Transforming heme proteins into solar driven redox catalysts by site-directed zinc porphyrin mutation.
All forms of life have ways to move electrons, and doing so is a key that allows our bodies to convert and manipulate energy. In his proposed Scialog work, Sean Elliott and his associates are studying microorganisms with the remarkable ability to interface with solid surfaces, and move electrical charge to those surfaces—exactly what you’d want to have in a biologically based fuel cell. (Invented in 1854 by British physicist William Robert Grove, a fuel cell is a device that converts chemical energy directly into electrical energy.) Elliott is focusing on a group of proteins that contain iron—and a lot of it!—called cytochromes. They’re responsible for the internal electrical wiring within the cell, and they’re largely responsible for the movement of electrons, or an electrical current, from one compartment to another, from the inside to the outside of the cell. He is tinkering with the cytochromes found in very a hardy and robust bacterium called Shewanella oneidensis. “Shewanella possesses not just cytochromes, but what are referred to as ‘multi-heme cytochromes,’” Elliott says. “These are proteins that have many units of iron in them that collectively form, if you will, a wire that passes the charge from the cellular interior to the exterior.” He adds that many scientists are very interested in Shewanella, and there’s a lot of work going on in his lab and in many others, trying to understand the relative contributions of one electron pathway versus other pathways, and exactly what the constituents are of that pathway to use charge. As part of his Scialog grant, however, Elliott and his group will be taking that work to the cutting edge by attempting to design a way to make Shewanella proteins capable of harnessing energy from light. “The end result, we hope, will be a new strain of Shewanella that will retain the fantastic ability to interact with electrodes, but will be light activated and capable of transforming the light from the sun into useful chemical fuels,” Elliott says. What especially fascinates Elliott about Shewanella is what the bacterium can “breathe.” Most people may not realize it, but when we breathe, the oxygen our lungs take in eventually goes into our cells where it’s used as what chemists refer to as an electron receptor. The electrons the oxygen molecule receives are the result of much of our other metabolic processes. The same is true for the oxygen atoms that a bacterium like Shewanella takes in. “Just like we breathe oxygen and then reduce it – that is, we add electrons to it to make water, at least that’s part of what we do with oxygen—an organism like Shewanella can use oxygen, or it can grow in other ways where it doesn’t have oxygen,” he says. “And so it’s also able to breathe, if you will, something else.” In fact, Elliott says, Shewanella is capable of “breathing” metals. “What is very remarkable is that it has this capacity to interact directly with metal oxide surfaces and mineral surfaces, and colonize them and use those insoluble materials – those materials that could be mineral in nature, or that could be an electrode in a microbial fuel cell – and pass charge directly to those materials as part of its breathing operation.” Elliott’s project involves a complicated dance – he’s working at the molecular level, trying to understand the nature of the cytochrome protein molecules, but he also has to pay attention to the biology of the bacteria – how does it work as an organism, how can it be encouraged to grow and thrive and to do the kind of chemistry he hopes it will do. “Our greatest innovative contribution is our understanding of what places within the Shewanella wiring are the most likely to yield positive results,” he says. “However, manipulating the organism in a useful way that will yield our desired result, and not just make the bug sick, is the greatest challenge we face.” The better Elliott and his colleagues understand how the organism works, the better “we can exploit it in any kind of device,” he says, whether it be to convert sunlight directly into electricity, or using it to produce liquid fuel, something other researchers have been exploring with algae. Although Elliott thinks the Shewanella bacterium has some advantages over algae. “Frankly, it’s a simpler beast than algae. It’s just a microbial organism, it’s called a prokaryotic organism (versus a eukaryotic organism). It has a smaller genome; it has smaller parts; it has fewer compartments than algae. There are things about it that make it very good from the standpoint of its unique ability to interact with electrode surfaces.” Luckily, he believes he already has a fairly good understanding of how Shewanella works, and he and his colleagues across several disciplines of science have developed a list of targets that they can go after in a systematic way. “Collaboration is utterly essential for us,” Elliott says. “In our proposal we are at the frontline of work that requires cross-disciplinary efforts—we work with X-ray crystallographers to develop molecular ‘snapshots’ of the structures of the individual cytochromes of interest to us, so we can both understand the charge-transfer elements of these proteins, but also how they may work together within the cell; we work with experts in photophysics and photochemistry to be able to measure light-induced charge- transfer processes; and we need interactions with microbiologists who are learning more about Shewanella and other related microorganisms every day.” Does Elliott, a chemist, think this work is pretty far-out for someone in his field? “Well, I’d say that the world of chemistry is definitely expanding its view, such that this is not hugely far-out,” he says. “Although it definitely falls into the scope of the high-risk/potentially high-reward project, there’s no question about that…The bottom line, though, is that chemistry is looking in lots of new places. And those places do tend to be very cross-disciplinary, particularly with the biological sciences. So I don’t think of this project as being totally crazy, or really out there. Although it is risky and there is certainly no guarantee for that ultimate application, that ultimate success.” If the project “fails,” he adds, “we will still learn about how biology moves electrons through the wiring of multi-heme cytochromes. It may be that the model organism that we have chosen is not the best one; but what we will learn about how to manipulate charge transfer and tailor the bioenergetic pathways of microbes will be widely useful, and may be applicable to other organisms (microbes, plants, algae) that will, one day, be part of the biological solutions that are applied to challenges in the energy sciences.” Elliott adds that high-risk/potentially high-reward work is intellectually invigorating, genuinely stimulating, and more than a touch nerve-wracking. “To some extent, one has to turn-off the natural inclination, as a scientist, to be critical and skeptical: you are forcing yourself to think about ideas that may not yield positive results, but would lead to tremendous strides forward if they actually do. As such, you are pulled in two directions at once—a strong desire to reach heights of illumination like Icarus, and the grounding pull of critical thinking and tried-and-true science. It’s an exciting space to occupy intellectually.”