent with a biological origin from the remains of Earth's oldest life forms.

To investigate the extent to which high-temperature metamorphism causes a loss in molecular, elemental and isotope signatures from biological matter in rocks, they analysed the same minerals from a 1,850 million year old BIF rock in Michigan which had metamorphosed in 550 degree Celsius heat.

In this second study, published today in Journal of the Geological Society, the team show that several biosignatures are found in the graphitic carbon and the associated apatite, carbonate and clays.

They used a variety of high-tech instruments to detect traces of key molecules, elements, and carbon isotopes of graphite and combined this with several microscopy techniques to study tiny objects trapped in rocks which are invisible to the naked eye.

Together, all of their observations of the composition are consistent with an origin from decayed biomass, such as that of ancient animal fossils in museums, but which has been strongly altered by high temperatures.

"Our new data provide additional lines of evidence that graphite associated with apatite in BIF is most likely biological in origin. Moreover, by taking a range of observations from throughout the geological record, we resolve a long-standing controversy regarding the origin of isotopically light graphitic carbon with apatite in the oldest BIF," said Dr Papineau.

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