Buried Life
Steven D'Hondt, Professor
Graduate School of Oceanography
Steven D'Hondt earned a BS from Stanford University and a PhD from Princeton University. He has been at GSO since 1989. His primary research interest is the interaction between Earth and life.
In the middle of the nineteenth century, biologists
assumed that the deep sea was devoid of life. The crushing hydrostatic pressure
and chilly temperature of the deep sea were thought to be conditions intolerable
for living organisms. This assumption was refuted in 1860 by the discovery of
corals and sponges attached to a transatlantic cable that was hauled up from
the seafloor for repair. From 1868 to 1870, C. Wyville Thomson led multiple
cruises of HMS Lightning and HMS Porcupine to dredge the Atlantic
seafloor at depths as great as 2,500 fathoms (about 4,600 meters). By the end
of his project, he had discovered diverse life on much of the ocean floor. Since
then, marine biologists have come to accept the existence of life on the seafloor
and in the first few meters of deep-sea sediments. However, they continue to
be skeptical of claims that living organisms are buried deep within those sediments.
During the last decade, this perspective has
been challenged by the work of John Parkes and his colleagues at the University
of Bristol, England, who have reported bacteria buried 800 meters or more below
the seafloor. Their work has raised a number of provocative questions. Are these
bacteria denizens of the drilled sediment or contaminants from the drilling
fluid? If they're truly from the sediment, are they alive? Are they active?
Or are they ghost cells? If they're active, what sustains them? If they're not
active, can they be resuscitated?
The Ocean Drilling Program (ODP) is an international
partnership of scientists and research institutions that samples the deeply
buried sediments and rocky crust of the open ocean. On ODP Leg 185 (1999), GSO
microbiologist David Smith, newly appointed GSO geochemist Art Spivack (then
at the University of North Carolina), Oregon State University marine geologist
(and GSO alumnus) Martin Fisk, and their shipboard colleagues Göteborg University
microbiologist Shelley Haveman and Scripps Institution of Oceanography geochemist
Hubert Staudigel set out to determine if the bacteria reside in the sediments
or are introduced during drilling. They injected a distinctive perfluorocarbon
molecule continuously into the drilling fluid while drilling old sediments and
crust in the western Pacific. The synthetic perfluorocarbon molecule permeates
the sediment, is fairly easy to identify and measure in trace quantities, and
acts as a tracer for drilling contamination of deep-sea sediments. They also
injected bacterium-sized fluorescent beads while drilling representative cores.
Although the centers of recovered sediment cores were generally found to be
free of the perfluorocarbon and beads, they consistently contained bacterial
cells. These studies show that bacteria do truly exist hundreds of meters beneath
the seafloor.
The Leg 185 studies did not tell us whether these
deeply buried bacteria were alive and active or the ghostly relicts of a long-buried
seafloor. To address this, Smith and Spivack joined ODP Leg 190 (2000), where
they and their shipboard colleagues measured products of microbial activity
in deep-sea sediments of the Japan Sea. Their shipboard work required careful
microbiological and geochemical analyses of the buried cells and bulk sediments
of uncontaminated cores. Their analyses required a fully equipped shipboard
microbiology laboratory. Last year, Smith, three colleagues from other institutions,
and I wrote a National Science Foundation (NSF) proposal to construct a microbiology
laboratory aboard the JOIDES Resolution. Our colleagues were Andreas Teske,
lead investigator and microbiologist at Woods Hole Oceanographic Institution;
Richard Murray, a geochemist at Boston University; and Elizabeth Screaton, an
earth scientist at the University of Florida. Our proposal was funded and, as
a result, microbiologists from any country in the ODP consortium can now go
to sea equipped to study the deeply buried marine sedimentary biosphere.
Scott Rutherford (GSO alumnus and post-doctoral
researcher at GSO and the University of Virginia), Spivack, and I are tackling
the issue of buried microbial activity in a different way. Like larger animals,
many buried microbes break down organic molecules (food) and oxygen-bearing
molecules to get energy. Unlike larger animals, buried microbial communities
generally don't require free oxygen (O2) to break down
their food, but instead use various oxidized molecules, including nitrate (NO3-),
sulfate (SO42-),
and oxidized metals. Of these many molecules, sulfate is the most abundant in
the deep ocean and deep-sea sediments. In fact, it's nearly 50 times as abundant
as all other oxidants combined. Sulfate, nitrate, and free oxygen diffuse down
into deep-sea sediments from the overlying ocean. Consequently, the concentrations
of these chemicals in sediments result from the balance between diffusion from
above and reduction by microbes within the sediments. Because rates of diffusion
can be estimated from dissolved concentrations and a few other sedimentary properties
(such as sediment porosity), we can use concentrations of dissolved sulfate
in deep sea sediments to estimate the amount of microbial respiration that occurs
in deeply buried sediments. For nearly thirty years, geochemists have measured
the concentrations of dissolved sulfate (and sometimes nitrate and oxidized
metals) in Deep Sea Drilling Project and ODP drill holes throughout the world.
Rutherford, Spivack, and I are compiling this data to develop global maps of
microbial activity in deep-sea sediments. This will allow us to assess whether
deeply buried microbes are active or relict cells.
Our understanding of deeply buried life remains
incomplete and many of the questions that I raised at the beginning of this
article remain unanswered. Furthermore, there are other, deeper questions to
be addressed. What are the relationships between buried microbial activity and
the surface world? How do microorganisms adapt physiologically to burial under
extreme conditions? What is the biotechnology potential for these organisms?
Are there unknown and possibly ancient types of bacteria to be found? How do
deeply buried bacteria get around? Can rock-locked bacteria survive and evolve
in isolation for millions of years? And last, but not least, if bacteria survive
in deep oceanic sediments and in hot or cold oceanic crust, can similar life
forms also survive on other planets? Can we learn to recognize molecular and
chemical signatures of life in Earth's deeply buried sediments and crust? Will
we be able to distinguish the elusive evidence of life in nonterrestrial samples?
The deeply buried biosphere is likely to be one
of the next major research topics for the earth and life sciences. Recent advances
in molecular biology, geochemistry, and deep-sea drilling make the detailed
study of deeply buried life possible. However, much like Wyville Thomson's nineteenth-century
study of seafloor life, study of subseafloor life in the twenty-first century
will require an ambitious program of multiple drilling cruises spaced over several
years. Fortunately, the Ocean Drilling Program and the international ocean drilling
community are committed to advancing such study. It's going to be interesting.