Insights into the Marine Deep Biosphere: Evolution and Survival

 

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Theme 4: Evolution and SurvivalCdebi

The Center for Dark Energy Biosphere Investigations (C-DEBI) is a multi-year research initiative sponsored by the National Science Foundation. This initiative and the projects it encompasses span many institutions and have four intertwining themes. Here, we present material on the fourth of these themes, Evolution and Survival. First, however, what is the center all about?

The world we live in is dominated by microbial life. You can’t see them, but microorganisms are all around us. Everything living thing depends on them in one fashion or another. Many natural processes that we take for granted, such as plants growing from sunlight, and the decomposition of waste, result from microbial activity. Microbes provide essential nutrients, vitamins and other essential molecules for human and animal diets. They even regulate oxygen and carbon dioxide in the air. Microbial organisms both produce and consume huge amounts of greenhouse gases like carbon dioxide and methane. On a global scale, even “small” shifts in microbial activity can change Earth’s entire climate.

Although microbial processes are essential to life on Earth, scientists don’t know some of the most basic biological details about many of these organisms: who, what, and where are they?

In this world of unanswered questions about microbes, an enormous new habitat has recently come to light as scientists’ explore the distant reaches of Earth–the deep biosphere. As it turns out, there are vast numbers of microbes living below the surface of the land, below the seafloor, and into the very crust of the Earth itself.

What new forms of life live there? How do they survive so far from light and under such extreme pressures and temperatures? Will their discovery change the way we look for life elsewhere? What useful species and biological, chemical, and physical processes might we find there, such as new ways to make energy, store carbon, or treat wastewater? C-DEBI addresses these questions and more.

 

The discovery of life in the deep biosphere has raised a conundrum for scientists: how in the world can anything persist buried far below the surface of the Earth for thousands, and even millions, of years? What adaptations allow organisms to flourish in this ecosystem poised at the edge of starvation and extinction? This is the topic of C-DEBI theme 4, Evolution and Survival: Adaptation, Enrichment, and Repair

At first, the presence of microorganisms far below the active seafloor was not too surprising. Just as seeds and nuts can be buried on land for millennia[i], it was originally thought that the buried microbes were merely detritus – the not-yet decayed leftovers of ancient communities. If this “leftover” assumption were true, analysis of their genes could shed light on evolution (how are the “ancient” organisms related to modern ones?) and adaptation (were certain genes more or less common when the climate was cooler, or when carbon dioxide levels were different from today?).

Equally interesting is the possibility of testing deep biosphere samples to see if any of the lingering microbes could still grow. Experiments like this help us understand how individuals and ecosystems could recover from enormous changes on the surface, such as ice ages or meteor impacts. Several times people have found woolly mammoths frozen in ice and buried for thousands of years, such as “Yuka”[ii], but no one expects them to start walking again. Seeds and spores, however, are different–as exhibited by the claim of 30,000-year-old flower seeds sprouting in a Russian laboratory[iii]. While permafrost, such as the home of the flower seeds, can be tens of thousands years old, the sediment record found at the bottom of the world’s oceans can span millions of years, potentially allowing scientists to test ideas about evolution and adaptation on a massive time scale.

In some locations in the ocean, such as coastal environments, material settles at a very high rate, piling up on the sea floor. Microbes are buried quickly in these locations. As a result, the organisms that took this express elevator down through the water column and now reside at fairly shallow depths below the sea floor–say, ten meters–can be quite young. In contrast, at a slow accumulation site like the middle of the Pacific Ocean, the material found ten meters down is very, very old. This raises two fascinating questions. Are the DNA sequences one finds in the old sediment different from those of the young sediment just because they are from different epochs in Earth history? Or have the microbes in the old, slowly deposited locations been surviving, growing, adapting, and evolving in their deep habitats?

In the laboratory, scientists have observed the evolution of a single common bacterium, E. coli, over the course of a long-term, 21-year experiment[iv]. Unfortunately for many researchers, multi-decadal experiments are not always practical. The good news for deep biosphere scientists is that a single suite of sediment samples collected on a single drilling expedition can provide DNA sequences that track entire communities over millions of years[v].

The jury is still out on the use of old sediments as unchanging scientific time machines because we are beginning to understand that even the oldest sediments harbor active life[vi]. In other words, if you examine a 15 million-year old chunk of ocean sediment, it isn’t only laden with 15 million-year old microbes; in the many millennia since that material first settled on the seafloor, some fraction of those microbes have stayed active, metabolizing microbial food in whatever form they prefer. Active cells here would represent a world less like an “Island Lost In Time” and more like Australia–isolated, but not static, with organisms changing and evolving into their own unique forms and states. Moreover, scientists also find microbial life, sometimes lots of it[vii], inhabiting the ocean crust itself. This isn’t detritus that settled out of the water, but raw rock freshly created from cooling lava on the bottom of the ocean, colonized by bacteria and archaea, and then buried below a blanket of sediment for millions of years. These cells are now thought to grow and multiply throughout ocean rock, but how microbes can spread through hard rock and how populations can flow in and out of the ocean crust remains a mystery. These very questions were the subject of a recent dedicated deep sea drilling expedition in the Atlantic Ocean[viii] as well as many upcoming and proposed cruises.

This long ignored concept of an active, dynamic microbial population in ocean sediment and crust is an exciting and active area of ongoing deep biosphere research. This includes many new results from C-DEBI researchers that are currently under review. In a study involving painstaking efforts to analyze sediment RNA, a macromolecule found only in living and active organisms (as opposed to DNA, which can be found in living, dormant, and dead organisms[ix]), Dr. Brandi Kiel Reese at the University of Southern California identified the fraction of deep biosphere community that is active.[x] Here “active” does not mean fast, however; in fact we are discussing some of the slowest life on Earth[xi].

How they survive and persist in such a dark, cold, and often inert environment, and what adaptations they accumulate to do so, is almost completely unknown. For example, we know that over thousands of years proteins and DNA spontaneously fragment and undergo chemical changes. For multicellular organisms (like you and I) that grow new cells and shed old ones by the second, the experiences of a single cell over a thousand year time frame may seem of little consequence. But in the deep biosphere, where biomass turnover is on the order of millennia[xii], the absence or occurrence of DNA mutations may be the deciding factor in whether or not an organism’s genes are available to pass on to the next generation[xiii].

For this and other reasons, the organisms that appear most successful in young sediment may, in the long run, be the biggest losers. Meanwhile, the slowest microbes–molecular handymen, capable of keeping the old clunker going–just keep truckin’ on. How they accomplish that is of interest to us all.

 

For more information:

C-DEBI website

This backgrounder was written by John Kirkpatrick, a post-doctoral fellow at the University of Rhode Island Graduate School of Oceanography, as part of the education and outreach efforts for C-DEBI.


[ix] Such as that of King Richard III.

[xi] Consider a lollipop, about 10 g of sugar. If you put that in a beaker with 1 liter of E. coli, they could metabolize that in about (very roughly) an hour. If you added it to 1 liter of deep sediment, at their in situ metabolic rate that lollipop could last 12 billion years – almost the age of the universe! Of course, lollipops are not often seen deep below the seafloor. (This calculation uses metabolic rates given in Wang, G., Spivack, A. J., Rutherford, S., Manor, U., & D’Hondt, S. (2008). Quantification of co-occurring reaction rates in deep subseafloor sediments. Geochimica et Cosmochimica Acta, 72(14), 3479–3488. doi:10.1016/j.gca.2008.04.024)