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Summary of Key Breakout Discussion Topics

Workshop participants met in three different breakout discussion groups during the course of the workshop. Each topical session of the workshop included a breakout discussion and a report-back time. The smaller size groups in the breakout sessions allowed for more in-depth and interactive discussion between workshop participants. The composition of the discussion groups was multidisciplinary and was meant to provide feedback to the larger group on key issues raised or important information provided by the guest speakers; research opportunities, especially for interdisciplinary collaborations; and resource and educational needs to support long-term advances. The key topics of discussion that came out of the breakout sessions (as reported back to all workshop participants) are described in detail in this chapter, and they are organized into the following general areas:

  • Defining “bioinspired”;
  • Microbial diversity and setting priorities;
  • Research and collaborative models;
  • Interdisciplinary education, training, and outreach;
  • Microbial nanowires and fuel cells;
  • Synthetic biology; and
  • The big picture.

The key topics discussed in the following sections were suggested by breakout group participants, who were not vetted for conflicts of interest



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3 Summary of Key Breakout Discussion Topics Workshop participants met in three different breakout discussion groups during the course of the workshop. Each topical session of the workshop included a breakout discussion and a report-back time. The smaller size groups in the breakout sessions allowed for more in-depth and interactive discussion between workshop participants. The composi - tion of the discussion groups was multidisciplinary and was meant to provide feedback to the larger group on key issues raised or important information provided by the guest speakers; research opportunities, espe- cially for interdisciplinary collaborations; and resource and educational needs to support long-term advances. The key topics of discussion that came out of the breakout sessions (as reported back to all workshop par- ticipants) are described in detail in this chapter, and they are organized into the following general areas: • Defining “bioinspired”; • Microbial diversity and setting priorities; • Research and collaborative models; • Interdisciplinary education, training, and outreach; • Microbial nanowires and fuel cells; • Synthetic biology; and • The big picture. The key topics discussed in the following sections were suggested by breakout group participants, who were not vetted for conflicts of interest 33

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34 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY or biases, and they therefore do not represent conclusions or recommen - dations of the workshop organizing committee or the National Research Council. DEFINING “BIOINPIRED” Given the diverse disciplinary backgrounds of the workshop partici - pants, a key question raised was “what does bioinspired mean?” Mimicry Versus Inspiration The term “bioinspired” is often used interchangeably with the term “biomimicry.” However, biomimicry really means to copy or recreate nat- ural systems, whereas bioinspired is about learning from nature to make something new. One participant explained that bioinspired really means to deeply understand the biological system being studied. Only when the biology is understood at the most fundamental level will it be possible to redesign it and create a better system. Artificial systems are desired over natural systems because biological systems often contain extra “baggage” (i.e., components that are useful for the organism, but not necessarily for the desired application function). Although there are advantages to natu - ral systems—for example, proteins can be excellent catalysts in the form of enzymes—they tend to have limitations. In the cell, enzymes need to compete with many other substrates. Cells spend a lot of time and energy trying to engineer specificity, which may or may not be needed for energy applications. In most cases, much of the natural structure is probably not needed in artificial systems. The specificity may not be needed where the enzyme can be artificially inundated with a large amount of substrate. One example discussed by some workshop participants is nitroge - nase, which is a very important nitrogen-fixing enzyme related to both agriculture and energy. James Liao noted that about 5 percent of the energy used in the world is spent in the synthetic nitrogen-fixing Haber process (catalytic reaction of hydrogen and nitrogen to produce ammonia) (Smith, 2002). Unfortunately, nitrogenase cannot currently serve as an alternative method for large-scale nitrogen fixation to compete with the Haber process. The enzyme utilizes a very complicated process, involving 16 adenosine triphosphates and many electrons. Despite all the efforts to study nitrogenases for many decades, the mechanism of the enzyme is still unknown. Liao said that if someone could understand nitrogenase better or design an artificial enzyme based on or inspired by nitrogenase, it could be a major contribution to reducing the amount of energy used in the world for nitrogen fixation. Many participants considered biomimicry to be a nearly impossible

