Richard T. Sayre

Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production

Due to the growing need to provide alternatives to fossil fuels as efficiently, economically, and sustainably as possible there has been growing interest in improved biofuel production systems. Biofuels produced from microalgae are a particularly attractive option since microalgae have production potentials that exceed the best terrestrial crops by 2 to 10-fold. In addition, autotrophically grown microalgae can capture CO2 from point sources reducing direct atmospheric greenhouse gas emissions. The enhanced biomass production potential of algae is attributed in part to the fact that every cell is photosynthetic. Regardless, overall biological energy capture, conversion, and storage in microalgae are inefficient with less than 8% conversion of solar into chemical energy achieved. In this review, we examine the thermodynamic and kinetic constraints associated with the autotrophic conversion of inorganic carbon into storage carbohydrate and oil, the dominant energy storage products in Chlorophytic microalgae. We discuss how thermodynamic restrictions including the loss of fixed carbon during acetyl CoA synthesis reduce the efficiency of carbon accumulation in lipids. In addition, kinetic limitations, such as the coupling of proton to electron transfer during plastoquinone reduction and oxidation and the slow rates of CO2 fixation by Rubisco reduce photosynthetic efficiency. In some cases, these kinetic limitations have been overcome by massive increases in the numbers of effective catalytic sites, e.g. the high Rubisco levels (mM) in chloroplasts. But in other cases, including the slow rate of plastoquinol oxidation, there has been no compensatory increase in the abundance of catalytically limiting protein complexes. Significantly, we show that the energetic requirements for producing oil and starch relative to the recoverable energy stored in these molecules are very similar on a per carbon basis. Presently, the overall rates of starch and lipid synthesis in microalgae are very poorly characterized. Increased understanding of the kinetic constraints of lipid and starch synthesis, accumulation and turnover would facilitate the design of improved biomass production systems.

Impact of nitrogen limitation on biomass, photosynthesis, and lipid accumulation in Chlorella sorokiniana

Induction of oil accumulation in algae for biofuel production is often achieved by withholding nitrogen. However, withholding nitrogen often reduces total biomass yield. In this report, it is demonstrated that Chlorella sorokiniana will not only accumulate substantial quantities of neutral lipids when grown in the absence of nitrogen but will also exhibit unimpeded growth rates for up to 2xa0weeks. To determine the physiological basis for the observed increase in oil and biomass accumulation, we compared photosynthetic and respiration rates and chlorophyll, lipid, and total energy content under ammonia replete and deplete conditions. Under N-depleted growth conditions, there was a 64xa0% increase in total energy density and a ∼20-fold increase in oil accumulation relative to N-replete growth leading to a 1.6-fold greater total energy yield in N-depleted than in N-replete cultures. We propose that the higher energy accumulation in N-depleted cultures is due to enhanced photosynthetic energy capture and conversion associated with reduced chlorophyll levels and reduced self-shading as well as a shift in metabolism leading to the accumulation of oils.

Electron transfer reactions: generalized spin-boson approach

We introduce a mathematically rigorous analysis of a generalized spin-boson system for the treatment of a donor–acceptor (reactant-product) quantum system coupled to a thermal quantum noise. The donor/acceptor probability dynamics describes transport reactions in chemical processes in presence of a noisy environment – such as the electron transfer in a photosynthetic reaction center. Besides being rigorous, our analysis has the advantages over previous ones that (1) we include a general, non energy-conserving system-environment interaction, and that (2) we allow for the donor or acceptor to consist of multiple energy levels lying closely together. We establish explicit expressions for the rates and the efficiency (final donor–acceptor population difference) of the reaction. In particular, we show that the rate increases for a multi-level acceptor, but the efficiency does not.

Iron and protein biofortification of cassava: lessons learned

Over two hundred and fifty million Africans rely on the starchy root crop cassava (Manihot esculenta) as their primary source of calories. Cassava roots, however, have the lowest protein:energy ratio of all the worlds major staple crops. Furthermore, a typical cassava-based diet provides less than 10-20% of the required amounts of iron, zinc, vitamin A and vitamin E. The BioCassava Plus program employed modern biotechnologies to improve the health of Africans through development and delivery of novel cassava germplasm with increased nutrient levels. Here we describe the development of molecular strategies and their outcomes to meet minimum daily allowances for protein and iron in cassava based diets. We demonstrate that cyanogens play a central role in cassava nitrogen metabolism and that strategies employed to increase root protein levels result in reduced cyanogen levels in roots. We also demonstrate that enhancing root iron uptake has an impact on the expression of genes that regulate iron homeostasis in multiple tissues. These observations demonstrate the complex metabolic interactions involved in enhancing targeted nutrient levels in plants and identify potential new strategies for further enhancing nutrient levels in cassava.

Strategies for optimizing algal biology for enhanced biomass production

One of the more environmentally sustainable ways to produce high energy density (oils) feed stocks for the production of liquid transportation fuels is from biomass. Photosynthetic carbon capture combined with biomass combustion (point source) and subsequent carbon capture and sequestration (BECCS) has also been proposed in the Intergovernmental Panel on Climate Change Report as one of the most effective and economical strategies to remediate atmospheric greenhouse gases. To maximize photosynthetic carbon capture efficiency and energy-return-on-investment, we must develop biomass production systems that achieve the greatest yields with the lowest inputs. Numerous studies have demonstrated that microalgae have among the greatest potentials for biomass production. This is in part due to the fact that all alga cells are photoautotrophic, they have active carbon concentrating mechanisms to increase photosynthetic productivity, and all the biomass is harvestable unlike plants. All photosynthetic organisms, however, convert only a fraction of the solar energy they capture into chemical energy (reduced carbon or biomass). To increase aerial carbon capture rates and biomass productivity it will be necessary to identify the most robust algal strains and increase their biomass production efficiency often by genetic manipulation. We review recent large-scale efforts to identify the best biomass producing strains and metabolic engineering strategies to improve aerial productivity. These strategies include optimization of photosynthetic light-harvesting antenna size to increase energy capture and conversion efficiency and the potential development of advanced molecular breeding techniques. To date, these strategies have resulted in up to two-fold increases in biomass productivity.

