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STUDY When oxygen can't serve as the final electron acceptor in respiration, some bacteria breathe dust instead. Under anaerobic conditions, the metal-reducing bacterium Shewanella oneidensis, for example, uses iron-containing minerals like goethite as its terminal electron acceptor. Because these minerals are solids under normal environmental conditions, the electron transfer must occur directly from the bacterium to the mineral.


CONTACT A single Shewanella oneidensis bacterium at the tip of a cantilever registers its attraction or repulsion to the surface of goethite through reflections of a laser beam off the top of the cantilever.
PHOTO BY S. LOWER, M. HOCHELLA, R. WEAVER, & M. FORTNEY

Bacteria that respire minerals are important in diverse processes, including the weathering of rocks and the biogeochemical cycling of nutrients. But the mechanism of this respiration mode has been a mystery that researchers only now are beginning to unveil. Using a new technique called biological force microscopy, they have quantitatively measured the interactive forces between an S. oneidensis cell and the surface of goethite. The bacterium expresses a specific protein to mediate the interaction, the data suggest.

In biological force microscopy, live cells are attached to a small bead at the end of an atomic force microscope tip. The technique allows force measurements at sub-nanonewton resolution. It was developed by Steven K. Lower, a recent Ph.D. in geological sciences and biochemistry from Virginia Polytechnic Institute & State University; Michael F. Hochella Jr., a Virginia Tech professor of geochemistry and mineralogy; and Terry J. Beveridge, a professor of microbiology at the University of Guelph [Science, 292, 1360 (2001)]. In July, Lower will be an assistant professor of geology at the University of Maryland, College Park.

The researchers measured in real time the forces between one live bacterium and the goethite surface as a function of distance under aerobic and anaerobic conditions. They compared the data with measurements against diaspore, a mineral with the same surface properties as goethite, but one that does not accept electrons from S. oneidensis. They also experimented with goethite and a dead bacterium.

They find that the attraction between S. oneidensis and goethite is strongest when oxygen is absent, when direct electron transfer should occur. Furthermore, theoretical modeling of the data with iron reductases associated with this bacterium suggests that a 150-kilodalton outer-membrane protein plays a prominent role in transferring electrons from the bacterium to the mineral, Lower says.

"This protein is not always on the surface," Lower explains. Under aerobic conditions, when there's no need to respire minerals, it's not there. But under anaerobic conditions and only in the presence of goethite, it is there--as if the bacterium senses the absence of oxygen, as well as the presence of a beneficial mineral, and changes the biomolecules on its surface on the basis of what it is sensing. The data represent the first "quantitative evidence that bacteria recognize inanimate objects, like a mineral surface," he explains.

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