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35 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS goal to achieve. For example, trying to mimic the relatively simple bacteri- orhodopsin photosystem—or even just its photosynthetic center—seemed virtually impossible. There would be a long way to go to reach the point of being able to recreate or mimic even such a simple system. Complete Understanding of Biological Systems Another group reported back that a complete understanding of bio- logical systems is needed to inform the development of synthetic systems. Janet Westpheling quoted Richard Feynman, who once said, “What I can- not create, I do not understand” (Feynman, 1988). However, it was not clear to many participants that successful creation of synthetic systems informed by design principles from nature will be significantly better than what nature itself has evolved. For example, Penelope Boston noted that a great deal of innovation has gone forward without that deep understand- ing and that, in fact, the very act of innovating and engineering design solutions has actually pushed the science in some fields. Tom Moore added that although a deep and complete understanding is the goal, it is not a prerequisite for moving forward on new ideas. Chemically Inspired Microbiology A participant suggested that the group should also talk about “chemi- cally inspired microbiology”—that is, using chemical knowledge to drive biological exploration. Participants highlighted two examples of biologi - cal discoveries made because of chemical insights. Karl Stetter,1 who often worked with biogeochemists, used his chemical insight to isolate novel microorganisms. Georg Fuchs2 similarly used his chemical knowledge in discovering novel autotrophic CO2-fixation pathways. In Fuchs’ case, the genomes of the organisms found were already known, but people did not know to look for the chemical pathways. References Feynman, R. 1988. en.wikiquote.org: On his blackboard at time of death in 1988; as quoted in The Universe in a Nutshell by Stephen Hawking. Smith, B. E. 2002. Nitrogenase reveals its inner secrets. Science 297(5587):1654-1655. 1 For more information, see http://www.biologie.uni-regensburg.de/Mikrobio/Stetter/ (accessed September 1, 2011). 2 For more information, see http://portal.uni-freiburg.de/ag-fuchs (accessed December 21, 2011).

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36 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY MICROBIAL DIVERSITY AND SETTING PRIORITIES Some participants noted that many of the speaker talks illustrated how biology provides a diversity of energy solutions; however, it is not always clear how to apply that diversity to meet human needs. Some - times the diversity is so great that it is almost paralyzing for the research community. Since it is possible to culture about 1 percent of the microbial biota on Earth (Pace, 2009), and “only about 10 percent of the kinds of organisms on Earth are known” (Wilson, 2006), there is enormous bio- logical diversity that is untapped. However, some participants questioned whether there should be much investment in culturing these organisms. Prioritizing the approaches for bioinspired energy may be needed. Ques- tions to be addressed include • What is most important to study in biology, and how can that be determined? • Which aspects should be applied to the energy problems? • What exactly does “bioenergy” mean? — Is it biomass? Is it solar? Or is it a combination of many different forms of energy transformation using biological components? Westpheling explained that right now it is hard to design a path because the “there” is unknown. She said that one of the challenges is defining the destination, before the science and technology can be developed. Thus, many participants said that there is a need to carefully identify the really important energy transformation problems and make sure that there is a potential biological solution to the challenges being addressed. For example, cost efficiency might be considered, or perhaps carbon- carbon bond formation and its importance to energy storage. Culturing Bacteria Penelope Boston pointed out that culturing brings organisms into a state where they can actually be studied. She said that it is useful to know about all the genomic biodiversity, but the microbes can really only be studied and manipulated if they are cultured. Although it may not be necessary to culture everything, she said that it is necessary to culture the right ones that are of interest as model systems and have genetic talents that can be manifested for these uses. Westpheling agreed and added that because approximately 50 percent of predicted genes are understood, there is much progress that needs to be made.

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37 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS Conserved Microbe Functions Some participants noted that one way of prioritizing biological mod - els systems may be to consider the unknown and conserved hypothetical proteins that are available (Galperin and Koonin, 2004). The conserved hypothetical proteins are found across a wide array of organisms. Addi - tional culturing may aid in this understanding. Understanding the bio - chemistry of microbe functions is also critically important. Some partici - pants noted that it is not enough to know about the genomic sequence or array of proteins expressed—the chemistry of those proteins and what they can do also needs to be understood. Biological Dark Matter The related topic of genome annotation (attaching biological informa- tion to gene sequences) (Stein, 2001), or what Ken Nealson referred to as the “biological dark matter” of the genome, was also discussed by some workshop participants. Nealson said that there are many problems in annotation. It can lead people to believe in false assumptions, because of incorrect annotations. For example, as Janos Lanyi explained, changing a single amino acid residue in bacteriorhodopsin transforms it from a chloride pump to a proton pump. This would have never been discovered with annotations, because the genome sequence would not have provided such an insight. Another example Nealson gave was for related Crp-FNR DNA binding proteins,3 which he said are found in both Shewanella and Escherichia coli, but regulate in Shewanella opposite to what they do in E. coli. In Shewanella, FNR regulates sugar metabolism and Crp regulates anaerobic/aerobic response, whereas in E. coli the two are reversed. He said that even when a genome sequence is properly annotated for one organism, the annotation may not apply to the same genomic sequence in a different organism. This presents a big problem to be addressed. Living Systems Baggage Doug Ray mentioned that it has been found that organisms in extreme environments may have less biological “baggage.” For example, E. coli is considered to have more excess components than most other microbial organisms. He said that before concluding the nonutility of organisms because of baggage, it may be necessary to think a little more broadly about the organisms that are present and available. 3 Crp-FNR = Cyclic AMP (cAMP) receptor protein (Crp)/fumarate nitrate reductase (FNR) regulator. For more information, see Körner et al. (2003).

