Microbe's Genome Reveals Insights Into Ocean Ecology

By deciphering and analyzing the DNA sequence of Silicibacter pomeroyi, a member of an important group of marine bacteria, scientists found that the metabolic strategies of marine bacterioplankton are more diverse and less conventional than previously thought.

In one surprise, the study found that S. pomeroyi has the genetic tools to enable it to use inorganic compounds (such as inorganic sulfur) for energy, which allows the microbes to use organic carbon more efficiently in low-nutrient ocean environments.

Analysis of the genome sequence also showed that the microbe has adapted in ways that allow it to take advantage of so-called ocean "hot spots" – microscopic areas of the ocean that are rich in organic matter, typically related to living and dead microbial cells. The study, which appears in the December 16 issue of Nature, was led by scientists at the University of Georgia's Department of Marine Sciences and at The Institute for Genomic Research (TIGR), along with several collaborators. The project was sponsored by the National Science Foundation.

S. pomeroyi – named for Lawrence Pomeroy, a UGA biologist who was a pioneer in the study of marine microbial ecology – is a member of an important group of marine microbes, the Roseobacter clade, found in both coastal and open oceans. Those bacteria account for an estimated 15 percent of the production of new microbial cells in the ocean.

The Nature paper's first author, Mary Ann Moran, says the DNA sequence sheds new light on ecological strategies that sustain microbial life in the world's oceans.

"This genome is especially significant for the new theories it will generate about the workings of the ocean," says Moran. "It provides new ideas and tools for investigating how microbes control carbon, sulfur, and nitrogen cycling on a global scale." The project was led by UGA's Moran and by TIGR scientist Naomi Ward, who is the paper's senior author. Other collaborators included: Ron Kiene of the University of South Alabama; Gary King of the University of Maine; Clay Fuqua of Indiana University; Robert Belas of the University of Maryland Biotechnology Institute's Center of Marine Biotechnology; and José González of the University of La Laguna in Spain.

The S. pomeroyi genome offers the first real glimpse at the genetic material harbored by the Roseobacter group of bacteria, which have evolved metabolic strategies that allow them to flourish in marine environments. While scientists knew from laboratory studies that the microbe would metabolize sulfur, the genome sequence offered several surprises about how bacteria make a living in the ocean.

One unexpected finding from the genomic analysis was evidence of "lithoheterotrophy," the ability of marine bacteria that typically rely on organic carbon fixed by primary producers as their source of cell material to also use inorganic compounds (in this case, carbon monoxide and sulfur) for energy. In that way, the microbes can save more of the organic compounds for biosynthetic processes – allowing more efficient use of organic carbon in an environment that has little to go around.

"The microbe's predicted ability to use such inorganic compounds was surprising," says Ward. "This study demonstrates how genome analysis allows us to propose new hypotheses of biological activity for a well-studied organism. We were able to test and confirm some of those hypotheses in the lab, providing more evidence for this lithohetrotropic strategy."

Another significant finding was that S. pomeroyi has numerous adaptations to living in association with ocean particles, so that it can take advantage of marine "hot spots," which feature rich areas of organic matter floating in an otherwise nutrient-poor ocean environment. The "hot spots" concept was first proposed more than a decade ago by Farooq Azam of the Scripps Institution of Oceanography.

Moran says the S. pomeroyi sequence "demonstrates that genomes of ecologically relevant cultured microbes have enormous potential to move marine biogeochemical research forward at a rapid pace, both by generating hypotheses about how the ocean works and by providing tools to investigate these hypotheses in the ocean."

Moran and colleagues at UGA along with Ward, John Heidelberg, and other scientists at TIGR headed up the project, including genome sequencing and annotation as well as experimental demonstration of properties suggested by the genome sequence. Three other groups joined the project after annotation began because of their expertise in specific genes:

* Gary King of the University of Maine confirmed that the genes which appeared to encode carbon monoxide oxidation were functional and that they allow the organism to oxidize CO at concentrations relevant to ocean waters.

* Clay Fuqua and associates at Indiana University confirmed that the two putative quorum sensing systems were functional by showing that the S. pomeroyi genes produce signaling compounds when moved into E. coli.

* Bob Belas and associates at UMBI's Center of Marine Biotechnology annotated the microbe's motility genes.

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The Institute for Genomic Research (TIGR) is a not-for-profit research institute based in Rockville, Maryland. TIGR, which sequenced the first complete genome of a free-living organism in 1995, has been at the forefront of the genomic revolution since the institute was founded in 1992. TIGR conducts research involving the structural, functional, and comparative analysis of genomes and gene products in viruses, bacteria, archaea, and eukaryotes.