RUST IN DAVEY JONES' LOCKER—Reddish-orange iron oxide (the same chemical compound we commonly refer to as "rust") coats the seafloor on Loihi Seamount, an active underwater volcano 25 miles off the island of Hawaii. The material is made by an abundance of microbes that live and grow by oxidizing iron directly from solid seafloor rocks. To study these newly discovered microbes, scientists have established FeMO—the Iron (Fe)-oxidizing Microbe Observatory—on Loihi. (Photo courtesy of Terry Kirby, University of Hawaii)
TRANSFORMING ROCK—Rusty-orange iron oxide coats the left side of this sample of seafloor rock, where microbes have oxided iron in the rock. They harness the chemical energy from this reaction to live and grow. The microbes did not progress to the right side of the rock, which remains its normal gray color. (Photo by Katrina Edwards)
A BUCKETFUL OF DATA—WHOI scientists prepared plastic buckets filled with thin, microbe-free samples of natural seafloor rock and placed them back on the seafloor. The experiment sought to find out what might “grow” on these “blank slates.” To their surprise, the scientists found that the samples were quickly colonized by intriguing microbes. (See animation below.) (Photo by Katrina Edwards)
An experimental sample of seafloor rock is put back on the seafloor.
Katrina Edwards, Associate Scientist
WHOI Marine Chemistry and Geochemistry Department
Between a rock and a hard place is the proverbial worst spot for people
to find themselves in. But for certain deep-sea microbes, it’s the
place to be. In 2000, to our surprise, we found that microscopic nooks
and pits within volcanic seafloor rocks harbor abundant colonies of
previously unidentified microbes.
These microbes are
different from other microorganisms living in the sunless depths. They
do not obtain the energy they need to grow and multiply by metabolizing
chemicals dissolved in seawater or in hydrothermal fluids venting from
the seafloor. Instead, these newly discovered microbes are living
directly off minerals in solid seafloor rocks.
The microbes are
oxidizing iron in the rocks, chemically altering the rocks, and
harnessing the energy produced by this chemical reaction to live. Their
discovery has raised a slew of intriguing questions:
Does our planet sustain abundant and ubiquitous populations of these microbes?
Do they play a pivotal role in chemically altering Earth’s crust?
Were they pioneering life forms on an early Earth, which was largely devoid of oxygen but full of iron?
Do they exist on other iron-rich, oxygen-poor planetary bodies such as Mars?
These
previously inconspicuous microorganisms may turn out to have starring
roles in shaping the evolution of life on Earth and other planets, and
shaping the evolution of the planet itself.
So why didn’t we
notice them before? Beyond the inherent difficulties and expense of
searching for microorganisms at the bottom of the ocean, the answer is
that we hadn’t really looked for them before. But now these
easy-to-overlook microbes have become hard to ignore.
Pumping iron on the seafloor
More and more, we are learning how life on the Earth and the Earth
itself—biology and geology—are intimately intertwined and evolve
together. Microbes are ubiquitous catalytic agents, sparking chemical
reactions that alter the physical and chemical properties of their
surroundings. Beyond our scope of vision, their cumulative metabolic
activities play a fundamental role in shaping and regulating our
environment. (Our world would be completely different, for example, if
microorganisms did not continuously decompose organic matter and
transform it back into inorganic material.)
A new field has
arisen called geomicrobiology. Scientists are now taking a closer look
at many unexplored regions of our planet, and other planets, searching
for populations of unknown microbes that may play major roles in
cycling chemicals through planetary systems.
In
geomicrobiology, the borders between rocks and living things are not so
ironclad. Many rocks are, however, and the microbes we found steal
electrons from iron atoms in the rock, changing them from ferrous
(Fe+2) to ferric (Fe+3). With the energy produced by this chemical
reaction, they convert carbon dioxide (from seawater) into organic
matter—much the way plants and plankton use solar energy and
photosynthesis to accomplish the same.
Microscopic, but mighty
Iron is one of the most abundant and reactive elements in the
environment near Earth’s surface, so the discovery of iron-oxidizing
microbes raises the potential that massive communities of them may
exist on Earth. If so, they could continually extract huge amounts of
carbon dioxide from seawater and microscopically exert a huge influence
on ocean chemistry over geologic time.
Does this large-scale
drawdown of carbon dioxide from seawater help the oceans absorb carbon
dioxide, a critical greenhouse gas, from the atmosphere? If so, it
would revise our understanding of how carbon cycles through the
planetary system—perhaps giving iron-oxidizing microbes an important,
previously unknown role in the evolution of Earth’s climate.
In their own way, the rise of microscopic photosynthetic plants caused
one of the most devastating, permanent alterations in all of Earth’s
history. They changed the chemical composition of the near-surface
environment that all life depended on, by simply pumping oxygen into
Earth’s atmosphere.
Before then, neither the atmosphere nor
the oceans contained much oxygen, but the oceans were filled with
iron-rich rocks and tons of dissolved iron. In such an iron-rich,
oxygen-poor environment, iron-oxidizing microbes may have been
dominant, pioneering life forms—a concept that compels us to reassess
our thinking about the evolution of life on early Earth.
The
existence of iron-oxidizing microbes also redirects our search for life
elsewhere in the universe. Similar microbes could have thrived, or
still thrive, in other iron-rich, oxygen-poor locales—such as Mars,
with its red, iron-rich soil, or on the volcanic seafloor below the
ice-covered ocean of Jupiter’s moon, Europa.