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38 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY Following Environmental Clues Julie Maupin-Furlow pointed out that the work of Rolf Thauer, and an understanding of the redox environment in nature, can drive an approach to isolate organisms. She said microbiologists often do not take such an approach and biological information is missed, because some research- ers address the wrong problem. As Thauer mentioned, many researchers presumed the anaerobic oxidation of methane (AOM) to methanol was not occurring because the CH bond in methane is one of the strongest aliphatic CH bonds. Fortunately, Thauer and other biogeochemists probed further and challenged the dogma of the time, and showed that AOM was occurring. This highlights the importance of bringing in people from one field to challenge those in other fields. Maupin-Furlow said some might call what Thauer did “microbiology myth busters.” Some participants also talked about looking at energy-limited sys - tems for inspiration, such as methanogens. Such systems utilize very little energy. The efficiency of enzymes that are catalyzing reactions in such systems are very different when compared with the enzymes involved in photosynthesis, in which there is typically excess energy, such as the “RuBisCo” (ribulose bisphosphate carboxylase/oxygenase) enzyme sys - tem in plants. Reversible Processes Some participants noted that it is a thermodynamic paradigm that says a reversible process is the most efficient process. Some mainstream biological processes are reversible, including those that generate proton- motive force. However, some key enzymes involved in energy transfor- mations are irreversible, including redox enzymes. The opportunity for rational design of redox cofactors, particularly with respect to reversibil - ity, might offer ways to understand natural systems better and perhaps to devise systems that could meet the energy requirements of humans. Matching the Solar Spectrum Tom Moore brought up the solar spectrum and photosynthesis. He said photosynthetic chemical work is not well matched to the solar spec - trum. The photons in the blue region of the spectrum are much more energy-rich than those in the red region of the spectrum, but photosyn - thesis degrades all the photons to the red region of the spectrum. Human technology offers opportunities to incorporate some of the multijunction features into biological systems, although this has not been done yet.

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39 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS Nutrient Cycles James Liao pointed out that making the nitrogen cycle more efficient has also been largely ignored. A lot of focus has been on understanding the carbon cycle, but the nitrogen cycle is equally important. It consumes energy and contributes to the greenhouse effect dramatically. Liao also said there are at least four different CO2-fixation cycles found in biological systems (Thauer, 2007). He said that those are impor- tant cycles, but the challenge for scientists is to do better. So far, to his knowledge, no one has even proposed an artificial working cycle that fixes CO2 in a biological setting. References Galperin, M. Y., and E. V. Koonin. 2004. “Conserved hypothetical” proteins: Prioritization of targets for experimental study. Nucleic Acids Res. 32(18):5452-5463. Körner, H., H. J. Sofia, and W. G. Zumft. 2003. Phylogeny of the bacterial superfamily of Crp-FNR transcription regulators: Exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol. Rev. 27(5):559-592. Pace, N. R. 2009. Mapping the tree of life: Progress and prospects. Microbiol. Mol. Biol. Rev. 73(4):565-576. The original reference actually appears to be Rappé, M. S., and S. J. Giovannoni. 2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369-394. Stein, L. 2001. Genome annotation: From sequence to biology. Nat. Rev. Genet. 2:493-503. Thauer, R. K. 2007. The fifth pathway of carbon fixation. Science 318(5857):1732-1733. Wilson, E. O., 2006. Explorers Club Speech, March 18. http://www.eowilson.org/index. php?option=com_content&task=view&id=75&Itemid=32. RESEARCH AND COLLABORATIVE MODELS Workshop participants discussed what is needed to support research in bioinspired energy. Importance of Discovery Science Julie Maupin-Furlow said that a lot of time in one of the breakout ses - sions was spent discussing task-oriented versus discovery-based and fun- damental research. Many in the group felt that it is important to balance discovery-based findings with hypothesis-driven projects. She stressed the need for balance. Doug Ray also commented that developing and testing a hypothesis is important, but it needs to be done in conjunction with discovery or exploratory science. There is some sense that it is not possible to get fund- ing for discovery science. It is important to balance the two—not to the exclusion of each other. Janet Westpheling pointed out that once a promising biological sys- tem is discovered, there is then a need for public and private research

