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A bug's life: Exceptional genomic stability yet rapid protein evolution in a carpenter ant mutualist

The recent surge in the number of microbial genome sequences available to the scientific community is allowing researchers to address interesting ecological questions and to observe how various genomic, evolutionary, and ecological forces interact to define an organism's role in the environment. Today, Dr. Jennifer Wernegreen's group from the Marine Biological Laboratory presents new data that support a fascinating model for genome evolution in bacteria that live inside insects.

The scientists show that symbiotic bacteria have undergone exceptionally fast rates of protein evolution despite having precisely maintained their genomic architecture over long periods of evolutionary time. In their report, published today in the journal Genome Research, the scientists discuss this model in the ecological context of host-symbiont interplay.

"Symbiosis is an important driver of evolutionary novelty and ecological diversity," explains Wernegreen. "Microbial symbionts in particular have been major evolutionary catalysts throughout the 4 billion years of life on earth and have largely shaped the evolution of complex organisms."

Symbiotic bacteria live in root nodules of leguminous plants, in gutless marine worms, in echinoderms such as starfishes and sea urchins, and in specialized cells of insects such as aphids and tsetse flies. Many symbiotic relationships are obligate; neither the bacterium nor its host can live without the other.

Wernegreen's group focused on the bacterium Blochmannia, which has lived inside Camponotus and related ant genera for the past 30 million years or more. The bacteria may utilize the ant host for basic metabolic functions, including the initiation of DNA replication. In turn, the microbes may synthesize certain nutrients that enable the ants to inhabit unique ecological niches and thrive on nutritionally unbalanced food sources. This mutualistic association is thought to contribute to the astounding ecological success of Camponotus, which, with approximately 1,000 species, represents the second largest ant genus.

By sequencing the genomes of symbiotic microbes, scientists are currently uncovering the biological and mechanistic basis for these mutualistic associations. One of the primary genomic characteristics of obligate bacterial symbionts is a massive reduction in genome size compared to their free-living counterparts ?a phenomenon called "genome streamlining." Additional genome sequences of bacterial symbionts are needed, however, to more fully understand the biological basis for these associations.

Research assistants Patrick Degnan (now a doctoral student in the Department of Ecology and Evolutionary Biology at the University of Arizona) and Adam Lazarus worked with Wernegreen to sequence the entire genome ?all 791,654 nucleotides ?of Blochmannia pennsylvanicus, the endosymbiont that is specifically associated with the black carpenter ant (Camponotus pennsylvanicus). In order to trace genetic changes that occurred in the context of this ant-bacterial mutualism, they then compared the B. pennsylvanicus genome to the sequence from a related carpenter ant mutualist, B. floridanus.

Although the two Blochmannia species diverged between 16 and 20 million years ago, Wernegreen's group made a striking observation: All 635 genes shared between the two genomes were completely conserved in terms of order and strand orientation.

This is a remarkable observation, given that bacteria are particularly noted for their rapidly evolving genomes characterized by extensive recombination, gene transfer, inversion, and translocation. In comparison, the genomes of E. coli and Salmonella, which diverged between 100-150 million years ago, have undergone extensive changes in their genomic architecture. Interestingly, the observations of Wernegreen regarding B. pennsylvanicus were consistent with those previously described for the 150-200 million-year history of Buchn era, an aphid mutualist. Taken together, these results indicate that genome stasis may be a general feature of insect mutualists.

Another important feature of B. pennsylvanicus tested by the researchers was the rate of protein evolution, as measured by amino acid changes, since the divergence of B. pennsylvanicus from their free-living ancestors. The researchers showed that the amino acid sequences of Blochmannia have diverged approximately 50 times more quickly than proteins in free-living bacteria. According to the scientists, endosymbiont proteins may be more tolerant of amino acid changes when they first become associated with their hosts, and this may account for the rapid rates of protein evolution observed.

In addition, protein sequences of the two Blochmannia species exhibited different rates of evolution; divergence rates were approximately two times faster in B. floridanus than in B. pennsylvanicus. The authors suggested that these lineage-specific differences may reflect life history differences of their respective ant hosts.

When the observations of the current study are coupled with results from previous studies, a new model for bacterial genome evolution in the context of a host-symbiont relationship emerges. As Wernegreen and her colleagues explain in their Genome Research article, long-term genome stasis is a striking characteristic of insect mutualists, and it may severely constrain the evolutionary potential of these symbiotic microbes.

However, whether rapid rates of protein evolution are important for the adaptation of insect mutualists remains unclear. While the current study documents rapid changes in amino acid sequence through evolutionary time, some studies suggest that most changes in proteins are slightly harmful to the bacterium and by extension, to its host.

"Overall, the picture emerging is one of genome deterioration, with the loss of many gene functions, and extreme genome stability," says Werne green. "This genomic stability may prevent the reacquisition of those lost functions or the evolution of new ones. In addition, rapid protein evolution seems to degrade the genes that remain."

In the future, major areas of research will include understanding the forces driving this mode of genome evolution, as well as the consequences on the fitness of the bacterium and its host. "Developments in endosymbiosis are important not only to questions in basic research, but may have important practical implications," notes Wernegreen. "A very promising area of endosymbiont research is the manipulation of these bacteria to control host populations in the field."


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Source:Cold Spring Harbor Laboratory


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