A search for unknown life
These unexpected new lines of inquiry began in 2000 when former WHOI
Postdoctoral Scholar Tom McCollom and I, with funding from the Mellon
Foundation and the National Science Foundation (NSF), joined a research
cruise aboard R/V Atlantis off the Oregon coast.
Since the late 1970s, when hydrothermal vents were discovered,
scientists have focused on deep-sea chemosynthetic microbes that derive
energy from dissolved hydrogen, hydrogen sulfide, and methane emitted
from these sites. Though it is easier for microbes to draw energy from
chemicals dissolved in seawater, WHOI biologist Carl Wirsen and others
had found evidence of sulfur-oxidizing bacteria that used solid
minerals as their only source of energy. (See Is Life Thriving Beneath the Seafloor?)
Enormous amounts of sulfur and sulfides are found in vent chimney
rocks, in broken chimney rubble on the seafloor, and in fine-grained
mineral particles that precipitate and “rain” out of plumes of
hydrothermal fluids spewing out of chimneys. We speculated that this
little-recognized but potentially large source of chemical energy may
sustain important microbial communities, which, in turn, could play
pivotal roles in altering the chemistry of seafloor rocks and the ocean
itself.
Our goal in 2000 was to try to identify unknown
microbes that live off solid minerals and that might be mediating
large-scale geochemical changes on Earth.
The perfect niche for microbes To explore what might be down there, we used the submersible Alvin
to place a variety of microbe-free samples of natural seafloor rock
back on the seafloor. Our aim was to see what might “grow” on these
“blank slates.”
WHOI geochemist Meg Tivey retrieved our experimental samples for us during an Alvin dive two months later (SeeThe Remarkable Diversity of Seafloor Vents). To our surprise, we found that many of the samples had thick burnt-orange coatings of oxidized iron (or “rust”).
Using a scanning electron microscope, we saw that the surfaces of the
samples were scarred with abundant pits and pores less than 20 microns
(0.0004 inches) deep and wide. In these tiny pits were large
accumulations of corkscrew-shaped stalks made of iron oxide, which
created the thick rusty coating.
Here’s what we believe is
happening: Iron-oxidizing microbes exploit a niche where the chemistry
is just right. At first, oxygen-loving microbes move into the pits.
They consume the available oxygen, which is not replenished because
seawater does not readily flow into the restricted pit areas.
That creates an ideal situation for the iron microbes, which need
low-oxygen conditions. The tiny sheltered coves within seafloor rocks
contain just enough oxygen from seawater for the iron microbes to
respire, but not an overwhelming amount that would oxidize all the
iron—without microbial intervention—before the microbes could use it.
As a byproduct of their iron-oxidizing process, the microbes produce
bundles of iron-oxide stalks that resemble a little girl’s braids.
These stalk accumulations effectively cap the pits, maintaining the
iron microbes’ preferred low-oxygen environment and securing their
turf.
FeMO—a microbial observatory
The rapid proliferation and sheer abundance of these iron microbes and
the quick chemical transformation of the rocks they lived on were
eye-opening. Now we have mobilized research that combines biology,
chemistry, and geology to explore many intriguing aspects of these iron
microbes.
Among the initial questions are: What kinds of
iron-oxidizing microbes are out there? How many are there? How are they
making a living?
These species have been notoriously
difficult to grow in the laboratory and therefore difficult to learn
about. But in our lab Dan Rogers and I, along with WHOI biologist Eric
Webb and others, have made strides recently to culture and interrogate
these elusive microbes, and we have begun to identify various species
of microbes and reveal their biochemical machinery and metabolic
capabilities.
Toward this end, we have just established
“FeMO”—an Iron (Fe)-oxidizing Microbe Observatory—to study these
microbes at a site where they are diverse and prolific. It is located
at Loihi, an active, submerged volcano, relatively conveniently located
only 25 miles southwest of the big island of Hawaii.
To
investigate the potential abundance of iron microbes, WHOI geochemist
Wolfgang Bach and I analyzed rock samples retrieved from an assortment
of holes drilled by the Ocean Drilling Program into the exposed
volcanic rock that spreads out on both sides of the mid-ocean ridge
mountain chain encircling the globe. We found that older rocks were
depleted of Fe+2 and full of Fe+3—exactly what iron-oxidizing microbes
use up and leave behind. The finding suggests that mid-ocean ridge
flanks represent millions of square miles of fertile habitat for iron
microbes.
Life on early Earth and elsewhere
We have also begun to sequence genomes of these microbes, in a project
with Mitch Sogin and Ashita Dhillion at the Marine Biological
Laboratory in Woods Hole, funded by the National Aeronautics and Space
Administration’s Astrobiology Institutes Program (NAI). These microbes
are pioneers that probably lived billions of years ago on Earth and may
exist on other planetary bodies. Identifying their genes, the enzymes
they produce, and the metabolic pathways these enzymes catalyze will
reveal an evolutionary heritage that will help us unravel the emergence
and development of life on Earth and guide our search for life
elsewhere in the universe.
A key to reconstructing the
evolution of life on Earth and other planetary bodies lies in the
ability of scientists to read the records, or “biosignatures,” that
long-dead microbes leave behind in ancient or extraterrestrial rocks.
To do that reliably, scientists must be able to distinguish changes
caused by microbial activity from those caused by abiotic oxidizing
processes such as rusting.
With this goal, scientists in our
group, including Bach, Postdoctoral Scholar Olivier Rouxel, and
graduate student Cara Santelli, are advancing a range of new approaches
to gain understanding of how microorganisms affect the microtextures,
isotopic chemistry, and history of the rocks they interact with.
If we can unravel their story, these long-neglected microbes will
reveal a profound tale about the co-evolution of Earth and life.