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40 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY institutes to provide a model for how to transition from academic discov- ery to commercial development. There seems to be a gap between basic science and the application of the basic science that needs to be filled. Some participants suggested the national laboratories as one possibility. Other models discussed included the following: IBM model. A participant who worked with IBM Research said one problem they faced was incorporating findings from the research labo- ratory into products. One successful approach was to have the people who were designing the technology to be on the implementation team. However, that can require an entirely new personnel and communication system. Pharmaceutical company model. Janet Westpheling said that the model followed in large-scale pharmaceutical companies can also be effective. She worked for a pharmaceutical company and was involved in develop- ing products from biological systems. They would have product meetings with different teams focused on everything from the research develop - ment of the organism that made the product, to the people who bought the raw materials that went into the fermentation, to the engineers, to the marketing people. No one would conduct an experiment that could not be carried out in practice in an industrial setting. Another participant added that these transformations in the pharmaceutical companies started in the 1980s and took time to show results. There had to be an effective collaborative team. Bell Labs model. Greg Petsko discussed the Bell Labs model, where some people did basic research and other people did applied research, all in the same building. A participant mentioned how Steve Chu, the Secretary of Energy, refers to the model in almost every speech he gives. Chu worked at Bell Labs for 6 years, and he often talks about how he wants to use the model for Department of Energy (DOE) labs (Chu, 2009; Morford, 2009). However, some questioned whether this model can still work in contemporary times. It may not be possible to hire the same type of talented people and give them freedom to experiment. Now, results are expected in a much shorter time frame—on the order of months, not years. DOE bioenergy centers. Westpheling argued that it is not always neces- sary to be in the same building for effective collaboration to occur. She is now part of the DOE-funded Bioenergy Science Center that is led by Oak Ridge National Laboratory. It is a virtual center that brings together people from all over the country. She said that it is not always feasible to bring together the equipment and the expertise in one place, or to get people to move to the same city to be involved in the same work. This

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41 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS is another model of reaching out to the larger community that has been shown to work. References Chu, S. 2009. Testimony before the Senate Committee on Appropriations, Subcommittee on Energy and Water Development, and Related Agencies, May 19, 2009 [online]. Avail - able: http://energy.gov/congressional/congressional-testimony-2011/congressional- testimony-2009 (accessed Sept. 22, 2011). Morford, S. 2009. Chu: DOE taking lead on renewables, looking for the next Bell Labs. Inside Climate News, April 7, 2009 [online]. Available: http://solveclimatenews.com/ news/20090407/chu-doe-taking-lead-renewables-looking-next-bell-labs (accessed Sept. 22, 2011). INTERDISCIPLINARY EDUCATION, TRAINING, AND OUTREACH Given the interdisciplinary nature of bioinspired research, many participants spent a lot of time talking about interdisciplinary training, or simply approaching their research in an interdisciplinary way. Many people in the group felt that it is most important to have the core curricu - lum intact and then, once there is a biological problem or a problem that needs to be solved, drive interdisciplinary work. Janet Westpheling added that while interdisciplinary training of sci- entists is critical, there is concern about how it can be done without “watering down” the individual disciplines. Effective Communication Many participants noted that interdisciplinary education, training, and outreach are needed so that efforts in bioinspired energy can be effec- tively communicated. Energy has been compared to the space program. Everyone supported the idea of the space program, because putting a man on the Moon was an exciting proposal. But that kind of enthusiasm is currently not there for energy—even though energy might be an equally important or even more important goal as going to the Moon. Outreach to the general public is an important aspect of effective communication. Because the participants came from many different disciplines, there was a lot of discussion about disciplinary language differences, and how to make that communication more efficient. Someone suggested that per- haps a workshop for workshops is needed—to explore how groups can learn each other’s disciplinary language to enable more efficient com - munication. Without making some improvements in communication, sci-

