Genomic comparison of ocean microbes reveals East-West divide in populations

Using a relatively new methodology called comparative population genomics, these scientists compare the entire genomes of different populations of the same microbe to see which genes are "housekeeping" or core genes essential to all populations and which are population-specific. Scientists are able to read a genome and translate the genes into proteins that serve particular functions. Population-specific genes sometimes tell a very clear story about the environment, for instance temperature and the availability of light and particular elements, and over time, they can point to the microbes' evolutionary adaptation to changes in the ecosystem. Occasionally, as was the case with recent research at MIT, the population-specific genes reveal this information with crystal clarity, even providing unmistakable clues about lifestyle.

Professor Sallie (Penny) W. Chisholm of MIT's Department of Civil and Environmental Engineering (CEE) and former doctoral student Maureen Coleman compared the genetic makeup of two populations of the same oceanic photosynthetic bacterium, Prochlorococcus, one living in the Atlantic Ocean and one in the Pacific.

They found that although a continent separates the populations, they differ significantly in only one respect: those in the Atlantic have many more genes specifically related to the scavenging of phosphorus, an essential element for these microbes. And just as the variations in the beaks of Darwin's finches were evolutionary adaptations related to food availability, so too are the variations in the Prochlorococcus genes related to phosphorus gathering. Both are examples of a powerful evolutionary force at work.

"We expected to see some difference in the genes related to phosphorus, because the Atlantic Ocean has an order of magnitude lower concentration of phosphorus than the Pacific, so Atlantic populations of Prochlorococcus carry many more genes involved in extracting phosphorus from the seawater. They need more creative ways of gathering it. But we didn't expect it to be the only difference," said Chisholm. "This indicates that phosphorus availability is the dominant selective force in defining these populations."

The researchers also noted that the microbes in the Atlantic Ocean had increased numbers of phosphorus-related genes that helped them neutralize arsenic, an element they sometimes take up by mistake when they're scavenging for phosphorus. This finding "buttresses the assertion" that this is the result of a strong selective process, Chisholm said.

"We're really diagnosing the ecosystem using a specific species of microbe as a reporter," said Chisholm. "We're letting the cells tell us what they have to deal with in their environment."

She and Coleman also compared the genomes of two populations of a neighboring bacterium, Pelagibacter, and found that genes related to phosphorus gathering in that bacterium appear in far greater numbers in the Atlantic Ocean population, but with a twist. These microbes have a somewhat different repertoire of phosphorus-related genes, suggesting subtle differences between these two microbial groups with respect to how they scavenge phosphorus. This could reflect an adaptive behavior known as "niche partitioning," which allows cells sharing a microenvironment to apportion resources according to a cell's "lifestyle" rather than all competing for the same element or same form of that element.

To obtain these findings, which were published in the online Early Edition of the Proceedings of the National Academy of Sciences the week of Oct. 11, the two scientists used the complete genomes of 13 strains of lab-cultured Prochlorococcus and Pelagibacter as reference genes, and compared these with the genes of well-documented wild microbe populations gathered at long-term oceanographic study stations near Bermuda (BATS) and Hawaii (HOTS). The work was funded by the Gordon and Betty Moore Foundation, the National Science Foundation and the U.S. Department of Energy.

The next step in this research is to make similar studies at different depths and locations to study the effects of temperature and chemical gradients on the genomes of microbial populations.

"How fast marine microbes adapt to environmental change is a big unknown," said Coleman, who is now a postdoctoral associate at Caltech. "One way to address this is to sample the population genomes over time, with parallel environmental monitoring. We might then be able to catch evolution in action. Long term study sites like HOT and BATS are crucial for this effort."