|Home | About | Journals | Submit | Contact Us | Français|
The DOE BioEnergy Science Center has operated as a virtual center with multiple partners for a decade targeting overcoming biomass recalcitrance. BESC has redefined biomass recalcitrance from an observable phenotype to a better understood and manipulatable fundamental and operational property. These manipulations are the result of deeper biological understanding and can be combined with other advanced biotechnology improvements in biomass conversion to improve bioenergy processes and markets. This article provides an overview of key accomplishments in overcoming recalcitrance via better plants, better microbes, and better tools and combinations. A perspective on the aspects of successful center operation is presented.
Biomass recalcitrance—the resistance of plants to release their sugars for fermentation or upgrading—is a primary barrier to efficient and economical production of advanced biofuels [1, 2]. Overcoming and understanding recalcitrance was the unifying vision of the US Department of Energy (DOE) BioEnergy Science Center (BESC), now in its final and 10th year of operation. The mission of BESC was “to enable the emergence of a sustainable cellulosic biofuels industry by leading advances in science and science-based innovation resulting in removal of recalcitrance as an economic barrier to cost-effective production of biofuels .” Due to advances in biotechnology, BESC believed that biological solutions were the most promising path by which to achieve these breakthroughs. In response to a DOE challenge , Oak Ridge National Laboratory (ORNL) led the formation of BESC by gathering experienced researchers from multiple US institutions, who had been separately interested in separate aspects of overcoming biomass recalcitrance targeting advanced biofuels and specifically cellulosic ethanol.
Recalcitrance began as an operationally defined phenotype. With both applied and fundamental goals, BESC perceived that we needed to transform the understanding of recalcitrance; this required detailed knowledge of the chemical, structural, and physical properties of biomass and how these properties influenced deconstruction by enzymes and thermophilic microorganisms. This search led to altering plant cell wall properties by manipulating key plant polymer biosynthetic pathways, which led to studies of the interactions of the plant cell walls and the enzymes and microbes during deconstruction and fermentation. The BESC team has redefined recalcitrance so that now recalcitrance is on the path to being an understandable and manipulatable set of properties based on cell wall formation and bioconversion. A key outcome of the BESC team’s approach was to transform understanding in both fundamental and operational impacts to strategies that will eliminate recalcitrance as an economic barrier to commercialization.
This singular focus on recalcitrance science was BESC’s hallmark worldwide. BESC was organized into three areas: Biomass Formation and Modification, Biomass Deconstruction and Conversion, and Enabling Technologies (Fig. 1). All three areas included both fundamental understanding and complementary proof-of-concept components. Our ability to design, conduct, and analyze wide-ranging campaigns, along with our effective communications and capacity to integrate cross-disciplinary teams within the BESC organization, has been key to our success in scientific areas that are critical to overcoming the formidable biological and technological barriers that biomass recalcitrance presents.
From late 2007 to fall 2017, BESC published more than 945 journal articles, 10% in high-profile journals (impact factor > 9) and advanced the education of more than 230 professionals, who are now productive members of the bioeconomy workforce. More details with respect to the output of BESC and the other two USDOE Bioenergy Research Centers are in Slater et al. .
Populus and switchgrass (Panicum virgatum) were the chosen feedstocks for studies of cell wall-related genetic modifications that could impact recalcitrance and inform understanding. Both are high yield perennials recognized as potential domestic biofeedstocks [4, 6]. Populus was the first sequenced woody feedstock . Switchgrass is a native herbaceous perennial that could grow on marginal land. Both were deemed tractable for studies aimed at determining the basis of, and ameliorating, recalcitrance. Key advances in biomass formation led by BESC include:
One-step Consolidated Bioprocessing (CBP) without added enzymes  was the central focus of BESC’s work in the conversion area, which featured both fundamental and applied components. BESC initially focused on two approaches (a) improving product formation in thermophilic cellulolytic bacteria (primarily Clostridium thermocellum and Caldicellulosiruptor bescii), and (b) conferring to yeasts the ability to ferment cellulose by virtue of heterologous expression of glycosyl hydrolases. We came to regard the former approach as more promising and by the end of BESC were focused exclusively on this path. Key conversion advances led by BESC included:
Enabling technologies were organized to develop and apply cutting-edge analytical methodologies to characterize biomass as well as its conversion. There was also significant omics and computational biology of the modified plants and microbes to help improve metabolic models. The resulting data were used to create new insights into how biomass structure and chemistry affect recalcitrance during CBP or pretreatment. These efforts included analyses of partially digested solid residues from CBP.
As a thematically rather than institutionally defined center, BESC recognized early on the need to develop a shared organizing vision, a sense of priority, and strong mechanisms for shared samples and data as well as strong management. This structure allowed us to recruit many of the nation’s experts in recalcitrance and to draw on the intellectual cultures and strengths of different institutions. BESC successfully implemented a flexible management approach, modeled after successful biotech startup companies that have relied on academic research to strengthen their science base and industrial partnerships to translate discoveries into commercial products.
Over the decade, BESC established a distinctive, high functioning collaborative team with participants from 22 institutions and a broad range of disciplines. As needs and research progressed, six partners left the center and five new partners joined. BESC included researchers from universities, national laboratories, and private companies. These partners included major efforts at ORNL, University of Georgia, Athens, and the National Renewable Energy Laboratory. Specialized expertise was provided by Dartmouth College, Georgia Tech, University of Tennessee, Knoxville, Cornell University, West Virginia University, University of California-Riverside, University of California-Los Angeles, North Carolina State University, University of North Texas along with The Samuel Roberts Noble Foundation (Noble). Earlier partners included Brookhaven National Laboratory, University of Minnesota, Washington State University, and Virginia Polytechnic Institute. Our industrial partners included DuPont, Mascoma Corporation, Diversa Corporation, ArborGen, Inc., Ceres, Inc., and GreenWood Resources, Inc.
