NATURE'S TINIEST GEOENGINEERS
It's becoming clear that microbial metabolism and geochemical processes are tightly linked

AMANDA YARNELL, C&EN WASHINGTON

Historically, geochemical processes were thought to be largely, if not entirely, driven by abiotic chemical reactions. "People ignored what bacterial metabolism might be contributing," noted Andrew L. Neal, a geomicrobiologist at the University of Georgia's Savannah River Ecology Laboratory. "But now we know that many important geochemical reactions are driven by bacteria."

	BACTERIA ROCK Found in a geothermal spring in New Zealand, these silica formations are composed of layers of inorganic silica and layers of bacterial colonies. COURTESY OF LIANE BENNING

The relationship between microorganisms and geochemistry was the subject of a symposium held last month at the American Chemical Society national meeting in New York City. The symposium was cosponsored by the Geochemistry, Environmental Chemistry, and Biological Chemistry Divisions. And it was co-organized by Neal and Craig Cooper, a geochemist at the Idaho National Engineering & Environmental Laboratory (INEEL).

Bacteria and other microbes impact just about every geochemical process that one can think of, including the weathering of rocks, the fate of metal-based contaminants in streams and rivers, and the formation and disappearance of minerals.

For instance, sometimes bacteria must resort to scavenging the metals they need to survive. In order to cope, these bacteria send out iron-loving organic molecules called siderophores to pilfer iron from iron minerals when sufficient dissolved iron is not available.

But siderophores also avidly bind other metals, including toxic ones like lead and cadmium, noted Patricia A. Maurice, a professor of civil engineering and geological sciences at Notre Dame University, in Indiana. At the symposium, Maurice discussed her lab's work on the potential geological consequences of indiscriminate metal binding by bacterially produced siderophores.

Previously, Maurice and her coworkers showed that siderophores can release aluminum ions from the aluminum silicate mineral kaolinite. This finding suggests that siderophores may mobilize toxic metals, she said.

But siderophores also may adsorb to mineral surfaces, trapping their toxic-metal cargo, Maurice noted. She and graduate student Sarah E. Hepinstall now have found that siderophore-mediated adsorption of metals to kaolinite can in fact occur, but the process is complex and pH-dependent. For instance, certain lead-loaded siderophores--but not others--can enhance adsorption of lead to kaolinite. Maurice and Hepinstall are now using synchroton-based methods to figure out why.

Bacteria and other microorganisms also have a hand in weathering of rocks and stones. Some bacteria produce a polysaccharide-based gel that helps them stick to the surface of the rocks that they call home. But depending on the environment and their chemical structure, these bacterially produced polymers can promote dissolution of the rock.

Graduate student Thomas D. Perry IV of Harvard University's division of engineering and applied sciences is studying bacterially produced polymers that promote degradation of limestone made of calcite. Perry, his adviser Ralph Mitchell, and professor Scot T. Martin are using atomic force microscopy to image polymer-promoted dissolution of a calcite surface while measuring the rate of dissolution.

---

Bacteria and other microbes impact just about every geochemical process that one can think of.

---

THE FIRST POLYMER they have investigated--alginic acid, a linear copolymer consisting primarily of -1,4-linked D-mannuronic acid and -1,4-linked L-glucuronic acid--is produced by many kinds of microorganisms. Even at concentrations as low as 0.1%, alginic acid dramatically increases calcite dissolution over a wide pH range, Perry reported at the symposium. He suggested that the polymer does so by preferentially binding to and chelating calcium ions found in exposed "pits" in the calcite surface.

Perry and colleagues are now investigating the effects of other polymers produced by microorganisms that live on the limestone blocks of the ruins of the ancient Mayan city of Ek Balam, located near Playa del Carmen in Mexico. He hopes the work may lead to methods to prevent microbe-mediated deterioration of these and other irreplaceable ancient structures.

