Role of respiratory terminal oxidases in the extracellular electron transfer ability of cyanobacteria.

Cyanobacteria are used as anode catalysts in photo-bioelectrochemical cells to generate electricity in a sustainable, economic, and environmental friendly manner using only water and sunlight. Though cyanobacteria (CB) possess unique advantage for solar energy conversion by virtue of its robust photosynthesis, they cannot efficiently perform extracellular electron transfer (EET). The reasons being, unlike dissimilatory metal reducing bacteria (that are usually exploited in microbial fuel cells to generate electricity), (1) CB do not possess any special features on their outer membrane to carry out EET and, (2) the electrons generated in photosynthetic electron transport chain are channeled into competing respiratory pathways rather than to the anode. CB, genetically engineered to express outer membrane cytochrome S (OmcS), was found to generate ∼nine-fold higher photocurrent compared to that of wild-type cyanobacterium in our previous work. In this study, each of the three respiratory terminal oxidases in Synechococcus elongatus PCC7942 namely bd-type quinol oxidase, aa3 -type cytochrome oxidase, and cbb3 -type cytochrome oxidase was knocked-out one at a time (cyd- , cox- , and cco- respectively) and its contribution for extracellular ferricyanide reduction and photocurrent generation was investigated. The knock-out mutant lacking functional bd-type quinol oxidase (cyd- ) exhibited greater EET by reducing more ferricyanide compared to other single knock-out mutants as well as the wild type. Further, cyd- omcs (the cyd- mutant expressing OmcS) was found to generate more photocurrent than the corresponding single knock out controls and the wild-type. This study clearly demonstrates that the bd-quinol oxidase diverted more electrons from the photosynthetic electron transport chain towards respiratory oxygen reduction and knocking it out had certainly enhanced the cyanobacterial EET.