A New Dawn for Industrial Photosynthesis The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Robertson, Dan E., Stuart A. Jacobson, Frederick Morgan, David Berry, George M. Church, and Noubar B. Afeyan. 2011. A new dawn for industrial photosynthesis. Photosynthesis Research 107(3): 269-277. Published Version doi://10.1007/s11120-011-9631-7 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:5130453 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Photosynth Res (2011) 107:269–277 DOI 10.1007/s11120-011-9631-7 REGULAR PAPER A new dawn for industrial photosynthesis Dan E. Robertson • Stuart A. Jacobson • Frederick Morgan • David Berry • George M. Church • Noubar B. Afeyan Received: 5 October 2010 / Accepted: 26 January 2011 / Published online: 13 February 2011 Ó The Author(s) 2011. This article is published with open access at Springerlink.com Abstract Several emerging technologies are aiming to conversion. This analysis addresses solar capture and meet renewable fuel standards, mitigate greenhouse gas conversion efficiencies and introduces a unique systems emissions, and provide viable alternatives to fossil fuels. approach, enabled by advances in strain engineering, Direct conversion of solar energy into fungible liquid fuel photobioreactor design, and a process that contradicts is a particularly attractive option, though conversion of that prejudicial opinions about the viability of industrial pho- energy on an industrial scale depends on the efficiency of tosynthesis. We calculate efficiencies for this direct, con- its capture and conversion. Large-scale programs have tinuous solar process based on common boundary been undertaken in the recent past that used solar energy to conditions, empirical measurements and validated grow innately oil-producing algae for biomass processing assumptions wherein genetically engineered cyanobacteria to biodiesel fuel. These efforts were ultimately deemed to convert industrially sourced, high-concentration CO2 into be uneconomical because the costs of culturing, harvesting, secreted, fungible hydrocarbon products in a continuous and processing of algal biomass were not balanced by the process. These innovations are projected to operate at areal process efficiencies for solar photon capture and productivities far exceeding those based on accumulation and refining of plant or algal biomass or on prior assumptions of photosynthetic productivity. This concept, D. E. Robertson (&) currently enabled for production of ethanol and alkane Biological Sciences, Joule Unlimited, 83 Rogers Street, diesel fuel molecules, and operating at pilot scale, estab- Cambridge, MA 02142, USA e-mail: [email protected] lishes a new paradigm for high productivity manufacturing of nonfossil-derived fuels and chemicals. S. A. Jacobson Á F. Morgan Engineering, Joule Unlimited, 83 Rogers Street, Cambridge, Keywords Cyanobacteria Á Metabolic engineering Á MA 02142, USA e-mail: [email protected] Hydrocarbon Á Alkane Á Diesel Á Renewable fuel Á Algae Á Biomass Á Biodiesel F. Morgan e-mail: [email protected] D. Berry Á N. B. Afeyan Introduction Flagship VentureLabs, 1 Memorial Drive, Cambridge, MA 02142, USA e-mail: dberry@flagshipventures.com The capture of solar energy to power industrial processes has been an inviting prospect for decades. The energy N. B. Afeyan e-mail: nafeyan@flagshipventures.com density of solar radiation and its potential as a source for production of fuels, if efficiently captured and converted, G. M. Church could support the goals of national energy independence. Department of Genetics, Harvard University, Analyses of photosynthetic conversion have been driven by School of Medicine, 77 Ave Louis Pasteur, NRB 238, Boston, MA 02115, USA this promise (Goldman 1978; Pirt 1983; Bolton and Hall e-mail: [email protected] 1991; Zhu et al. 2008, 2010). The deployment of solar- 123 270 Photosynth Res (2011) 107:269–277 based industries for fuels has, however, been limited by the Table 1 Technological innovations leading to high-energy capture lack of efficient cost-effective technologies. Projects fun- and conversion characteristics of a direct, continuous process for ded between 1976 and 1996 under the US Department of photosynthetic fuel production Energy (DOE) aquatic species program explored photo- Process innovation System design trophic organisms and process technologies for the pro- Maximize energy capture and • Metabolic engineering for duction of algal oils and their refinement into biodiesel. conversion by process recombinant pathway to directly The results of these efforts were summarized in a report organism synthesize final