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42 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY entists may be unable to effectively speak with one another about their work. One participant commented on the need to effectively communicate about energy research to the general public and to the funding agencies. He said the message should be that studying biological energy systems is the most fundamental and basic research that can be done on the planet. It is the findings and rational design principles based on physics and chemistry that are going to underpin synthetic biology—if nine billion people are going to be supported on the planet, some fundamentally new approaches in energy are needed. Cross-Disciplinary Research and Training Ken Nealson commented on cross-disciplinary training efforts, espe - cially the positive impact he has witnessed in interdisciplinary summer courses. He said there is a huge transformation that happens to students during these summer courses. If the course is taught effectively, the stu - dents are exposed to many different disciplines. He now teaches a course in geobiology and previously taught one in the past on planetary biology, which involved isotope chemists, organic chemists, and microbiologists. In the course, he lectured and conducted labs with the students. He saw interdisciplinary workers emerge from these courses; they did not have to take a course in interdisciplinary science—they had to see how exciting it was. He said this was an effective way for funding agencies to invest in the future. It was a 10-year time period (largely during the 1980s) (Nealson and Nealson, 1993) when the National Aeronautics and Space Administration (NASA) funded the Planetary Biology and Microbial Ecol- ogy program. Nealson said that many current rising stars in the field (including speaker Felisa Wolfe-Simon) attended those summer courses. He encour- aged funding agencies to continue to support these successful interdisci- plinary courses, which offer a great opportunity for the next generation. Wolfe-Simon added that the United States also needs centers that foster interdisciplinary work—especially for the up-and-coming researchers, who need to be supported and given freedom to explore. She added that while she is a fan of new media, there are significant advantages to being able to walk down the hallway or the next building to talk about research with a colleague in astronomy or engineering. Skype does not provide that type of interaction. She does not know what might be the mechanism for creating the centers, but she said this country needs a place where an early-career scientist has some freedom to do science, because research faculty members are often overwhelmed by large teaching loads, com - mittee memberships, or other responsibilities.

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43 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS Many participants discussed how it may take a combination of activi- ties, centers, summer courses, and people visiting different labs, with funding from multiple agencies to support the interdisciplinary research and educational needs. Current Opportunities Robert Stack described current DOE support for the microbial ecology summer school at Woods Hole.4 It is a 6-week summer class, which does exactly what Nealson and Wolfe-Simon discussed. The class is funded jointly by the DOE Biological and Environmental Research program and the Basic Energy Sciencesprogram, the NASA Astrobiology program, and the National Science Foundation. However, he said that it is a very expen- sive class, given that only 20 students take the course each year. There is a principal investigator for the class that rotates every 3 to 5 years, and the instructors change. Stack said DOE also often puts together workshops to achieve similar goals. They try hard to build interdisciplinary working relationships by holding annual or biannual contractor meetings. For example, every - one funded by his program in physical biosciences meets every 2 years. It includes everyone from chemists, to x-ray crystallographers, electron paramagnetic resonance spectroscopists, molecular biologists, and micro- bial ecologists. DOE also provides seed money to people who have great new ideas. The group discussed the value of this workshop and the need for more in which a variety of kinds of expertise are brought together to address a common theme. Reference Nealson, M. S., and K. H. Nealson, eds. 1993. Planetary Biology and Microbial Ecol - ogy: Molecular Ecology and the Global Nitrogen Cycle. NASA Contractor Report 4497 [online]. Available: http://ntrs.nasa.gov/archive/nasa/casi.ntrs.nasa.gov/ 19930016968_1993016968.pdf (accessed Aug. 30, 2011). SYNTHETIC BIOLOGY Many participants talked about how to use the molecules that are discovered in biological systems, such as the photoactive chromophore of bacteriorhodopsin in harvesting energy. Bacteriorhodopsin is a very 4 Microbial Diversity Summer Course at Woods Hole [online]. Available: http://www. mbl.edu/education/courses/summer/course_micro_div.html and http://courses.mbl. edu/microbialdiversity/ (accessed Sept. 22, 2011).

