Photosynthetic pigment-protein complexes as highly connected networks: implications for robust energy transport

Abstract

Photosynthetic pigment-protein complexes (PPCs) are a vital component of the light-harvesting machinery of all plants and photosynthesizing bacteria, enabling efficient transport of the energy of absorbed light towards the reaction centre, where chemical energy storage is initiated. PPCs comprise a set of chromophore molecules, typically bacteriochlorophyll species, held in a well-defined arrangement by a protein scaffold; this relatively rigid distribution leads to a viewpoint in which the chromophore subsystem is treated as a network, where chromophores represent vertices and inter-chromophore electronic couplings represent edges. This graph-based view can then be used as a framework within which to interrogate the role of structural and electronic organization in PPCs. Here, we use this network-based viewpoint to compare excitation energy transfer (EET) dynamics in the light-harvesting complex II (LHC-II) system commonly found in higher plants and the FennaMatthews-Olson (FMO) complex found in green sulfur bacteria. The results of our simple networkbased investigations clearly demonstrate the role of network connectivity and multiple EET pathways on the efficient and robust EET dynamics in these PPCs, and highlight a role for such considerations in the development of new artificial light-harvesting systems.

Modeling the photosynthetic system I as complex interacting network

“…We simulated different nodes removal (attack) processes over the PSΙ network [18,52] . The PSΙ network nodes removal may describe functionality loss of the chromophores, that can be due by aging, disease, pollution or others [3] .…”

“…The ability of photosynthetic oxygenic organisms to convert light energy into chemical energy depends on a group of large membrane-bound complexes whose coordinated activity allows the capture of photons and their conversion into highly energetic molecules as NADPH and ATP through an electron transport chain [1] . The whole photosynthetic process is driven by the biological complexes possessing the light-capturing function: photosystem I (PSΙ) and photosystem ΙΙ (PSΙΙ) [2,3] . The photosynthetic process starts with the catch of an incoming photon by PSII that utilizes it to oxidize water.…”

“…Other cofactors present in PSΙ are also involved in the processes of light capturing, charge separation and prevention of photodamage, like carotenoids (Cars). This network of pigments, whose absorption spectra spans a broad spectral range, is embedded in a protein scaffold which enforces chromophores spatial organization by holding them in a relatively rigid position and orientation [3] .…”

“…Our outcomes open new perspectives of research, such comparing the PSI energy transfer efficiency of different natural and agricultural plant species and investigating the light-harvesting mechanisms of artificial photosynthesis both in plant agriculture and in the field of solar energy applications. Keywords: Complex network, photosystem I, photosynthetic network, biological network, network robustness, network attack.been directed to unveil the underneath structural and topological patterns shaping the high EET efficiency of the PSI system [2,3].The purpose of this research is the analysis of the structural organization of a plant PSΙ as a complex networked system for EET by means of network science viewpoint. Network science has proven to be a powerful tool for the study of complex systems from many different realms [18][19][20][21][22][23][24][25][26] .…”

“…been directed to unveil the underneath structural and topological patterns shaping the high EET efficiency of the PSI system [2,3].…”