Long-distance extracellular electron transfer has been observed in Gram-negative bacteria and plays roles in both natural and engineering processes. The electron transfer can be mediated by conductive protein appendages (in short unicellular bacteria such as Geobacter species) or by conductive cell envelopes (in filamentous multicellular cable bacteria). Here we show that Lysinibacillus varians GY32, a filamentous unicellular Gram-positive bacterium, is capable of bidirectional extracellular electron transfer. In microbial fuel cells, L. varians can form centimetre-range conductive cellular networks and, when grown on graphite electrodes, the cells can reach a remarkable length of 1.08 mm. Atomic force microscopy and microelectrode analyses suggest that the conductivity is linked to pili-like protein appendages. Our results show that long-distance electron transfer is not limited to Gram-negative bacteria.
Microbial anode respiration in microbial fuel cells (MFCs) can enhance the degradations of many electron acceptor-type contaminants which are presumed to be competitive to anode respiration. The mechanisms underlying those counterintuitive processes are important for MFCs application but are unclear. This study integrated MFCs with anaerobic baffled reactor (ABR), termed MFC-ABR, to enhance the reduction of azo dye acid orange-7 (AO-7). Compare with ABR, MFC-ABR enhanced the degradation of AO-7, especially at high AO-7 concentration (800 mg/L). Acute toxicity test suggested a higher detoxication efficiency in MFC-ABR. Higher microbial viability, dehydrogenase activity and larger sludge granule size were also observed in MFC-ABR. MFC-ABR significantly enriched and reshaped the microbial communities relative to ABR. Bacteria with respiratory versatility, e.g., Pseudomonas, Geobacter, and Shewanella, were significantly enriched. Functional prediction showed that six metabolism functions (manganese-, iron-, fumarate- and nitrate-respiration, oil bioremediation and chemoheterotrophy) were significantly stimulated while methanogenesis, sulfate-respiration, hydrogen-oxidation were suppressed in MFC-ABR relative to ABR. The results provided important information for understanding the role of microbial anode respiration in contaminated environments.
Bacterial anaerobic respiration using an extracellular electron acceptor plays a predominant role in global biogeochemical cycles. However, the mechanisms of bacterial adaptation to the toxic organic pollutant as the extracellular electron acceptor during anaerobic respiration are not clear, which limits our ability to optimize the strategies for the bioremediation of a contaminated environment. Here, we report the physiological characteristics and the global gene expression of an ecologically successful bacterium, Shewanella decolorationis S12, when using a typical toxic organic pollutant, amaranth, as the extracellular electron acceptor. Our results revealed that filamentous shift (the cells stretched to fiber-like shapes as long as 18 m) occurred under amaranth stress. Persistent stress led to a higher filamentous cell rate and decolorization ability in subcultural cells compared to parental strains. In addition, the expression of genes involved in cell division, the chemotaxis system, energy conservation, damage repair, and material transport in filamentous cells was significantly stimulated. The detailed roles of some genes with significantly elevated expressions in filamentous cells, such as the outer membrane porin genes ompA and ompW, the cytochrome c genes arpC and arpD, the global regulatory factor gene rpoS, and the methyl-accepting chemotaxis proteins genes SHD_2793 and SHD_0015, were identified by site-directed mutagenesis. Finally, a conceptual model was proposed to help deepen our insights into both the bacterial survival strategy when toxic organics were present and the mechanisms by which these toxic organics were biodegraded as the extracellular electron acceptors. IMPORTANCE Keeping toxic organic pollutants (TOPs) in tolerable levels is a huge challenge for bacteria in extremely unfavorable environments since TOPs could serve as energy substitutes but also as survival stresses when they are beyond some thresholds. This study focused on the underlying adaptive mechanisms of ecologically successful bacterium Shewanella decolorationis S12 when exposed to amaranth, a typical toxic organic pollutant, as the extracellular electron acceptor. Our results suggest that filamentous shift is a flexible and valid way to solve the dilemma between the energy resource and toxic stress. Filamentous cells regulate gene expression to enhance their degradation and detoxification capabilities, resulting in a strong viability. These novel adaptive responses to TOPs are believed to be an evolutionary achievement to succeed in harsh habitats and thus have great potential to be applied to environment
Bacterial extracellular electron transfer (EET) plays a key role in various natural and engineering processes. Outer membrane c-type cytochromes (OMCs) are considered to be essential in bacterial EET. However, most bacteria do not have OMCs but have redox proteins other than OMCs in their extracellular polymeric substances of biofilms. We hypothesized that these extracellular non-cytochrome c proteins (ENCP) could contribute to EET, especially with the facilitation of electron mediators. This study compared the electrode respiring capacity of wild type Shewanella decolorationis S12 and an OMC-deficient mutant. Although the OMC-deficient mutant was incapable in direct electricity generation in normal cultivation, it regained electricity generation capacity (26% of the wide type) with the aid of extracellular electron mediator (riboflavin). Further bioelectrochemistry and X-ray photoelectron spectroscopy analysis suggested that the ENCP, such as proteins with Fe–S cluster, may participate in the falvin-mediated EET. The results highlighted an important and direct role of the ENCP, generated by either electricigens or other microbes, in natural microbial EET process with the facilitation of electron mediators.
Bacterial extracellular electron transport (EET) plays an important role in many natural and engineering processes. Some periplasmic non-heme redox proteins usually coexist with c-type cytochromes (CTCs) during the EET process. However, in contrast to CTCs, little is known about the roles of these non-heme redox proteins in EET. In this study, the transcriptome of Shewanella decolorationis S12 showed that the gene encoding a periplasmic sulfite dehydrogenase molybdenum-binding subunit SorA was significantly up-regulated during electrode respiration in microbial fuel cells (MFCs) compared with that during azo-dye reduction. The maximum current density of MFCs catalyzed by a mutant strain lacking SorA (sorA) was 25% higher than that of wild strain S12 (20 vs. 16 µA/cm 2). Both biofilm formation and the current generation of the anodic biofilms were increased by the disruption of sorA, which suggests that the existence of SorA in S. decolorationis S12 inhibits electrode respiration. In contrast, disruption of sorA had no effect on respiration by S. decolorationis S12 with oxygen, fumarate, azo dye, or ferric citrate as electron acceptors. This is the first report of the specific effect of a periplasmic non-heme redox protein on EET to electrode and provides novel information for enhancing bacterial current generation.
Natural microbes employing c-type cytochromes (c-Cyts) for extracellular electron transport (EET) were greatly valuable to develop redox-based bioelectrochemical applications. However, low levels of c-Cyt expression limited the phylogenetically diverse Gram-positive species to be used in bioelectrochemical devices. This work reported the remarkable finding that a high level of c-Cyts was expressed in the cells of the Gram-positive strain Lysinibacillus varians GY32. c-Cyts in Lysinibacillus varians GY32 cells were expressed at a level close to those in Shewanella oneidensis. These c-Cyts were found to cluster in cytoplasmic membrane and periplasmic space, along the length of Lysinibacillus varians GY32 cell. With voltammetry and spectroelectrochemical titration, phenazine methosulfate-mediated electron transfer between the c-Cyts and an electrode was proved. These results expanded the accessible natural models of EET and suggested a new microbial platform for developing bioelectrochemical applications.
Extracellular electron transport (EET) is a key driving force in biogeochemical element cycles and microbial chemical-electrical-optical energy conversion on the Earth. Gram-positive bacteria are ubiquitous and even dominant in EET-enriched environments.
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