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| Enlarge ImageIn 1991, scientists aboard the submersible Alvin witnessed the aftermath of a very recent volcanic seafloor eruption and found themselves in a virtual blizzard of white debris.
( Photo by Rachel Haymon (UCSB) and Dan Fornari, (WHOI), first published in Haymon et al., 1993 (EPSL). WHOI National Deep Submergence Facility, Alvin Operations Group. Research supported by the National Science Foundation) |
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| Enlarge ImageExamining the white flocs discharged from the 1991 seafloor eruption, WHOI scientists discovered a new genus of bacteria called Arcobacter. (Photo courtesy of Craig Taylor & Carl Wirsen, WHOI) |
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| Enlarge ImageA titanium ring deployed at a Pacific hydrothermal vent site indicates the presence of bacteria thriving beneath the seafloor. Within days, Arcobacter bacteria, discharging from the subsurface, rapidly colonize the ring, producing a white sulfur filament mat up to 3 centimeters thick as they grow. (Craig Taylor and Carl Wirsen, WHOI and Françoise Gaill, Université Pierre et Marie Curie, Paris, France) |
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| Enlarge ImageWorld’s largest bacterium—In 1999 scientists discovered a previously unknown bacterium, which is large enough to be seen with the naked eye. Found off the coast of Namibia, the bacteria grow in long lines of single cells, each stuffed with reflective white globules of sulfur. The bacteria resembled a string of pearls to its discoverers, who named it Thiomargarita namibienus (“Sulfur pearl of Namibia”). The bacteria have evolved to live on seafloor sediments, where they find hydrogen sulfide for energy and nitrate for respiration. Their size is due to a large vacuole that fills the interior of their cells like inflated balloons. The vacuole stores nitrate, giving Thiomargarita the ability to survive periods when oxygen is lacking—a built-in equivalent of an oxygen-storing SCUBA tank that allows humans to remain alive underwater. (Photo courtesy of Ferran Garcia-Pichel, Arizona State University.) |
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Carl Wirsen, Oceanographer Emeritus
Biology Department
Woods Hole Oceanographic Institution In 1991, scientists aboard the submersible Alvin were in the
right spot at the right time to witness something extraordinary. They
had sailed into the aftermath of a very recent volcanic eruption on the
seafloor and found themselves in a virtual blizzard.
They
were densely surrounded by flocs of white debris, composed of sulfur
and microbes, which drifted more than 30 meters above the ocean bottom.
The seafloor was coated with a 10-centimeter-thick layer of the same
white material.
This vast volume of microbes did not come from the ocean. The eruption had flushed it out from beneath the seafloor.
The discovery was transforming. It strongly suggested that previously
unimagined and potentially huge communities of microbial life were
thriving in the dark, increasingly hot, oxygen-depleted rocky cracks
and crannies below the ocean bottom. An abundance of life apparently
flourished in conditions we had considered too extreme. It shattered
our narrow preconceptions and stretched our view of the places and
circumstances that can harbor life.
‘Everything is everywhere’
With our horizons expanded, we have launched new initiatives in the
past decade to search for life deep within the earth—to explore the
so-called subsurface biosphere. In recent years, scientists have
discovered many new subsurface biosphere habitats—reaffirming the
principle of the pioneering microbiologist Martinus Willem Beijerinck
(1851-1931), who said, “Everything is everywhere, the environment
selects.” Beijerinck’s approach—to study “the relation between
environmental conditions and the special forms of life corresponding to
them” —certainly applies to the subsurface realm, where biology and
microbiology interact with geology and hydrology.
What
organisms inhabit this deep biosphere? How deep are they living? How
long can they survive under these conditions? How have they adapted to
take advantage of energy supplied by the planet, rather than by the
sun?
What impact, in turn, does this biosphere have on the
oceans and the planet? What can these hardy, entrepreneurial organisms
teach us about the origin and evolution of life on Earth? How can they
guide our search for possible life on other planetary bodies?
We are at the frontiers of answering these questions.
Better living through chemistry
The amazing discovery of life at seafloor hydrothermal vents in 1977
reminded us that solar energy, oxygen, organic matter, and
photosynthesis are not the only fundamental building blocks and
chemical processes that foster life.
In place of energy from
the sun, certain organisms use chemosynthetic reactions to live and
grow. They use inorganic chemicals, such as hydrogen and hydrogen
sulfide, rather than organic matter for their energy and carbon dioxide
as their source of carbon. Geothermal, rather than solar, energy
catalyzes chemical reactions that generate these life-sustaining
chemicals from rocks and seawater. Water is the only absolutely
essential ingredient.
