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January, 2007
Bacteria, the Real Survivors
How Bugs Evolve by Cooperating

Bacteria are ubiquitous, able to survive under some of the most extreme environmental conditions on this planet. A key to this remarkable adaptability is a genomic repertoire that enables them to detect niche-specific signals. In an extensive new study, Berkeley Lab researchers have identified two distinctly different evolutionary strategies by which bacteria acquire these genes.

Microbial organisms can exist in the hot liquid environments of sea vents and thermal springs, the cold and dark environment beneath the Antarctic ice sheet, and the super-dry environment of the desert. A key to this remarkable adaptability is the acquisition of genes that enable them to detect niche-specific signals. (Images courtesy of the National Science Foundation)

"We are learning about the mechanisms by which bacterial organisms are able generate new behaviors in response to changes in their environment on an evolutionary time scale," says computational biologist Adam Arkin, director of Berkeley Lab's Virtual Institute for Microbial Stress and Survival (VIMSS). "What we are seeing is that a community of diverse bacteria is like an economy in which, at shorter time scales, you have cooperation and competition in which members exchange metabolites, quorum signals, antibiotic attacks, and other signals to survive and compete for resources."  

What's more, says Arkin, "On a longer time scale members even exchange DNA, which in some ways is a common currency, transferred between novel gene generators and novel gene consumers. If these exchanges are profitable, then the economy of the community will be strong and grow."

Arkin and his colleagues recently reported their studies of the two main strategies, horizontal gene transfer and gene duplication, by which bacteria acquire new histidine protein kinases (HPKs), in the Computational Biology section of the online Public Library of Science (PLoS). HPKs help bacteria sense and respond to their environment by detecting external signals and relaying internal signals via response regulator proteins, which implement changes in gene expression or other cellular behaviors such as motility.

"We wanted to know which of these strategies best explains the large diversity of HPKs in a variety of bacteria," says Arkin.

Arkin's co-authors were Eric Alm and Katherine Huang, who both hold joint appointments with the VIMSS and MIT University. Arkin is a member of the Department of Computational and Theoretical Biology in Berkeley Lab's Physical Biosciences Division, a UC Berkeley professor in bioengineering, and an investigator for the Howard Hughes Medical Institute.

Bacteria are among the most ubiquitous and oldest forms of life on earth, with ancestors dating back nearly four billion years. The ability of these unicellular prokaryotic organisms to survive in just about any environment is well documented. This adaptability has been linked to a number of different signaling proteins, the most prominent of which are HPKs. Present in just about all bacterial species, but most abundant in those bacteria that inhabit the most varied environments, HPKs can sense environmental conditions like the presence of nutrients and other chemicals and can coordinate the behavior of bacterial cell populations in response to environmental change.

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Adam Arkin, director of Berkeley Lab's Virtual Institute for Microbial Stress and Survival (VIMSS), was the principal investigator in a study that identified two distinctly different strategies by which bacteria acquire and activate niche-specific signaling genes. (Photo by Roy Kaltschmidt, Creative Services Office, Berkeley Lab)

Says Arkin, "In this study, we investigated the distribution of HPKs in sequenced bacterial genomes to address such fundamental questions as: what fraction of HPKs in a given genome represents newly acquired or ancient genes? What are the evolutionary processes that give rise to new HPKs? And do newly acquired HPKs sense similar signals, or do they evolve new functionality?"

Alm, Huang and Arkin identified nearly 5,000 HPKs from 207 different bacterial genomes. First they categorized these HPKs into domains, structurally and functionally defined protein units, including core kinase signaling domains and sensor domains that confer the ability to sense environmental signals and perhaps target the HPK to its appropriate response regulator.

The researchers then analyzed the evolutionary history of each domain. With this approach, they were able to distinguish between proteins that were the result of lineage-specific expansion of existing gene families within a bacterium's own genome, a variation of the gene duplication process, and proteins that came about through the process of horizontal gene transfer (HGT), in which a gene from one bacterial genome is acquired by the genome of another bacterium.

"We looked specifically at genes that recently entered into each lineage, on the assumption that recent additions are more likely to provide insight into the evolutionary basis of niche (environmental) adaptation," says Arkin. "The gene histories inferred by this procedure were used to estimate the relative contribution of HGT and gene duplication events to the evolution of new HPKs in each genome."

In comparing the two mechanisms, the researchers discovered differences in the extent to which signaling domains and their attached sensor domains were genetically conserved. They found that HPK genes imported via horizontal gene transfer usually retain their original functions in the new genome, whereas HPK genes generated through lineage-specific expansion were a major source of novel functionality when accompanied by "domain shuffling," a phenomenon in which DNA segments coding for different domains are brought together to create a brand new gene.

"We think that domain shuffling is a trial-and-error process, and we think that viruses might help bacteria with this process, though the data is far from clear. But we don't know why it is that some bacteria can do it and others can't," says Arkin. "In our study, however, we did see that HPK duplication followed by domain shuffling is the main source of new HPK genes for some bacterial species, such as Desulfovibrio vulgaris, whereas for others, like Escherichia coli, the preferred method of diversifying their sensing portfolio is through HGT."

The difference between the preferred adaptive evolution strategies of Desulfovibrio vulgaris and Escherichia coli illustrates that while the two mechanisms of gene acquisition, horizontal gene transfer and gene duplication, are widespread across bacterial taxa, there are clear, species-specific preferences for each strategy.

"How novelty is generated during the evolution of a microbial species, and how novel function might be transferred around the vast microbial universe, are central questions in biology and for understanding the architecture of cellular networks," says Arkin. "Why some mechanisms seem to be novelty producers and others seem to be consumers is a question for further research. However, the implication of such an economy of function is changing the way we think about bacterial species and communities."

Arkin says, "The ability of bacteria to create and transfer function underlies the ability of microbial communities to degrade cellulose, produce energy, and clean up waste, as well as to develop resistance to drugs and cross-species barriers to infection. Learning how evolutionary processes create novelty and are differentially regulated in different organisms is the key to harnessing and controlling these bacterial functions."

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