Bacteria also affect the flow of water containing organic contaminants through topsoil, gravel, and rock, according to Randall A. LaViolette, an INEEL geochemist who also spoke at the symposium. INEEL is studying whether native microorganisms can be coaxed to degrade dissolved organic contaminants in aquifers. Although this bioremediation process appears promising in lab tests, it happens far more slowly in the field. LaViolette and colleague Daphne L. Stoner have turned to modeling to figure out why.

THEIR MODELING shows that differences in the spatial distribution of bacteria underground produce "hot spots" of contaminant concentration. Lab tests, on the other hand, mix bacteria and a dilute, homogenous solution of contaminant--suggesting that more contaminant would be left in the field because bacteria are unevenly distributed. He told C&EN that their results have inspired proposals of how bacteria in the field might be "stirred" to speed up bioremediation.

METAL SPONGE Using an X-ray spectroscopic technique, Warren has shown that bacteria (green) in a stream draining from a mine form a manganese oxyhydroxide biomineral (blue) that might be harnessed to sop up metal contaminants. In the center is another iron-based mineral (pink) thought to be formed abiotically. COURTESY OF ADAM HITCHCOCK
BYSTANDER An empty sheath covered with 20- to 200-nm silica spheres is all that is left after a cyanobacterium undergoes silica biomineralization in the lab. COURTESY OF LIANE BENNING

Associate professor Lesley A. Warren of the School of Geography & Geology at McMaster University, Hamilton, Ontario, is also studying the role microbes play in the fate of contaminants. She's particularly interested in microbes found in a stream that drains a mine site in northern Ontario. Despite the stream's harsh conditions--its pH often dips below 3, and it is laden with metals--microbes flourish, Warren reported at the ACS meeting. They live in complex communities called biofilms--the microbial equivalent of high-rise apartments--that form where water and sediment meet.

In collaboration with professor Adam P. Hitchcock of McMaster's chemistry department, Warren and graduate student Elizabeth A. Haack are using a host of X-ray methods to characterize the three-dimensional architecture of these biofilms. A technique called scanning transmission X-ray microspectroscopy reveals that the biofilms are made up of small, diverse minicommunities of bacteria. It also shows that some of the bacteria in these minicommunities produce a mineral on the outside of their membranes. Using X-ray absorption fluorescence spectroscopy, Warren's team has shown that this biomineral is manganese oxyhydroxide--and that it sequesters trace toxic metals like nickel, cobalt, and chromium from the stream.

Warren thinks that such bacterially produced manganese oxyhydroxide biominerals play a crucial role in whether metals are carried downstream, away from the mine. "If we understand how, then we will be able to target these metal-retention processes for bioremediation," Warren told C&EN.

IN ADDITION TO these and other active roles that microbes play in geochemical processes, the simple presence of bacteria can have indirect geochemical consequences. Liane G. Benning, a geochemist at the University of Leeds, in England, is studying how microbes contribute to the formation of porous silica crusts. She told symposium attendees about her lab's successful use of synchrotron-based infrared microspectroscopy to follow the course of silica biomineralization in vitro. Her results show that cyanobacteria provide a surface for silica accumulation by inorganic precipitation--but that they don't actively contribute to silica formation.

Benning's work, as well as that of the other symposium speakers, demonstrates that the chemistry that occurs close to microbial surfaces is very different from that of the bulk solution, Cooper pointed out. "The chemistry of this 'microbial space' becomes even more complex when the microorganism is in contact with a mineral surface. The science of biogeochemistry is attempting to uncover the processes that occur at these interfaces and explain how they affect larger environmental cycles," he added. High-resolution synchrotron-based methods such as scanning transmission X-ray microspectroscopy and X-ray absorption fluorescence microscopy are helping to fuel discoveries in this area.

This emerging area of geochemistry is brimming with opportunity, Warren believes. She pointed out that because microbes are widely distributed on Earth--microorganisms have been found in even the harshest of environments, including deep-sea hydrothermal vents, toxic abandoned mine sites, and even deep under Earth's surface--their influence is likely to be profound. "We are only just beginning to scratch the surface of microbes' role in geochemistry."

Top