But below the seafloor and deeper into
the subsurface, it was reasonable to assume that conditions would
become more extreme and life would become sparser or nonexistent. Yet
in the past decade we have found an extraordinary diversity of
subsurface microbes living in a wide range of conditions—buried deep
within ocean sediments, in hot ocean crust crevices, in frozen polar
soils, and in the subterranean bowels of deep mines.
In all
these places, individual species have adapted to extreme conditions
that include high pressure, high and low temperatures, unusual or toxic
chemicals and minerals, or low availability of essential nutrients.
Often they take advantage of specific extreme conditions to carve out a
niche where they can thrive and other species cannot.
Life finds a way—often cleverly
Take, for example, the mats of white microbial sulfur debris witnessed by scientists aboard Alvin
in 1991. WHOI scientist Craig Taylor, Stefan Sievert, and I
subsequently found that such mats are produced by a genus of bacteria
called Arcobacter. It lives in low-oxygen conditions and
metabolizes hydrogen sulfide (H2S) to obtain energy. An end-product of
this metabolism is a unique form of sulfur, which the bacteria
ingeniously excrete in the form of solid, white filaments.
Together, large populations of these bacteria produce crosshatched mats
of these filaments. In the face of flowing subsurface hydrothermal
fluids, these mats help keep the bacteria anchored to rocky surfaces
where Arcobacter are perfectly suited. They are bathed in
hydrothermal fluids percolating from the ocean crust, which are low in
oxygen and high in hydrogen sulfide. In this niche, Arcobacter feasts on ample H2S-rich fluids and outcompetes other oxygen-respiring bacteria.
It turns out that these discharged bacterial mats may also provide an
important carpeting around hydrothermal vents that attracts other
animals, such as Alvinella tubeworms, and encourages them to settle and grow. And when we looked closer to home, we found Arcobacter bacteria
in sediments in the shallow depths of Eel Pond in Woods Hole that grow
and produce the same sulfur filaments as those at the deep-sea vents.
The world’s largest bacterium
Remarkable microbial adaptations like this seem to be common nearly
everywhere we look. In 1999, far from any undersea volcanic areas, the
world’s largest bacteria were identified by an international scientific
team that included former WHOI microbiologist Andreas Teske, who is now
at the University of North Carolina. They were found in the surface
layers of ocean sediments off the coast of Namibia, where they find
what they need: hydrogen sulfide for energy and nitrate to respire.
This bacterium, Thiomargarita namibienus
(“Sulfur pearl of Namibia”) reached sizes up to 750 microns (normal
bacteria are only 1 to 2 microns). It was so large it could be seen
with the naked eye, and it shattered our conventional wisdom that
inherent bacterial physiology prevented them from ever getting so big.
Their size is due to a large vacuole in their cells, in which they
store nitrate, as do some hydrothermal vent microbes, to survive
periods when oxygen is lacking—much the way we might store oxygen in
external SCUBA tanks to remain alive underwater.
Deep, dark, old, and cold
Arcobacter and Thiomargarita
are examples of well-adapted bacteria found in the shallow subsurface.
But deeper subsurface explorations in the past decade have revealed
unique, heretofore unknown microbial habitats.
Some of the
first investigations of the deep subsurface were motivated by concerns
about pathogens and toxic chemicals in groundwater supplies. The
Witwaterstrand Deep Microbiology Project, for example, a multinational
effort led by Princeton geomicrobiologist T.C. Onstott, sampled
groundwater in fractured rock from 3-kilometer-deep gold mines in South
Africa and found a wealth of microbial diversity in the deep
continental crust.
In 2000, researchers from West Chester
(Penn.) University claimed to have discovered the oldest known living
microorganism in an ancient salt deposit in New Mexico, buried 610
meters (2,000 feet) below ground. It was trapped in a tiny brine-filled
pocket that formed in a salt crystal 250 million years ago. Long after
the dinosaurs became extinct 65 million years ago, it lay in a dormant
state, waiting for the right conditions to “awaken” its genetic
machinery and resume growing and reproducing, the researchers said.
In the Arctic and Antarctic, scientists have found metabolically active
microbes in subsurface permafrost frozen at temperatures of -10°C
(14°F) or colder for 2 million to 3 million years. High populations of
viable microbes have been found in oceanic sediment cores deeper than a
half-kilometer, which would make them older than 10 million years.
