Engineered cell elongation promotes extracellular electron transfer of Shewanella oneidensis

To investigate how cell elongation impacts extracellular electron transfer (EET) of electroactive microorganisms (EAMs), the division of model EAM Shewanella oneidensis MR-1 was engineered by reducing the formation of cell divisome. Specially, by blocking the translation of division proteins via anti-sense RNAs or expressing division inhibitors, the cellular length and output power density were all increased. Electrophysiological and transcriptomic results synergistically revealed that the programmed cell elongation reinforced EET by enhancing NADH oxidation, inner-membrane quinone pool, and abundance of c-type cytochromes. Moreover, cell elongation enhanced hydrophobicity due to decreased cell-surface polysaccharide, thus facilitated initial surface adhesion stage in biofilm formation. The output current and power density all increased in positive correction with cellular length. However, inhibition of cell division reduced cell growth, which was then restored by quorum sensing-based dynamic regulation of cell growth and elongation phases. The QS-regulated elongated strain thus enabled a cell length of 143.6 ± 40.3 µm (72.6-fold of that of S. oneidensis MR-1), which resulted in an output power density of 248.0 ± 10.6 mW m-2 (3.41-fold of that of S. oneidensis MR-1) and exhibited superior potential for pollutant treatment. Engineering cellular length paves an innovate avenue for enhancing the EET of EAMs. To investigate the specifc mechanisms underlying enhanced power production of cell elongation, the transcriptomes of SulA and WT were comparatively analyzed.