Quantum Biological Switch Based on Superradiance Transitions

A linear chain of connected sites with two asymmetric sinks, one attached to each end, is used as a simple model of quantum (excitonic and/or electron) transport in photosynthetic biocomplexes. For a symmetric initial population in the middle of the chain, it is expected that transport is mainly directed toward the strongly coupled sink. However, we show that quantum effects radically change this intuitive “classical” mechanism so that transport can occur through the weakly coupled sink with maximal efficiency. Using this capability, we show how to design a quantum switch that can transfer energy or charge to the strongly or weakly coupled branch of the chain, by changing the coupling to the sinks. The operational principles of this quantum device can be understood in terms of superradiance transitions and subradiant states. This switching, being a pure quantum effect, can be used as a witness of wavelike behavior in molecular chains. When realistic data are used for the photosystem II reaction center, th...

Dynamics of a chlorophyll dimer in collective and local thermal environments

We present a theoretical analysis of exciton transfer and decoherence effects in a photosynthetic dimer interacting with collective (correlated) and local (uncorrelated) protein-solvent environments. Our approach is based on the framework of the spin-boson model. We derive explicitly the thermal relaxation and decoherence rates of the exciton transfer process, valid for arbitrary temperatures and for arbitrary (in particular, large) interaction constants between the dimer and the environments. We establish a generalization of the Marcus formula, giving reaction rates for dimer levels possibly individually and asymmetrically coupled to environments. We identify rigorously parameter regimes for the validity of the generalized Marcus formula. The existence of long living quantum coherences at ambient temperatures emerges naturally from our approach.

Possible role of interference, protein noise, and sink effects in nonphotochemical quenching in photosynthetic complexes

We analyze theoretically a simple and consistent quantum mechanical model that reveals the possible role of quantum interference, protein noise, and sink effects in the nonphotochemical quenching (NPQ) in light-harvesting complexes (LHCs). The model consists of a network of five interconnected sites (excitonic states of light-sensitive molecules) responsible for the NPQ mechanism. The model also includes the “damaging” and the dissipative channels. The damaging channel is responsible for production of singlet oxygen and other destructive outcomes. In our model, both damaging and “dissipative” charge transfer channels are described by discrete electron energy levels attached to their sinks, that mimic the continuum part of electron energy spectrum. All five excitonic sites interact with the protein environment that is modeled using a stochastic process. Our approach allowed us to derive the exact and closed system of linear ordinary differential equations for the reduced density matrix and its first momentums. These equations are solved numerically including for strong interactions between the light-sensitive molecules and protein environment. As an example, we apply our model to demonstrate possible contributions of quantum interference, protein noise, and sink effects in the NPQ mechanism in the CP29 minor LHC. The numerical simulations show that using proper combination of quantum interference effects, properties of noise, and sinks, one can significantly suppress the damaging channel. Our findings demonstrate the possible role of interference, protein noise, and sink effects for modeling, engineering, and optimizing the performance of the NPQ processes in both natural and artificial light-harvesting complexes.

Superradiance Transition and Nonphotochemical Quenching in Photosynthetic Complexes

We demonstrate numerically that superradiance could play a significant role in light-harvesting complexes, when two escape channels into continuum for the exciton are competing. Our model consists of a network of five interconnected sites (discrete excitonic states). Damaging and charge transfer states are linked to their sinks (independent continuum electron spectra), in which the chemical reactions occur. The superradiance transition in the charge transfer (or in the damaging) channel occurs at particular electron transfer rates from the discrete to the continuum electron spectra and can be characterized by a segregation of the imaginary parts of the eigenvalues of the effective non-Hermitian Hamiltonian. All five excitonic sites interact with their protein environment that is modeled by a random stochastic process. We find the region of parameters in which the superradiance transition into the charge transfer channel takes place. We demonstrate that this superradiance transition has the capability of p...

Noise-assisted quantum electron transfer in photosynthetic complexes

Electron transfer (ET) between primary electron donor and acceptor is modeled in the photosynthetic complexes. Our model includes (i) two discrete energy levels associated with donor and acceptor, which are directly interacting and (ii) two continuum manifolds of electron energy levels (“sinks”), each interacting with the donor and acceptor. We also introduce external (classical) noise which acts on both donor and acceptor. We derive a closed system of integro-differential equations which describes the non-Markovian quantum dynamics of the ET. A region of parameters is found in which the ET dynamics can be simplified, and described by coupled ordinary differential equations. Using these simplified equations, both cases of sharp and flat redox potentials are analyzed. We analytically and numerically obtain the characteristic parameters that optimize the ET rates and efficiency in this system. In particular, we demonstrate that even for flat redox potential a simultaneous influence of sink and noise can significantly increase the efficiency of the ET. We discuss a relation between our approach and the Marcus theory of ET.