Some like it hot
Ultimately, a combination of physical and chemical factors will set the
limits at which life can exist. In general, increasing pressure will
not limit the depth at which subsurface life is found. Increasing heat
is the primary limiting factor, and it is doubtful that we have
discovered the maximum temperature at which life can exist.
At hydrothermal vents, volcanic heat has created an environment in
which so-called hyperthermophilic (super-heat-loving) microbes thrive.
The maximum growth temperature for a microorganism so far was
discovered in 2003 by scientists at the University of Massachusetts.
They called it Strain 121, because it grows at a 121°C (250°F). But
scientists generally agree that life could exist at temperatures as
high as 140° to 145°C (284° to 295°F).
In the mid-1990s,
scientists found novel hyperthermophilic microbes in hot oil reservoirs
3 kilometers below the North Sea and the North Slope of Alaska. Oil
producers had thought that microorganisms, which “sour” or contaminate
oil, were introduced into wells, but, in fact, they are naturally
occurring and live on organic compounds in oil.
Such
discoveries push our understanding of the limits of life and the limits
of where to look for it. The known largest biosphere—fully 80 percent
of Earth’s available living space—is in the deep ocean, yet this may be
eclipsed by the subsurface biosphere as research into this realm
proceeds.
Drilling down to search for life
Deep-sea drilling remains the best way to sample the subsurface, though
it has limitations. It is costly, and potentially results in
contamination of the samples retrieved.
The deep biosphere has
been targeted as a major research initiative of the new multinational
Integrated Ocean Drilling Program, which operates deep-sea drill ships
for the oceanographic community. A new permanent microbiology
laboratory was outfitted aboard the JOIDES Resolution drill ship.
Scientists have also developed new instrument packages that plug into
and seal drilled seafloor holes, where they remain for months. These
probes offer potential windows into the interacting chemical,
hydrological, geological, and biological processes that occur beneath
the seafloor. These long-term observatories have been dubbed “CORKs,”
which is both an eponym and an acronym (Circulation Obviation Retrofit
Kits).
The real challenge is to develop sensors that can be
placed in situ in a way that doesn’t disrupt the ecosystems they are
meant to record and that are sensitive enough to provide continuous,
even real-time, monitoring of processes occurring on even a molecular
scale.
Drilling cruises are scheduled to search for microbial
life buried hundreds of meters deep under thick ocean sediments piled
atop ocean crust in volcanically quiescent continental slope regions.
In 2000, a consortium of Japanese scientists launched a several-year
project using drill ships, manned submersibles, remotely operated
vehicles, and long-term sensors, to explore, drill, and monitor the
subsurface biosphere beneath hydrothermal vents near Suiyo Seamount, an
active subsea volcano in the western Pacific.
Going to extremes
A major research goal of the Deep Ocean Exploration Institute at Woods
Hole Oceanographic Institution is to extend our subsurface search into
conditions on Earth that are deeper, hotter, and harsher than anything
previously studied. We want to learn more about the biological and
geochemical interactions that take place within this biosphere.
Any residents we find in these frontiers may well be biochemical
pioneers. In their genes, they will still have the original blueprints
for a wide range of possible biological processes. Some of these
processes—like Arcobacter’s sulfur filament machinery, or Thiomargarita’s large nitrate-storing vacuole, or the extreme heat tolerance of Strain 121—we may never have seen before.
Life on Earth and other planets
We may never know with complete certainty where and how life originated
on Earth, but the hot subsurface around hydrothermal vents is a likely
candidate. It is an environment that seems to have all the necessary
ingredients to spark critical chemical reactions that could create the
precursor building blocks of living organisms—ultimately resulting in
amino acids for proteins, the genetic machinery DNA and RNA, sugars for
energy, and lipids to make membranes.
In a hot subsurface
melting pot, far from solar ultraviolet radiation that can break down
complex molecules, these chemicals could find sanctuary in tiny rocky
crevices where they could congregate, interact, and perhaps combine
eventually with a membrane around them. Below the sea, they would
certainly be sheltered from meteor bombardment and other
life-threatening conditions that buffeted the early Earth’s surface.
Further insights into life’s ability to survive harsh conditions will
guide our search for extraterrestrial life. New evidence from Mars
shows that it once had water, and it may once have had seas that left
salt deposits like those in New Mexico. Europa, Jupiter’s moon, is
probably volcanic, and beneath its ice-covered surface may lie oceans
with hydrothermal activity. The same tools and techniques we devise to
search for life within and beneath Earth’s volcanic oceans will prove
useful there.
Our journey into Earth’s subsurface biosphere is a quest to find the limits of life.
Posted: April 12, 2004 [top] |
