The development of the biochemical process of photosynthesis is
one of nature’s most important events, but how did it actually happen?
This is a question that molecular biology has first posed, and now
perhaps answered.

"The process of photosynthesis is a very complex set of interdependent
metabolic pathways," said Robert Blankenship, professor of
biochemistry at Arizona State University. "How it could have
evolved is a bit mysterious."

Photosynthesis is one of the most important chemical processes
ever developed by life — a chemical process that transforms sunlight
into chemical energy, ultimately powering virtually all the living
things and allowing them to dominate the earth. The evolution of
aerobic photosynthesis in bacteria is also the most likely reason
for the development of an oxygen-rich atmosphere that transformed
the chemistry of the Earth billions of years ago, further triggering
the evolution of complex life.

After decades of research, biochemists now understand that this
critical biological process depends on some very elaborate and rapid
chemistry involving a series of enormously large and complex molecules
– a set of complex molecular systems all working together.

"We know that the process evolved in bacteria, probably before
2.5 billion years ago, but the history of photosynthesis’s development
is very hard to trace," said Blankenship. "There’s a bewildering
diversity of photosynthetic microorganisms out there that use clearly
related, but somewhat different processes. They have some common
threads tying them together, but it has never been clear how they
relate to each other and how the process of photosynthesis started,
how it developed, and how we actually wind up with two photosystems
working together in more complex photosynthetic organisms."

In a paper forthcoming in the November 22 issue of the journal
Science, Blankenship and colleagues partially unravel this mystery
through an analysis of the genomes of five bacteria representing
the basic groups of photosynthetic bacteria and the complete range
of known photosynthetic processes. The paper is co-authored by ASU
doctoral student Jason Raymond, Olga Zhazybayeva and J. Peter Gogarten
of the University of Connecticut at Storrs, and Sveta Y. Gerdes
of Integrated Genomics in Chicago, Illinois.

The analysis revealed clear evidence that photosynthesis did not
evolve through a linear path of steady change and growing complexity
but through a merging of evolutionary lines that brought together
independently evolving chemical systems — the swapping of blocks
of genetic material among bacterial species known as horizontal
gene transfer.

"We found that the photosynthesis-related genes in these organisms
have not had all the same pathway of evolution. It’s clear evidence
for horizontal gene transfer," said Blankenship.

The team examined the genes of five already sequenced photosynthetic
bacterial genomes – a cyanobacterium known as Synechocystis sp.
PCC 6803; Chloroflexus aurantiacus, a green filamentous bacteria;
Chlorobium tepidum, a green sulfur bacteria; Rhodobacter capsulatus,
a proteobacteria; and Heliobacillus mobilis, a heliobacteria. They
found a set of 188 genes that appeared to be related (orthologous)
between these organisms. The five species belong to very separate
classifications, but since they share, to varying degrees, the same
photosynthetic chemical systems, the team deduced that the photosynthesis-related
genes must be among the shared genes.

Blankenship and his colleagues then performed a mathematical analysis
of the set of shared genes to determine possible evolutionary relationships
between them, but they arrived at different results depending on
which genes were tested.

"We did a kind of tree analysis of all 188 genes to determine
what the best evolutionary tree was. We found that a fraction of
the genes supported each of the different possible arrangements
of the tree. It’s clear that the genes themselves have different
evolutionary histories," Blankenship said.

Blankenship argues that this explains the how the complex biochemical
machinery of photosynthesis could have developed: Different pieces
of the system evolved separately in different organisms, perhaps
to serve purposes different from their current function in the photosynthesis.
Brought together either by fusion of two different bacteria or by
the "recruitment" of blocks of genes, the new combination
of genes resulted in a new combined system. Further evolution of
the system and further re-combination probably occurred many times
in different organisms.

The team also compared the set of shared photosynthetic bacteria
genes with known genomes from other bacteria and found that very
few of the shared genes are actually unique to photosynthetic organisms.
While a number of the widely shared genes are probably "housekeeping
genes" that are basic to most bacteria, Blankenship thinks
that many of the shared genes involve metabolic pathways in non-photosynthetic
bacteria that have been recruited to be part of photosynthesis systems.

"This kind of evolution in bacteria is kind of like what happens
at a junk dealer," said Blankenship. "Bits and pieces
of whatever there is out in the yard get hauled back and welded
together and made into this new thing. All these metabolic pathways
get borrowed and bent a bit and changed."

Blankenship points out that nature’s way of creating useful and
complicated chemical systems through horizontal gene transfer also
points to how human-directed biodesign might co-opt the process.

"This work gives us some insights into how complex metabolic
pathways originated and evolved, so this might give some ideas about
how to engineer new pathways into microorganisms," he said.
"These organisms could be designed to carry out new types of
chemistry that may benefit mankind, such as multi-step synthesis
of drugs."

The research applies as well to collaborative efforts going on
at ASU between the university’s Center for the Study of Early Events
in Photosynthesis and its membership in the NASA Astrobiology Institute.

"A major focus of the astrobiology program is to try to figure
out what path life might have taken on some other world besides
Earth," he said "There are people that make the argument
that it would be likely to have taken a similar trajectory. You
have to have some kind of energetic source for organisms to live
on and certainly sunlight is one of the most likely options, since
it’s a high quality flow of energy. Now we have a picture of how
life has developed that source on our planet."