More that twenty years ago, Penn State's James G.
Ferry first isolated Methanosarcina acetivorans from anaerobic
sediment beneath a kelp bed. Ferry and Christopher House, also at
Penn State, have helped uncover the biochemistry this microbe uses
to make vinegar out of carbon monoxide. Now they suggest that this
a primitive version of this unique biochemistry may have fueled
the metabolism of the first life forms on earth.
James G. Ferry is Stanley Person Professor of
Biochemistry and Molecular Biology, and Christopher House is Assistant
Professor of Geosciences, both at Penn State. They will announce their
new theory in the June issue of Molecular Biology and Evolution.
William Martin, editor-in-chief of that journal, says "The paper is a
very significant contribution, and a wonderful example of
interdisiplinary work as well."
"We've taken a new approach to thinking about the
evolution of life from a thermodynamic perspective," Ferry says. "It
reshapes the two previous theories of life's origin, it shows how they
overlap, and it extends both of them significantly." The apparently
irreconcilable "heterotrophic" and "chemoautotrophic" theories of the
origin of life both focus on the processes by which chemical building
blocks first appeared for primitive life to assemble into complex
molecules. "But that's not really what the driving force was in early
evolution," Ferry asserts. "Nobody had properly considered
"The problem of early energy sources has largely
been ignored by the classical origin-of-life field," Molecular Biology
and Evolution's Martin says, "which has largely been the domain of
chemists. But microbiologists are the only ones who understand where
the origin of life needs to get--modern microbial life."
According to the heterotrophic theory, a primordial
soup of simple molecules arose first, driven by nonbiological energy
sources like lightning, and led eventually to primitive life forms.
One difficulty with this theory is due to the huge variety and
complexity of organic molecules that would have had to arise
spontaneously. In contrast, the chemoautotrophic theory rests on the
idea that primitive life forms themselves, perhaps associated with
catalytic iron and sulfur minerals, gave rise to the first simple
biological molecules. The obstacles to this theory are the large
number of steps in the biochemical cycles that have been suggested,
and the staggering structural complexity of the only known enzyme
complexes that drive those reactions. Debate between the two camps has
raged for two decades.
By studying a microbe that Ferry discovered
thriving in the oxygen-free, carbon-monoxide-rich sediment beneath
kelp beds, he and his group have helped to break this impasse. Life
may have emerged in just such an environment, and this microbe's
unique biochemistry may harbor the molecular fossil of the first
metabolism on Earth.
While other microbes make methane from carbon
monoxide, this particular species (one "Methanosarcina acetivorans")
also produces acetate - -better known as vinegar. Ferry and House, in
collaboration with Barry Karger at Northeastern University, showed how
carbon monoxide is converted to acetate in a biochemical pathway that
includes a well-known pair of enzymes, called Pta ("phosphotransacetylase")
and Ack ("acetate kinase"). The two researchers realized that, in the
presence of minerals containing iron sulfides, acetate could have been
catalytically converted to a sulfur-containing derivative called an
acetate thioester. Attached to the mineral surface, a "protocell"
containing primitive forms of these two enzymes could then have
generated biochemical energy by converting this derivative back to
acetate. Excreting acetate would have completed the cycle. "Our paper,"
House suggests, "contains a very sensible early metabolism." "It is
quite possible," Ferry says reverently, "that this could be the first
As in virtually every metabolic reaction on Earth,
the energy produced by these reactions is stored in a molecule called
ATP. The Ack enzyme catalyzes the synthesis of ATP directly. On the
other hand, most ATP molecules--including those that this microbe
makes by converting carbon monoxide into methane--are produced by
multi-enzyme protein machines within the cell membrane that get their
energy indirectly, from yet another protein machine that pumps an
osmotic imbalance across the membrane. "It's difficult to imagine that
something so complex could have emerged all at once," Ferry says, as
the chemoautotrophic theory requires.
The acetate-producing species appears to be the
direct descendant of one of the earliest true microbes. "We know that
this bug is very ancient indeed," Ferry told the Penn State
Astrobiology Research Center's annual meeting earlier this week. "There
is strong phylogenetic evidence that acetate kinase is a very ancient
enzyme." No such evidence can pinpoint the age of Pta, "but these two
enzymes always work together," suggesting that they evolved together.
The two enzymes' primeval genetic provenance and the simplicity of the
three-step cycle, House says, "are absolutely central to the idea."
"This longstanding debate between the heterotrophic
and chemotrophic theories," House continues, "revolved around carbon
fixation." The new thermodynamic theory inverts the focus, Ferry says.
"All these pathways evolved first to make energy. Afterwards, they
evolved to fix carbon. These ideas suggest a totally new perspective.
It's truly a quantum leap - a milestone."
The paper also proposes mechanisms by which Ferry
and House's mineral-bound protocell could have evolved into a
free-living cell, and how the metabolism of acetate to methane could
have evolved based on the pathways they discovered. The genomic and
proteomic analyses of carbon monoxide conversion to methane and
acetate, carried out in collaboration with Northeastern's Karger, will
appear later this year. The Department of Energy and the NASA
Astrobiology Institute sponsored the research.