Performance of a Bacterium as an Energy Conversion Device in Terms of Energy-Return-On-Investment Determined from Atomic-Detail Structural Models

Abstract

The energy-return-on-investment (EROI) time, defined as the time for a biological cell or a subcomponent to produce enough ATP to manufacture a new copy, is determined for an entire phototrophic bacterium, Rba. sphaeroides, as a function of incident light intensity at growth. The EROI is determined through a combined computational-experimental approach, using atomic-detail structural and functional models of bacterial bioenergetic domains at protein, organelle, and cell scales, based on AFM, cryo-electron tomography, mass spectrometry, crystallography, and spectroscopy data modalities. The hierarchy of time scales in the energy conversion processes was addressed via a multitude of computational models for each scale, from electronic excitation transfer to charge carrier diffusion to structure based rate kinetics, wherein the output of each model becomes an input parameter for the next scale. The EROI is formulated in relation to cell doubling time for a controlled growth environment that removes energy expenditure channels other than replication and base metabolism, such as motility, as well as energy input channels other than light absorption. Under these controlled conditions, the approach successfully reproduces light-dependence of growth behavior over nearly three orders of magnitude of illumination. Rational design principles for bioengineered energy solutions are revealed by identifying bottlenecks of energy conversion at protein level. The EROI also provides a systems-level integrative performance metric for quantifying evolutionary competitiveness between different species as well as a comparison to artificial energy harvesting systems. Current efforts extending this approach to the structural models from cyanobacterial and granal bioenergetic domains, comprising more than 4,000 proteins, will also be presented.