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44 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY successful system for converting photoenergy to proton-motive force. However, it is not clear how this proton-motive force can be used in an energy production system on a large scale. Some participants asked what might be done to understand this system better. For example, are there synthetic analogs of the transformation in retinal? Is there any way to sim- plify the system so that protons can be pumped on a large scale? Instead of limiting it to the cell membrane, can the system be designed on a large enough scale to harness this energy? Rational Design of Proteins As Les Dutton indicated, it is possible through rational design to think about creating synthetic electron transfer proteins and components of future synthetic biology systems. Dutton also mentioned that it is important to focus on the rational design of proton transfer systems— proton pumps or proton-transfer-linked transducers that can run in two directions. In one direction, these proton-transfer systems would pump protons against a proton electrochemical gradient, and in the other direc - tion, they would do some work, chemical or mechanical, by transducing protons back across the system. Tom Moore said that, right now, no one really has an idea of how to rationally design a proton pump. He pointed out that it is important to remember that biology never operates without the combination of proton-motive force and electromotive force. However, the progress on understanding the two systems is uneven. A lot is understood about the fundamentals of electron transfer systems, but not as much is known about proton transfer. Moore said protons offer an incredibly rich research area, because protons are, in a sense, between classical and quantum mechanical particles. Sometimes their motion is not limited by mass transport considerations. Proton wires exist and, under short distances, protons can tunnel. Thus, he said that it is hoped that the environment for research in proton-motive force, particularly synthetic and artificial systems to generate proton-motive force and then couple that proton-motive force to either chemical or mechanical work, will increase in the future. There was some discussion among participants about defining syn- thetic biology. Westpheling said that she thought the group meant it as the synthesis of microbial functions. Tom Moore added that he thinks it is an unlimited definition, because right now the field is open and no one knows where synthetic biology can lead. He said that if someone asked Bardeen to define the transistor in 1948, he probably would have given a similarly broad answer regarding semiconductor physics. Looking ahead, they knew they had to go somewhere that vacuum tubes could not take them, but it is worth noting that they did not have a path. They did not

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45 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS know where they were going. They just knew that they could not go there with vacuum tubes. The way they addressed that issue was to hire bright people and give them the freedom to explore. Moore said that it was the type of focused-up/diffused-down management and leadership that needs to be seen more. There was a discussion about what the role of synthetic biology will be in developing bioinspired systems going forward. Many in the group believe that it is probably a long way to go from de novo synthesis of a biological system to a useful application. Modifying known biological systems is probably a more productive approach in the short term. MICROBIAL NANOWIRES AND FUEL CELLS Ken Nealson’s talk about bacterial nanowires in Shewanella sparked a lot of discussion among participants about alternative electron transfer architectures, including the microbial synthesized nanowires (Gorby et al., 2006). There was a lot of interest in the ubiquity, or not, of nanowires and electrically conductive extracellular material in nature and what that might mean, how one might use that for different purposes. Moore commented that he thinks this is one of the most fascinating things that has been discovered in the last 10-15 years—how living organ- isms use the nanowires to remove electrons from the system. He said, “In removing electrons from their cells, they in a sense feed themselves reduced carbon, electron carriers, that then are taken up in nutrition.” The bacteria Nealson discussed in his presentation do the same thing. They take in an external source of reducing power of low-potential electrons and get rid of them, under conditions where other electron acceptors are not available. They move the electrons completely out of their cells through the nanowires. Moore noted that in order to keep charge balance, the bacteria also have to get rid of protons. Microbial Nanowires Les Dutton talked about how some researchers have incorporated the nanowires into artificial liposomal membranes and have studied electron transport within these systems. John Golbeck added that the idea of using long-distance microbial nanowires to connect one cell to another has great potential. He said that, right now, one of the problems in generating solar biofuels, such as making hydrogen, is that the electrons also need to come from water, which means that there is an oxygenic environment. The approach is to reduce protons with hydrogenase in an oxygenic environ - ment, but that is not going to be possible with the current approach of using a single cell.

