INSIGHTS | PERSPECTIVES
Energy-releasing chemical reactions are at the core of the living process of all organisms. These bioenergetic reac- tions have myriad substrates and prod- ucts, but their main by-product today is adenosine triphosphate (ATP), life’s
primary currency of metabolic energy. Bioenergetic reactions have been running in a sequence of uninterrupted continuity since the
first prokaryotes arose on Earth more than
3.5 billion years ago, long before there was
oxygen to breathe (1). Under what conditions
did these bioenergetic processes first evolve?
Many ingenious ideas about energy at
life’s origins have nothing in common with
modern life. It is conceivable that early life
harnessed energy from volcanic pyrite synthesis (2), zinc sulfide–based photosynthesis
(3), ultraviolet radiation, or lightning, yet
none of these processes powers known microbial life forms. For biologists, the origin of
energy-harnessing mechanisms used by real
microbes is the issue. Recent studies point to
parallels between the energy-harnessing systems of ancient microbes and the geochemistry of alkaline hydrothermal vents (see the
figure), suggesting that natural ion gradients
in such vents ignited life’s ongoing chemical
How did the first cells harness energy? Because life arose in a world without molecular oxygen, some anaerobes are likely to be
ancient, and anaerobic environments should
harbor primitive bioenergetic reactions (4,
5). Ancient anaerobic niches deep in Earth’s
crust often contain acetogens (bacteria) and
methanogens (archaea), groups that biologists have long thought to be ancient (4).
However, anaerobic environments harbor
very little energy to harness (6, 7). In the anaerobic environments of submarine hydrothermal vents, geochemically generated H2
is the main source of chemical energy.
In addition to being strict anaerobes, ace-
togens and methanogens live from H2, us-
ing the simplest and arguably most ancient
forms of energy metabolism (8). Both syn-
thesize ATP by reducing CO2 with electrons
from H2 to make acetate and methane, re-
spectively. They use a chemical mechanism
called flavin-based electron bifurcation (6)
to generate highly reactive ferredoxins—
small, ancient iron-sulfur proteins (5) that
are as central to their energy conservation
as is ATP (6). The shared backbone of their
energy metabolism is the acetyl–coenzyme
A pathway, the most primitive CO2-fixing
pathway (8) and the one typical of sub-
surface microbes (9). Metabolism in these
anaerobes is furthermore replete with reac-
tions catalyzed by transition metals such
as iron, nickel, molybdenum, or tungsten,
another ancient trait (2, 5–8).
All known life forms, including methanogens and acetogens, use two basic mechanisms to tap environmentally available
energy and harness it as ATP. The first is
substrate-level phosphorylation, in which
highly reactive phosphate-containing compounds phosphorylate adenosine diphosphate (ADP) to make ATP (6, 10). The energy
conserved in ATP is released in a subsequent
reaction that does chemical work for the
cell or allows more sluggish reactions to go
forward. The highly reactive phosphate compounds are generated during conversions of
carbon compounds. Their synthesis is driven
by environmental sources of chemical energy such as H2 plus CO2 that are harnessed
during conversion to more thermodynamically stable compounds such as methane
The second mechanism that cells use to
harness energy involves ion gradients and
is called chemiosmotic coupling. Here, an
energy-releasing reaction is coupled to the
pumping of ions across a membrane from
inside the cell to the outside. The most common ions used for this purpose are protons,
By William F. Martin,1
Filipa L. Sousa,1 Nick Lane2
1Institute of Molecular Evolution, Heinrich-Heine-Universität,
Universitätsstrasse 1, 40225 Düsseldorf, Germany. 2Research
Department of Genetics, Evolution and Environment,
University College London, London WC1E 6BT, UK. E-mail:
… the primordial ATPase
could have harnessed
gradients at an alkaline
Energy at life’s origin
Analysis of the bioenergetics of primitive organisms
suggests that life began at hydrothermal vents
EVOLUTION ing management criteria for qualification,
and expanding their total area, building
on country-level evidence and experience
(recommendations 3 and 6 to MSs); (iv) develop longer-term perspectives for more effective and comprehensive protection and
restoration of grasslands and peatland; (v)
reevaluate the usefulness of the crop diversity measure.
Our recommendations should encourage
MSs and the EU to start moving toward
more sustainable agriculture, securing
food provision alongside biodiversity and
ecosystem services for current and future
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We thank P. Ibisch, T. Vandermaesen, A. Barnett, E. Ellis, L.
Podmaniczky, T. Hartel, J. Y. Humbert, M. Liebman, S. Becheva,
G. Beaufoy, S. Boldogh, J. Tzanopoulos, J. Hegarty, T. Lancaster,
and P. Vorisek for valuable inputs. G.P., K.H., and A.V.S.
acknowledge EC FP7 projects SCALES (contract 226852),
R.A. was supported by the Swiss National Science Foundation
(31003A-120152) and the Swiss Government; A.A.B. and D.K.
acknowledge EC FP7 project LIBERATION (311781); A.A.B.
acknowledges MTA Lendület; W.J.S. acknowledges Arcadia;
L.V.D. is funded by the Natural Environment Research Council
(NE/K015419/1); The Pan-European Common Bird Monitoring
Scheme is a joint initiative of the European Bird Census Council
and the BirdLife International, funded by the EC and the Royal
Society for the Protection of Birds.