Photosynthesis Analysis Shows Work Of Ancient Genetic Engineering

"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."