BESC brought together individuals, institutions, and disciplines to focus on understanding and ameliorating biomass recalcitrance. As a result of discussions at our retreats and other fora, ideas emerged that would not have happened without a center so designed. As a result of common management, resources, and non-disclosure agreements, barriers to collaboration were substantially lowered as compared to individual investigators acting on their own. Students and postdoctoral staff were among the greatest beneficiaries. Upon hiring BESC-supported students, companies observed that they had extraordinary experience functioning as part of interdisciplinary teams. As an indication of the extent of collaboration, about half of our publications in year 9 had co-authors from more than one BESC institution.
Top-down structures and bottom-up networking were useful and complementary in fostering integration. Weekly calls were held by the science and operational management team. Twice-monthly calls were held with a larger group (roughly 15) consisting of the science management and activity leads, with topics alternating between science and management calls. BESC refreshed its management, all but two of the original eight management team members being replaced by year 10; this included hiring a new Director. Keeping leadership fresh was also accomplished as early and mid-career staff—some of them graduate students at the start of BESC—were promoted and given added responsibility such that by the end of BESC they comprised over half of BESC activity and project leads. Task- and organism-specific points of contact were designated to facilitate interactions among teams and individuals.
Technology transfer, managed by a Commercialization Council chaired by ORNL, and consisting of the COO and technology transfer leads from each partner institution operated as a community of best practice to strategically and effectively engage with industrial partners. A “storefront” on the BESC website provided a centralized online portal for industry to view available technologies for licensing and partnering. The IP management plan was built on a common Inter-Institutional Agreement template that allows a designated lead institution to offer jointly owned IP from multiple BESC members . Another assessment of the value of the advances is shown by technoeconomic evaluation of several advanced disruptive improvements; CBP with co-treatment was projected to have a potential eight-fold improved return-on-investment .
Tech transfer metrics at the time of writing featured more than 190 invention disclosures resulting in 60 patent applications and 21 executed licenses. For example, in 2016, two companies licensed a gene discovered using GWAS in Populus trichocarpa . GreenWood Resources plans to utilize the gene to select low lignin poplar variants for further breeding resulting in lower-cost improvements in either conversion processes or pulping. Forage Genetics Intl. will commercialize this genetic mechanism to reduce lignin and increase desirable flavonoids. This will increase digestibility and the nutritional value of animal feedstocks such as alfalfa, corn, and sorghum.
The ability to freely share materials and protect potential IP that belong to the BESC partners is an essential function for expeditious collaboration within the Center. A laboratory information management system (LIMS) served as the main mechanism for documenting the transfer of materials among BESC partners as allowed under the innovative BESC Master Material Transfer Agreement. The LIMS also represented the primary system for tracking large experimental campaigns, protocols, data, and metadata and for data quality assurance. LIMS is a relatively mature system developed during BESC using a commercial LIMS software package, Nautilus (http://www.thermo.com), which was specifically designed to manage flexible laboratory processes. This system has an Oracle relational database engine as its back end and generated numerous customized workflows and web interfaces to view results from laboratory processes and experimental campaigns, which has successfully been used to track more than 100,000 samples during the BESC project.
The nationwide BESC Outreach program targeted science enrichment and educational standards in 4th–6th grades. In collaboration with the Creative Discovery Museum in Chattanooga, Tennessee, we developed a hub-and-spoke model using hubs at 18 national museums and science centers in 14 states (Utah, Idaho, Montana, New Mexico, Kansas, Oregon, Washington, Georgia, Tennessee, Alabama, Texas, Michigan, Illinois, Florida, and Oklahoma) . The “Farming for Fuels” Program is available on our websites. Over 225,000 students, parents, and teachers have participated in hands-on activities. These are not hits on a website, they are person-to-person contacts and educational activities. The enhanced Biofuels website (http://www.learnbiofuels.org) with information and downloadable biofuels-related lesson plans has received more than 45,000 page views. A Biofuels/Alternative Energy iPad software app “Road Trip Challenge” is available through the iTunes App Store with eight “trips” between hub museums. Importantly, the program is moving closer to becoming self-sustaining. Of the over 50,000 students, teachers, and parents reached during 2016, 81% were served with no direct program-support cost to BESC.
BESC has redefined biomass recalcitrance from an observable phenotype to a better understood and manipulatable fundamental and operational property. These manipulations are the result of deeper biological understanding and can be combined with other advanced biotechnology improvements in biomass conversion [76, 77] to improve bioenergy processes and markets.
BHD and PG prepared the manuscript draft. LRL, MFD, and DM edited and provided pertinent references. BHD compiled the final version. All authors read and approved the final manuscript.
We acknowledge Martin Keller, the first BESC director, and Alan Darvill for contributions to the initial science vision and management.
This manuscript has been authored by UT-Battelle. LLC under Contract No. DE-AC05-00OR22725 with the US Department of Energy. The publisher, by accepting the article for publication, acknowledges that the United States Government retains a non-exclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan).
The authors declare that they have no competing interests.
This research was funded by the BioEnergy Science Center (BESC) which is a US Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. ORNL is managed by UT-Battelle, LLC, Oak Ridge, TN, USA, for the DOE under contract DE-AC05-00OR22725.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Paul Gilna, Email: vog.lnro@panilg.
Lee R. Lynd, Email: firstname.lastname@example.org.
Debra Mohnen, Email: ude.agu.crcc@nenhomd.
Mark F. Davis, Email: vog.lern@sivaD.kraM.
Brian H. Davison, Phone: 865-574-0955, Email: vog.lnro@hbnosivad.