Direct interspecies electron transfer (DIET) may prevail in microbial communities that show methanogenesis and anaerobic methane oxidation and can be an electron source to support anaerobic photosynthesis. Previous mutagenic studies on cocultures of defined Geobacter species indicate that both conductive pili and extracellular cytochromes are essential for DIET. However, the actual functional role of the pili in DIET is uncertain, as the pilus mutation strategy used in these studies affected the extracellular cytochrome profile. Here we repressed the function of pili by deleting the pilus polymerization motor PilB in both Geobacter species. The PilB mutation inhibited the pilus assembly but did not alter the pattern of extracellular cytochromes. We report that the two pilus-free Geobacter species can form aggregates and grow syntrophically with DIET. The results demonstrate that the Gmet_2896 cytochrome of Geobacter metallireducens plays a key role in DIET and that conductive pili are not necessary to facilitate DIET in cocultures of Geobacter species, and they suggest cytochromes by themselves can meditate DIET, deepening the understanding of DIET.
Electrically conductive pili (e-pili) enable electron transport over multiple 11 cell lengths to extracellular environments and play an important role in extracellular 12 electron transfer (EET) of Geobacter species. To date, the studies of e-pili have 13 mainly focused on Geobacter sulfurreducens and the closely related Geobacter 14 metallireducens because of their developed genetic manipulation systems. We Surprisingly, strain GSP was deficient in Fe(III) oxide reduction and current 25 production due to the impaired content of outer-surface c-type cytochromes. These 26 results demonstrated that heterologous pili of G. sulfurreducens severely reduces the 27 content of outer-surface c-type cytochromes and consequently eliminates the capacity 28 for EET, which strongly suggests an attention should be paid to the content of c-type 29 cytochromes when employing G. sulfurreducens to heterologously express pili from 30 other microorganisms. 31 IMPORTANCE The studies of electrically conductive pili (e-pili) of Geobacter 32 3 species are of interest because of its application prospects in electronic materials. e-33Pili are considered a substitution for electronic materials due to its renewability, 34 biodegradability and robustness. Continued exploration of additional e-pili of 35Geobacter soli will improve the understanding of their biological role in extracellular 36 electron transfer and expand the range of available electronic materials. 37Heterologously expressing the pilin genes from phylogenetically diverse 38 microorganisms has been proposed as an emerging approach to screen potential e-pili 39 according to high current densities. However, our results indicated that a Geobacter 40 sulfurreducens strain heterologously expressing a pilin gene produced low current 41 densities that resulted from a lack of content of c-type cytochromes, which were likely 42 to possess e-pili. These results provide referential significance to yield e-pili from 43 diverse microorganisms. 44
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