Modelling photosystem I as a complex interacting network

Abstract

In this paper, we model the excitation energy transfer (EET) of photosystem I (PSI) of the common pea plant Pisum sativum as a complex interacting network. The magnitude of the link energy transfer between nodes/chromophores is computed by Forster resonant energy transfer (FRET) using the pairwise physical distances between chromophores from the PDB 5L8R (Protein Data Bank). We measure the global PSI network EET efficiency adopting well-known network theory indicators: the network efficiency (Eff) and the largest connected component (LCC). We also account the number of connected nodes/chromophores to P700 (CN), a new ad hoc measure we introduce here to indicate how many nodes in the network can actually transfer energy to the P700 reaction centre. We find that when progressively removing the weak links of lower EET, the Eff decreases, while the EET paths integrity (LCC and CN) is still preserved. This finding would show that the PSI is a resilient system owning a large window of functioning feasibility and it is completely impaired only when removing most of the network links. From the study of different types of chromophore, we propose different primary functions within the PSI system: chlorophyll a (CLA) molecules are the central nodes in the EET process, while other chromophore types have different primary functions. Furthermore, we perform nodes removal simulations to understand how the nodes/chromophores malfunctioning may affect PSI functioning. We discover that the removal of the CLA triggers the fastest decrease in the Eff, confirming that CAL is the main contributors to the high EET efficiency. 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.

The robustness of the photosynthetic system I energy transfer complex network to targeted node attack and random node failure

“…The PSI network describes the FRET energy transfer occurring among chromophores toward the reaction centre (RC). The building of the PSI complex network was recently presented in Montepietra et al [28], where the PSI is modelled as a directed and weighted network with a total number of nodes/chromophores N = 192. For details about the PSI network construction, see Montepietra et al [28].…”

“…Building different sub-networks starting from the complete PSI network is a solid strategy capable of providing insights into the system's different functioning regimes [28,39]. These sub-networks are obtained from the complete one where all possible links are present (as described above) by removing links whose…”

“…through directed weighted paths [28,33,37] associated physical distance is higher than a threshold value called cut-off distance (CD). A longer distance means that the link will have a lower FRET efficiency value.…”

“…In this article, we implement node attack strategies over a recent and newly assembled biological network, that is, the photosynthetic system I (PSI) energy transfer complex network of the common pea plant Pisum sativum [28], to assess the robustness of this real-world system. Photosystem I is a membrane protein-chromophore complex functioning as a light-driven electron pump within the oxygenic photosynthetic process [29,30].…”

“…Photosystem I is a membrane protein-chromophore complex functioning as a light-driven electron pump within the oxygenic photosynthetic process [29,30]. The PSI is a weighted and directed network in which the nodes represent the chlorophyll and carotenoid molecules, while the links between the nodes model the energetic coupling between the chromophores (see Montepietra et al [28] for details).…”