Welcome to the deep biosphere

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Remember in Journey to the Center of the Earth when Hans, Lindenbrock and Axel discover giant insects, mastodons and other prehistoric creatures miles beneath the surface? While this was considered science fiction in the mid 19th century, I think most of us today would be more apt to call this story pure fantasy. We know now that such an idea is preposterous. Plants need sunlight to obtain their energy, and animals need plants for food. There is no energy source capable of sustaining complex, multicellular life far away from the sun. The biosphere as we know it can only exist on the surface, where ample sunlight and moderate temperatures prevail.

Single celled life is a bit more creative. Recent drilling expeditions beneath the surface of the continents and the ocean floor have revealed a surprisingly large number of bacteria and archaea living well beneath the surface of the earth- 3 x 10^29 cells according to current estimates!* The scientists behind these projects have coined the term “deep biosphere” to describe the areas of the earth beneath the surface that are still occupied by single-celled life. A great mystery surrounding the deep biosphere is how such communities can survive in environments that seemingly provide minimal energy. In short, how are these critters making a living?

So that we’re all on the same page here, I’ll just briefly review the three basic requirements for life as we know it on planet Earth:

1) A carbon source

2) An energy source

3) A pair of molecules that can donate and accept electrons.

More on the third one later, which relates to how organisms actually break down and harvest energy inside their cells. For now, let’s suffice it to say all life requires an energy source and a carbon source. For us, both of these requirements are satisfied by eating food. The metabolism of our food releases energy. As  we break down the complex organic molecules contained in our food, we are provided with simple carbon molecules which can be rebuilt into different molecules for growth and cellular repair. All animals use organic carbon as both an energy and a carbon source, because of the high energy yields associated with this strategy. By contrast, plants use light as an energy source and carbon dioxide from the atmosphere as a carbon source. Light energy is used to power a series of biochemical transformations, ultimately allowing plants to convert carbon dioxide into sugar: photosynthesis. Thus even in the world we are familiar with there exist two vastly different strategies for meeting life’s basic requirements.

Might the microbes of the deep biosphere choose one of these metabolic strategies? Clearly, the second one is dependent on light, which I probably don’t need to tell you is in rather short supply miles beneath the ocean floor. But what about organic carbon? Is enough organic carbon from, say, dead plant, animal and microbial bodies in the surface ocean or soils making its way into subsurface environments to sustain microbial communities?

At a first approximation, the answer is probably not. Best estimates are that < 1 % of the carbon fixed by plants on the planet’s surface is making it into the “buried organic carbon” pool- the stuff that might be available as food for deep biosphere organisms. Compared with the estimated size of the biomass inhabiting the subsurface, this flux of carbon provides, at best, enough energy to carry out only the most basic life support functions, certainly not enough for growth and reproduction.

What else could be feeding the deep biosphere? The answer is a bit complex, and something I will be exploring in much more detail throughout future posts. Many different options present themselves. Some microbes can use metals, such as iron, as an energy source, allowing them to convert carbon dioxide to sugar without light. This strategies is known as chemolithotrophy.

Dormancy might be another option for some inhabitants of the deep biosphere: in essence, forming a spore and entering a state of metabolic inertia until better conditions present themselves in the future. It is known that only certain groups of bacteria have this capability, but how widespread this strategy might be in the deep biosphere is uncertain. There is an argument to be made against dormancy in the deep biosphere; namely, that it is an evolutionary dead end. Dormancy might make sense in, for instance, a seasonal rainforest, where dry season conditions force microbes to go into hibernation but the onset of the wet season allows them to “wake up” and start growing again. But in a world that is always harsh, always lacking in energy, for thousands and millions of years, would a dormant cell ever wake up? Would it ever reproduce?

Finally, there may be sources of energy available to the deep biosphere that we simply do not understand yet. Perhaps there are microbes that can harvest energy released during the radioactive decay of elements in the earth’s crust? Or perhaps heat energy from even deeper inside the earth fuels the deep biosphere?

In short, there are many questions and many mysteries surrounding life in the deep biosphere. As scientists continue to answer these questions the answers will undoubtedly expand our understanding of what it means to be alive.

*Kallmeyer, J., Pockalny, R., Adhikari, R. R., Smith, D. C. & D’Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl Acad. Sci. USA 109, 16213–16216 (2012).

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