Oceanic Bacterium Is Big For Its Size

By Colleen F. Craig

A research team at Oregon State University (OSU) recently reported in Science that the tiny oceanic bacterium called SAR11 possesses the smallest known genome, or set of DNA, of any free-living organism. Not only does SAR11's genome appears to contain instructions for nearly all the basic cellular functions observed in its larger-genomed cousins, but now researchers have determined that it provides a mechanism to extract energy directly from sunlight.

This mechanism, described by the OSU team in the journal Nature in November, may serve as a "back-up" energy generator when few nutrients are available.

The ocean is a tough place for bacteria to grow, since the concentration of nutrients in the sea can vary dramatically. And yet SAR11 is one of the most abundant of marine bacteria. The combined weight of all SAR11 cells in the ocean would be larger than that of all the fish, and the organism can be found in nearly every ocean.

"It appears that evolution has acted on SAR11 to make it a very efficient, simple, and well-integrated cell," says Stephen Giovannoni, professor of microbiology at OSU and principal investigator for the SAR11 studies.

The very thing that makes the ocean such a harsh environment–the varying and at times extremely low concentration of nutrients–helped SAR11 adapt to take full advantage of scarce resources. Its small genome is one adaptation: less energy is required to replicate a small genome than a large one during cell division, the method by which bacteria reproduce.

Its small size is another adaptation. SAR11 has more surface area relative to its volume than bigger cells, so it can absorb relatively more nutrients.

But the most intriguing adaptation is the presence of a gene for the light-sensitive protein called proteorhodopsin, which is similar to pigments, known as rhodopsins, found in the human eye. Whereas rhodopsin just detects light, initiating a chain of chemical reactions that ultimately alerts the brain to what it's "seeing," proteorhodopsin may serve as a kind of "back-up" energy system for SAR11 during periods when few nutrients are available.

Under normal conditions, the cell absorbs carbon-containing compounds from its surroundings through channels called "membrane transporters." Through a process called respiration, these nutrients are broken down to form a molecule called adenosine triphosphate (ATP), which stores energy for the cell. Proteorhodopsin is thought to short-circuit this process by allowing SAR11 to produce ATP using light energy, without absorbing nutrients.

Proteorhodopsin was first discovered in sequences cloned from DNA in cells obtained from seawater by Oded Beja and coworkers at the Monterey Bay Aquarium Research Institute (MBARI) in 2000. But SAR11 is the first bacterium that has a proteorhodopsin gene to be grown in a lab, thanks to new technology supported by a $3.4-million grant from the Gordon and Betty Moore foundation. The new cell-culturing technology gave Giovannoni's team the opportunity to study SAR11 at an unprecedented level of detail.

To test the function of proteorhodopsin in SAR11, Giovannoni's team exposed different cultures to different levels of light as they grew. Just as a plant cannot grow in the dark, the SAR11 population would be similarly affected by a lack of light if the proteorhodopsin mechanism were essential to normal growth. Surprisingly, there was no significant difference in population size between cultures grown in light and dark conditions, which suggested that proteorhodopsin has a more subtle role in SAR11's survival.

"We are especially interested in how the respiratory energy-generating system and the light-driven energy-generating system interact. That we have not figured out," says Giovannoni.

One idea is that the proteorhodopsin system may kick in during times of starvation. If the cell is deprived of nutrients, it enters a dormancy phase, but still monitors its surroundings so it will know when more nutrients become available and it can wake up. "The best membrane transporters that bring in nutrients require ATP," says Giovannoni. "This cell has a lot of those transporters. If it can't make ATP, it can't turn on its transporters. We suspect that the proteorhodopsin system jump starts the cell when it can't make ATP. We haven't proved it."

The problem is that SAR11 must be grown in seawater, which is a complex mixture of thousands of different compounds that may or may not affect SAR11's metabolism. "We need to be able to turn things on and off by providing different nutrients," says Giovannoni. "Once we can modify seawater to control what nutrients the cell is getting then we can test these ideas."

Ultimately the team hopes to develop a computer model of SAR11's metabolism using the results of the seawater study. Cellular metabolism in general is an exceptionally complicated collection of thousands of inter-related chemical reactions that present an extreme challenge to computer modelers. SAR11's small size and relatively straightforward metabolism makes it an ideal candidate for computer modeling.

In addition to the interplay between the proteorhodopsin and respiration mechanisms, simulations could shed light on how other metabolic pathways in SAR11 interact, and how the cell reacts to changing conditions in the open ocean. This is important to understand because SAR11 plays a key role in global geochemistry, converting carbon-containing compounds dissolved in the ocean into the carbon dioxide consumed by oceanic algae, which produce about half of the world's oxygen through photosynthesis.

Colleen Craig is an intern with Northwest Science & Technology and a fifth year graduate student in theoretical chemistry at University of Washington.

Image at Top:

OSU scientist Steve Giovannoni considers a spoonful of seawater, which probably contains half a million bacterial cells. Photo: Lynn Ketchum