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46 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY The wire enables a new approach, because now space and time are separated. For example, there could be an oxygenic environment in one cell connected with a wire and an anaerobic environment in another cell, completely separated in space. Having that separation opens totally new avenues to explore. He thinks that interest and advances in this wire technology are going to grow, but will require a lot of imagination for it to succeed. There needs to be more thinking done in terms of the sepa- ration of space and time, and the possibilities that presents for the next generation of fuels. Tom Moore agreed. He pointed out that Nealson actually demon- strated in his talk that he had an aerobic side and an anaerobic side hooked together with a wire. “So you can do the chemistry that tran- scends 2 billion years of evolution, from a non-oxygenic to an oxygenic— you can combine them both with a wire. Better than that, the wire is a biological wire. It’s just remarkable and fantastic, and wonderful to hear about,” said Moore. He added that Nealson’s work is a great illustration of successfully combining technology and natural systems to meet larger societal needs. Microbial Fuel Cells There was also a lot of discussion about uses of the nanowires, espe- cially in microbial fuel cells, which have real potential for distributed application and to save money and decrease energy. Doug Ray said that these are great examples, potentially, of so-called appropriate technologies. Moore talked about how microbial fuel cells could be deployed, even at this early stage, into the world, particularly Nealson’s water purifica - tion system. Moore thinks it is not too soon to think about putting these technologies out there. They have one huge advantage over deploying higher technology systems, in that the question of translating a high-tech energy conversion system into a very low-tech, underdeveloped environ- ment is challenging, for a number of reasons. For example, fuel cells and catalytic converters have a high risk of being stolen for their valuable materials. The advantage of the fuel cells that Nealson described in his talk is that they have no value except for what they do. The cells do not contain any valuable components such as metals, so they are less likely to be stolen. Yet, they can produce pure water.

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47 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS References Gorby, Y. A., S. Yanina, J. S. McLean, K. M. Rosso, D. Moyles, A. Dohnalkova, T. J. Beveridge, I. S. Chang, B. H. Kim, K. S. Kim, D. E. Culley, S. B. Reed, M. F. Romine, D. A. Saffarini, E. A. Hill, L. Shi, D. A. Elias, D. W. Kennedy, G. Pinchuk, K. Watanabe, S. Ishii, B. Logan, K. H. Nealson, and J. K. Fredrickson. 2006. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl. Acad. Sci. U.S.A. 103(30):11358-11363. THE BIG PICTURE Given the scale of energy needs, there was a lot of discussion about the ability of learning from biology to meet those needs. Many partici - pants asked, in the long run and in the big picture, will biology really contribute to energy versus bioenergy? Doug Ray said that scientists often neglect to consider the importance of cost and scale of working with biological systems. For example, in terms of the global energy system, electricity from coal costs 4 cents per kilowatt-hour. It is very hard for other energy sources to compete with that, which is why coal is burned. Beating that price point is a challenge for everyone to consider. Biology, Energy, and Sustainability John Golbeck said that, in at least the next couple of decades, the big place for biology to contribute to energy is in understanding necessary land-use changes. Thauer added that in their breakout group the discus- sion was not that biology cannot contribute anything, but how much can it contribute? He said it may be small (1 or 2 percent), or it may be larger (10 percent), or larger still (50 percent). The other question is: Can it be done sustainably? If fertilizers are used, N2O will be produced which is a 200-fold-times-more-efficient greenhouse gas than CO2. That is not going to be sustainable. Thauer said to consider his home country of Germany as an example. If Germany decided to take 100 percent of the area for agriculture and fertilize less—that might be more sustainable than devoting part of its land to make biofuels and continuing to fertilize. He said the numbers would be different for the United States. Germany has a population den - sity of 239 per square kilometer, whereas United States has 30 people per square kilometer, and so the two countries will need to approach biomass development very differently. He said that, on average, per person, the United States has more biomass, and so, in principle, more options than the Europeans. Judy Wall said her group also discussed the land-use issues high- lighted by Rolf Thauer. For example, if all the available surface of the Earth could be used for biomass production, what is the maximum energy

