Santa Barbara, Calif.--A research team report findings that "have significant implications for the cycling of iron in the oceans," according to their article published in the Sept. 27 issue of Nature. Their experiments show that iron bound to siderophores (small molecules produced by bacteria and other micro-organisms) reacts to light. The authors state that this photoreacivity "is an important new concept in our understanding of how siderophores function in biological iron acquisition."
Bacteria with the exception of only two known species need iron to carry on enzymatic processes essential to their existence. In many areas of the ocean, other substances that marine bacteria need are plentiful, so iron is the limiting nutrient for their growth. Starve those bacteria of iron, and many types of bacteria produce small molecules or ligands that bind iron and are therefore called "siderophores" (Greek for "iron loving").
The membranes on the surface of bacteria have receptors for the iron-bound ligands, and scientists have determined that the bacterial production of siderophores enables the organism to acquire iron. The authors of the Nature paper have discovered a new aspect of that acquisition process for many marine bacteria and likely other marine micro-organisms.
The authors of "Photochemical Cycling of Iron in the Surface Ocean Mediated by Microbial Iron(III)-Binding Ligands" are all affiliated with the University of California. First author Katherine Barbeau, a postdoctoral fellow in the laboratory of UC Santa Barbara chemist Alison Butler, has this September assumed an assistant professorship at San Diego's Scripps Institution of Oceanography. In addition to Barbeau and Butler, the other two authors are Eden Rue, a postdoctoral fellow, and oceanographer Ken Bruland; both Rue and Bruland are affiliated with the Institute of Marine Sciences at UC Santa Cruz.
Rue and Bruland and two other research teams have previously shown that the iron "in the upper oceans occurs almost entirely in the form of complexes with strong organic ligands presumed to be of biological origin," according to the Sept. 27 Nature paper. Some of these organic ligands may be siderophores produced by marine bacteria. The bond of iron [as iron(III)] to oxygen in siderophores is among the strongest possible molecular configurations of iron and oxygen. The marine siderophores studied by Butler's group are amphiphilic peptides, meaning that the peptide head of the two-sided molecule is attracted to water and the tail to fatty substances.
"The question we asked," said Butler, "is 'Are these siderophore-iron complexes photochemically reactive, and if so how does that affect iron availability to marine organisms?'" Subsequent research demonstrated that exposure to light not only results in the temporary reduction of iron(III) to iron(II), but in the dropping of the fatty-acid-loving tail of the siderophore ligand, thereby leaving the peptide head bound to iron. "Possibly the dropping of the tail," said Butler, "coincident with the reduction of iron(III) to the more readily usable iron(II) enables the bacteria to acquire more easily the essential iron."
To test this hypothesis Barbeau acquired a sample of ocean water off Bermuda in the mid North Atlantic. Said Barbeau, "We wanted to get our water with micro-organisms from the open ocean, where levels of dissolved organic carbon and iron are relatively low. In such a place the processes we are studying--bacterial acquisition of iron through production of siderophores--may be especially important." Barbeau incubated her water sample with added siderophore-iron complexes, looking for an effect of sunlight on the uptake of iron by the native biological community. Results clearly demonstrated that the effects of light on the iron-ligand complexes increased the biological availability of iron, adding a significant new dimension to our understanding of the oceanic iron cycle.
"The way iron cycles in the oceans is important because it affects the carbon cycle," said Bruland.
Back in the late 80's/early '90s, scientists asked whether fertilizing the oceans with iron would stimulate the growth of plant life that consumes carbon dioxide and thereby counteracts global warming. So experiments were conducted in which iron was added from ships into surface waters of the open ocean. In the wake of the seeded iron, phytoplankton indeed bloomed profusely but only for a short while. Reading about this effort in the Los Angles Times provoked Butler to begin to investigate how oceanic microorganisms acquire iron; these investigations, in turn, led her to team up with the Santa Cruz researchers and to conceive the experiments reported in Nature.
Iron is an essential and limiting element for growth not only of marine bacteria but other minute life forms that populate the ocean surfaces. "Understanding the uptake of this scarce micro-nutrient will," said Bruland, "help provide more insight into how these microscopic plants and bacteria cope in these oceanic environments. For example, the photochemical cycling described in this paper can make what would have been an unavailable form of iron into an available form for some micro-organisms."
In addition to being a chemistry professor at Santa Barbara, Butler is associate dean for bioengineering in the College of Engineering, and a participant in the California NanoSystems Institute (CNSI). Her research group published a paper in Science in February 2000 which showed that the ligands that bind iron can form vesicles about 100 nanometers in diameter--essentially a fat sheath lined on the inside and outside with the water-loving head groups.
In July Butler addressed the NanoSystems group at UCSB and envisioned possibilities that emerge from combining implications of the research findings reported separately in Science and in Nature.
"If you have a vesicle," said Butler, "you can trap something in it. Now we know that if you shine light on these ligands, they lose their fatty acid tales. That leaves us with tantalizing possibilities. One can presumably open up this little sphere of molecules by shining light on it. So there is the possibility of using these ligands as a drug delivery system within the body. And perhaps we can use these vesicles as reaction vessels in which we can make different nanoscale particles."
The Environmental Molecular Science Institute at Princeton University, called the Center for Environmental BioInorganic Chemistry (CEBIC), supported jointly by the National Science Foundation and the Department of Energy, funded the research reported in Nature. Through its NanoScale Interdisciplinary Research Team program, the National Science Foundation has also funded a large-scale bioengineering research project at UCSB headed by Engineering Dean Matthew Tirrell. That grant will enable Butler to explore the tantalizing possibilities for applications that she has envisioned.