product that delineated the technological barriers to industrial • Gene regulation control to development (Sheehan et al. 1998). optimize carbon partitioning to The traditional photosynthetic fuels process is one wherein product triglyceride-producing algae are grown under illumination • Metabolic switching to control carbon flux during growth and and stressed to induce the diversion of a fraction of carbon to production phases oil production. The algal biomass is harvested, dewatered and Minimize peripheral • Cyanobacterial system to obviate lysed, and processed to yield a product that is chemically metabolism mitochondrial metabolism refined to an acyl ester biodiesel product. Many companies • Operation at high ([1%) CO2 to have been founded since the DOE final report that strive to minimize photorespiration make incremental improvements in this process to create Maximize yield and • Decoupling of biomass formation viable solar energy-to-fuel technologies. However, many of productivity from product synthesis the fundamental barriers to industrial photosynthetic effi- • Engineering continuous secretion ciency remain and threaten to constrain this approach to one of product wherein only associated coproduct generation can salvage the • Optimization of process cycle time via continuous production process economics (Wijffels and Barbosa 2010). Enable economic, efficient Photobioreactor that Here, we reassess industrial photosynthesis in light of reactor and process • minimizes solar reflection the development of powerful tools for systems biology, • optimizes photon capture and gas metabolic engineering, reactor and process design that have mass transfer at high culture enabled a direct-to-product, continuous photosynthetic density process (direct process). Many of these innovations were • optimizes thermal control presaged by DOE as well as academic and industrial sources (Gordon and Polle 2007; Rosenberg et al. 2008) who suggested that these types of technological advances comparative illustration of the algal biomass process and could enable the success of industrial photosynthesis (see the direct photosynthetic concept is shown in Fig. 1. Many Table 1 for a list of innovations and advances inherent in analyses have been performed for the algal process the direct process). (Benemann and Oswald 1994; Chisti 2007; Gordon and The direct process uses a cyanobacterial platform Polle 2007; Dismukes et al. 2008; Rosenberg et al. 2008; organism engineered to produce a diesel-like alkane mix- Schenk et al. 2008; Angermayr et al. 2009; Stephens et al. ture, to maximally divert fixed CO2 to the engineered 2010; Weyer et al. 2009; Wijffels and Barbosa 2010; pathway, and to secrete the alkane product under conditions Zemke et al. 2010; Zijffers et al. 2010) and for photosyn- of limited growth but continuous production. This creates a thetic efficiency associated with production of plant bio- process analogous to those of engineered fermentative mass (Zhu et al. 2008, 2010) and we have incorporated the systems that use heterotrophic organisms, e.g., yeast, E coli, relevant aspects of these published reports to bound the etc., whose phases of growth and production are separated current analysis. Our analysis of the algal process closely and whose carbon partitioning is controlled to achieve very follows the assumptions of Weyer et al. (2009) with the high maximal productivities (for example, see Ohta et al. exception that we use the more common open-pond sce- 1991; Stephanopoulos et al. 1998). Such processes, where nario. Note that we also make a clear distinction between cells partition carbon and free energy almost exclusively to biodiesel esters derived from algal biomass and fungible produce and secrete a desired product while minimizing alkane diesel synthesized directly. energy conversion losses due to growth-associated metab- olism, have much longer process cycle times and higher system productivities than those requiring organism growth Photosynthetic efficiency and downstream biomass harvesting and processing. For purposes of energy conversion analysis, we compare The cumulative energy input and the derived energy output the direct process to a conventional algal pond biomass- are critical factors in comparing processes for fuel pro- based process producing biodiesel esters. A simple duction. In discussing energy input, photosynthesis has an 123 Photosynth Res (2011) 107:269–277 271 Fig. 1 Schematic comparison between algal biomass and direct waste CO2 at concentrations 50–1009 higher than atmospheric. The photosynthetic processes. The direct process, developed by Joule