Current Biology Vol 25 No 5
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Cyanobacterial Evolution: Fresh
Insight into Ancient Questions
The invention of oxygenic photosynthesis by cyanobacteria 2.4 billion years
ago forever transformed Earth. This biogeochemical shift set into motion the
evolution of subsequent microbial metabolisms and lifestyles. A new study
provides a novel approach in piecing together evidence for how this
evolutionary transition may have occurred.
Patrick M. Shih
Of all the bacterial phyla, the
cyanobacteria stand out as a group
that is intimately intertwined with the
defining geological feature of Earth:
the presence of both water and oxygen.
Even more amazing is that this
planet-changing metabolism has only
evolved once: in over three billion years
of bacterial evolution, only
cyanobacteria have reaped the
benefits of stripping electrons from a
globally plentiful molecule such as
water in order to drive photosynthesis,
producing oxygen as a byproduct.
Plants and other eukaryotes only
gained this ability by commandeering
cyanobacterial endosymbionts into
plastid organelles. Prior to the
metabolic innovation of oxygenic
photosynthesis, the world was an
anaerobic landscape, dramatically
different from the present day. Because
of the importance of how
cyanobacteria came to become
masters of oxygenic photosynthesis,
understanding the origins of this
biological feat has perplexed scientists
from different fields spanning
disciplines such as biology, chemistry,
geology, and paleontology. A new
study by Harel et al. [1] reported in this
issue of Current Biology has compiled
and analyzed protein similarity
networks from an extensive list of
bacteria from disparate redox lifestyles
to get at the heart of how cyanobacteria
evolved and how their predecessors
lived.
Although cyanobacterial evolution
is fundamental to many aspects of
our understanding of early life, there is
a high level of uncertainty regarding
how and when photosynthesis
evolved. Traditionally, scientists have
relied on the geological and fossil
record to study ancient biological
events. The geological record has
been crucial in providing evidence for
which microbial metabolisms were
present in Archean sediments [2,3],
providing novel hypotheses as to
how photosynthesis arose [4].
However, it is more difficult to
pinpoint and prove which specific
organisms were responsible for
these metabolisms; thus, scientists
have also turned to the fossil record.
Because all Precambrian life was
microbial, assigning taxonomic
lineages to microbial fossils is
inherently challenging due to the
limited number of morphological
markers that can be used to
identify them unequivocally. This
difficulty is highlighted by the
controversy surrounding the
authenticity of microfossils dating
from over three billion years ago
as either cyanobacteria or
artifacts formed from amorphous
graphite [5,6].
Molecular phylogenetics has
drastically advanced the field of
systematics in clarifying evolutionary
relationships that were once
impossible to discern; however,
interpreting deep evolutionary
relationships is still difficult, as there
may not be adequate levels of
phylogenetic signal to fully
reconstruct phylogenetic
relationships at the deepest nodes
of the Tree of Life [7,8]. In order to
address these phylogenetic
challenges, scientists have pursued
different approaches in improving
the phylogenetic signal necessary
to more confidently reconstruct
ancient relationships, such as
improved phylogenetic coverage [9],
use of horizontal gene transfer
events as phylogenetic information
[10], and use of gene duplication
events [11–13]. Although no one
method is a silver bullet, the
culmination of the body of literature
devoted to the deep evolutionary
placement of cyanobacteria within the
Tree of Life has provided many clues,
not always in agreement, for
hypotheses concerning the origin of
this phylum.
With a scant fossil record and
molecular phylogenetics methods
being strained with such deep
evolutionary questions, Harel et al. [1]
present an outside-the-box approach
complementary to traditional
phylogenetic approaches by instead
utilizing protein similarity networks to
provide clues as to how and from
whom cyanobacteria evolved. They
examine 48 cyanobacterial and 84
microbial proteomes that represent
four major metabolic groups:
methanogens, obligate anaerobes,
facultative aerobes, and obligate
aerobes. Over the course of Earth’s
history, the planet has slowly
transitioned from highly anoxic to a
more oxidizing environment. Thus,
one would expect the emergence of
each of these groups to come in
order from most reducing to most
oxidizing. By utilizing protein similarity
networks, connections between the
different metabolic groups can be
represented, providing evidence for
which groups are more closely
associated with one another. Harel
et al. [1] recapitulate the expected
order of relation between these
metabolic groups, placing
cyanobacteria fittingly between
anaerobes and obligate aerobes.
These findings logically make
sense: if cyanobacteria were the
first organisms in an anaerobic world
to evolve oxygenic photosynthesis,
it would be reasonable to suspect
that they would have deep connections
with both the preexisting anaerobes
and the subsequently evolving
aerobes.
One of the most interesting
implications of the study is how
metabolic innovation may drive
biological diversity. What would life
look like had oxygenic photosynthesis
never evolved? Aerobic respiration
would most likely never have evolved,
drastically changing what we know
of many branches scattered across
the Tree of Life. With evidence
connecting cyanobacteria to both
anaerobes and aerobes, one can infer
that the innovation of oxygenic
photosynthesis opened an entirely
new metabolic chapter in life’s history.
It seems likely that more complex
forms of life such as eukaryotes
may not have been able to evolve
in the absence of respiration.
In line with this, a growing body
of evidence has suggested that
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Johnson, T., Fischer, W.W., and Lyons, T.W.
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have set out to answer, an analogy can be able to perform genome sequencing oxygen levels and the delayed rise of animals.
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be drawn from the more common of organisms that existed billions of 15. Mills, D.B., Ward, L.M., Jones, C., Sweeten, B.,
example of birds and dinosaurs. It years ago. In light of this humbling fact, Forth, M., Treusch, A.H., and Canfield, D.E.
would be difficult to imagine what the novel studies such as Harel et al. (2014). Oxygen requirements of the earliest
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ancient predecessors of birds, i.e. provide keen insight that will continue 4168–4172.
dinosaurs, would look like if we had to fuel the debate around this hotly
no access to fossil data and had contested field. Nonetheless, it is Joint BioEnergy Institute, 5885 Hollis St,
only ever seen modern crocodiles studies like this that will also help push Emeryville, CA 94608, USA and Physical
and birds. It would be a far stretch of the field forward and promote the Biosciences Division, Lawrence Berkeley
the imagination to concoct the discussion necessary to prompt National Laboratory, One Cyclotron Rd,
Berkeley, CA 94720, USA.
wide range of morphological scientists to come up with the next
E-mail: pmshih@lbl.gov
differences that we know to have creative approach to addressing this
existed based on the dinosaur fossil incredibly difficult yet profoundly
record. Now, imagine doing this with an important question. http://dx.doi.org/10.1016/j.cub.2014.12.046