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48 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY that it might be able to generate? Wall said that there are estimates that it is about 20 terawatts per year. However, based on the current population on Earth, the estimated need for energy 50 years from now is about 40 to 50 terawatts. That presents a large energy deficit to begin with—without accounting for population growth and other factors such as the land needed for houses, roads, and cities. Additional land is also needed for food, as well as to preserve wild habitats. The need for food reduces the amount of available land by about 50 to 70 percent more. Then, there is the consideration to leave some natural environment. Wall also noted that a realistic contribution to energy from biomass is thus relatively small, on the order of perhaps 1 to 2 percent of the total budget. That raises the question then, is that large enough to worry about? She said yes, because the 1-2 percent translates into meeting the annual energy needs for somewhere between 3 million and 6 million people which is the size of a large city. Participants also discussed some of the current liquid biofuel production from cyanobacteria (Atsumi et al., 2009), which is making progress and looks as if it could make a significant con - tribution, on a per-hectare basis, relative to other biomass considerations as well. Wall said energy from biomass is not something to give up on, because every small contribution to that energy budget is going to be important. Another issue discussed among workshop participants is with large- scale production of commodity chemicals using microbes. This presents a promising alternative to using fossil fuels for chemicals. However, right now it is not feasible to use it on a large scale. A good approach for now is to start with making specialty chemicals and then develop into the more bulk commodity chemicals. Janet Westpheling commented that there has been at least one success in commodity chemicals. One of the real successes in metabolic engineer- ing in E. coli is to make succinic acid for plastic production. She said there are manufacturing plants being constructed in the United States for that purpose. The process used is based on Lonnie Ingram’s technology for making succinic acid in E. coli. This example illustrates that it is possible to economically use microbes to produce commodity-scale chemicals. Maupin-Furlow agreed, but said that, for newly developed systems by startup companies, often it is better to start with a high-value specialty chemical and then go bulk. She said projects do not always fully think about how difficult it can be to produce chemicals on bulk scales. It was mentioned that isolation of specific enzymes from microorgan - isms for specific applications is happening today. Several participants indicated that isolating and expressing enzymes is not much of a chal- lenge anymore. The real interest and challenge is understanding more

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49 SUMMARY OF KEY BREAKOUT DISCUSSION TOPICS complex, perhaps emergent properties of enzymes and figuring out how to take advantage of those in the energy applications. James Liao agreed that isolating enzymes from one organism and inserting into a foreign organism is a solved problem for the most part. He said that there is plenty of evidence of this in the current literature. However, he said that most people only demonstrate that the insertion produces a few micrograms or milligrams and call that a success. He said a microgram or milligram quantity is not going to burn in someone’s engine. The real challenge is not to just show an enzyme can be made, but that it can be done in a high-flux way. There needs to be a goal of more than discovering enzymes and expressing them in different organisms. Consideration also needs to be given to throughput and scale. Photosynthesis and Energy Storage Photosynthesis was discussed as the main source of sustainable energy for the future. Judy Wall said that there are three main issues with photosynthesis: harvesting the energy, storing the energy, and converting the energy. For harvesting, photosynthesis works well for nature’s pur- poses, but it is not as efficient as it could be for engineering devices for human needs. This is because Earth is not limited in light, for the most part, so it does not have to be particularly efficient. Thus, there is room to improve efficiency of the system. Photosynthesis also presents a biological contribution to energy stor- age. The primary approach to energy storage is batteries. One problem is that current battery technology depends a lot on rare earth elements. James Liao added that the battery is also not a highly efficient storage material because the energy density is low. However, he said that it appears that chemical bonds are the most efficient way to store energy. For example, carbon-carbon bond or carbon-hydrogen bond would probably be the most practical energy storage in the near future. To store energy in liquid fuel, particularly biologically derived liquid fuel, the carbon- carbon bond formation ability provided by biological systems is probably the most unique aspect of biology’s contribution to this energy problem. One concern brought up by a participant is the energy density in bio - logical products is also low, and will limit some of the applications. Also there are energy losses at every step away from the initial harvesting of light or energy. That has to be taken into consideration when looking to biology for inspiration for energy solutions.

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50 RESEARCH FRONTIERS IN BIOINSPIRED ENERGY The Human Element Aside from the many scientific and technological issues discussed in the workshop, many participants said that, in the end, much of what happens in the future will ultimately depend on the actions of humanity. Many of the existing technologies available today could at least partially solve some energy problems. However, some participants noted that the implementation of those technologies is often driven by large political or economic forces. Education was discussed as one way to address this issue. The impacts of lifestyle and energy use are also a huge factor in addressing the energy issue. Some participants asked: Should everything be left up to free markets, or does there need to be a set of stricter regula - tory policies? There was acknowledgment among many participants that societal values need to be influenced to change the way energy is used, and to understand the importance of conserving energy. A participant commented that “we have to be careful what we implement, because once we are set on a course, it may or may not be reversible.” For example, once U.S. farmers are paid subsidies to grow corn, will it be possible to go from corn ethanol to a different product? Reference Atsumi, S., W. Higashide, and J. C. Liao. 2009. Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat. Biotechnol. 27(12):1177-1180.