The oxygen-transporting protein haemo-
globin has undergone repeated adaptations
as animals evolved to conquer new environ-
ments — from the depths of the oceans
1
to high
mountain ranges
2
. These adaptations relied
on changes in the long-range interactions
between oxygen-binding sites buried in the
protein’s subunits, and between these regions
and binding sites for a multitude of small effec-
tor molecules on the protein’s surface
3
. How
did this complex molecular machine, which
can respond so exquisitely to available levels
of both oxygen and several other effector
molecules, come into being? On page 480,
Pillai et al.
4
reconstruct the stepwise evolution
of haemoglobin from precursors that existed
more than 400 million years ago.
Almost nothing was previously known about
how the four-subunit (tetrameric) form of
haemoglobin that is found in modern-day
jawed vertebrates evolved from ancient mono-
mers. Tetrameric haemoglobin consists of two
α- and two β-subunits. Pillai et al. computa-
tionally reconstructed an evolutionary tree to
chart the protein’s ancient history, using the
amino-acid sequences of a large collection of
the closely related vertebrate globin proteins,
which exist as either monomers or tetramers.
Molecular biology
Evolution of a
molecular machine
Michael Berenbrink
The multi-subunit protein haemoglobin relies on complex
interactions between its components to function properly.
Analysis of ancient precursors suggests that its evolution
from a simple monomer involved only a few steps. See p.480
The authors’ tree was constructed taking into
account that amino-acid substitutions a given
protein shares with close relatives tend to have
originated in more-recent common ancestors
than have those it shares with more-distant
relatives. The reconstructed evolutionary
tree indicates that multiple rounds of gene
duplication and subsequent divergence
gave rise to the globin family and, by way
of several ancestral proteins, to tetrameric
haemoglobin (Fig. 1).
What is special about the study is that Pillai
and colleagues went on to resurrect several of
these extinct ancestral proteins, generating
them from the amino-acid sequences pre-
dicted by the tree. The group then tested these
proteins’ functions.
First, Pillai and colleagues analysed whether
each ancestral protein could form dimers
and tetramers of like or unlike subunits. The
earliest protein — a common ancestor of
haemoglobin and the monomeric globin pro-
tein myoglobin, named AncMH by the authors
— exists only as a monomer. A later protein,
named Ancα/β, which is the ancestor of all
existing haemoglobin subunits, forms homo-
dimers when expressed at high levels. The
authors’ tree indicates that Ancα/β underwent
gene duplication to produce two proteins:
the ancestors of all existing α- or β-subunits,
which the group respectively named Ancα and
Ancβ. These proteins also form homodimers,
or even homotetramers, when expressed
alone. However, when the two are expressed
together in equal proportions, they can form
heterodimers, which then further align to yield
haemoglobin tetramers.
The group next investigated the oxygen-
binding affinity of the ancestral proteins,
along with their oxygen cooperativity (the
ability of oxygen-binding subunits to interact
with one another) and their ‘allosteric’ regula-
tion by a potent, artificial effector molecule,
inositol hexaphosphate (IHP). They found
that only Ancα and Ancβ — when expressed
together at high concentrations — show simi-
lar oxygen-binding affinity, cooperativity and
allosteric regulation to today’s haemoglobin
protein. These features are shared by all living
jawed vertebrates, but are absent or achieved
in a different way in jawless vertebrates, whose
haemoglobin proteins are of more ancient ori-
gin. This indicates that the basic functions of
jawed-vertebrate haemoglobin had already
evolved in a common ancestor of these animals
but at some time after the split with jawless
vertebrates.
Next, Pillai et al. modelled the stepwise
changes in α- and β-subunit interfaces that
might have allowed Ancα and Ancβ first to
form heterodimers with one another, and later
heterotetramers from pairs of such dimers.
The modelling indicated that strikingly few
amino-acid substitutions might have been
needed to transform a simple monomeric
for the hydrogen-producing reaction in a
protective shell of a chromium compound.
This combination of complex mitigation
strategies proved highly successful: the
authors reported EQEs of up to 96% when their
photocatalysts were irradiated with light in the
wavelength range of 350–360 nanometres.
This is excellent news, because it means they
have designed an almost perfect photocatalyst
— the IQE must be between 96% and 100%.
This is a spectacular result for several
reasons, even though strontium titanate is ‘just’
a model system for visible-light photocatalysts.
First, it demonstrates that experiments can
be designed in which EQEs come close to IQEs
within an acceptable error margin of less than
4%. Improved experimental set-ups in which
measured EQEs are very near to IQEs should
facilitate the comparison of photocatalysts
and therefore accelerate progress in this field.
Second, it proves that the combination
of design strategies used by the authors can
indeed eliminate efficiency losses associated
with recombination. It is to be expected that
the strategies used to improve the efficiency
of strontium titanate will also apply to photo-
catalysts driven by visible light — and could
therefore enable the conversion of solar energy
to hydrogen with efficiencies of about 10%.
Finally, and most importantly, Takata and
colleagues’ findings will inspire and encourage
other researchers to continue their work on
photocatalysts. One of the authors of the work,
Kazunari Domen, published his first paper
9
on
the use of strontium titanate as a photocatalyst
in 1980. This shows the timescale needed for
success in this area. Although we do not yet
have a route for the sustainable and econom-
ically viable production of hydrogen, we stand
a good chance of finding one in the next few
decades. This paper vouches for it.
Simone Pokrant is in the Department of
Chemistry and Physics of Materials, University
of Salzburg, Salzburg A-5020, Austria.
e-mail: simone.pokrant@sbg.ac.at
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in Hydrogen Supply Chains 8–11 (Academic, 2018).
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(2013).
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Chem. 22, 17–29 (1977).
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J. Chem. Soc. Chem. Commun. 543–544 (1980).
“Pillai and colleagues’ work
serves as one of the clearest
examples so far of how such
complexity can arise.”
388 | Nature | Vol 581 | 28 May 2020
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