Transcriptomic, Proteomic, and Bioelectrochemical Characterization of an Exoelectrogen Geobacter soli Grown With Different Electron Acceptors

Abstract

The ability of Geobacter species to transfer electrons outside cells enables them to play an important role in biogeochemical and bioenergy processes. Our knowledge of the extracellular electron transfer (EET) process in the genus Geobacter is mainly from the study of G. sulfurreducens, and in order to fully investigate the EET mechanisms in the genus Geobacter, other Geobacter species should also be considered. This study focused on the EET of Geobacter soli GSS01, which exhibited a capability of reducing insoluble Fe(III) oxides and generating electrical current comparable with G. sulfurreducens PCA. Electrochemical characterization, including cyclic voltammetry, differential pulse voltammetry, and electrochemical in situ FTIR spectra, revealed that different redox proteins contributed to the electrochemical behaviors of G. soli and G. sulfurreducens. Based on comparative transcriptomic and proteomic analyses, OmcS was the most upregulated protein in both G. soli and G. sulfurreducens cells grown with insoluble Fe(III) oxides vs. soluble electron acceptor. However, the proteins including OmcE and PilA that were previously reported as being important for EET in G. sulfurreducens were downregulated or unchanged in G. soli cells grown with insoluble electron acceptors vs. soluble electron acceptor, and many proteins that were upregulated in G. soli cells grown with insoluble electron acceptors vs. soluble electron acceptor, such as OmcN, are not important for EET in G. sulfurreducens. We also identified 30 differentially expressed small RNAs (sRNAs) in G. soli cells grown with different acceptors. Taken together, these findings help to understand the versatile EET mechanisms that exist in the genus Geobacter and point to the possibility of sRNA in modulating EET gene expression.

Novel Extracellular Electron Transfer Channels in a Gram-Positive Thermophilic Bacterium

“…In particular, constitutive expression has been reported for different terminal oxidoreductases of a thermophilic iron-reducer Melioribacter roseus from a deep subsurface aquifer ( Gavrilov et al, 2017 ), as well as for several multihemes involved in electron transfer to different electron acceptors in a mesophilic iron-reducing soil bacterium Geobacter soli ( Cai et al, 2018 ). A modular principle of the respiratory system organization, which implies differential activity of various multihemes, has been previously proposed for S. oneidensis ( Coursolle and Gralnick, 2010 ) and Geobacter species ( Butler et al, 2010 ; Aklujkar et al, 2013 ; Cai et al, 2018 ). However, the key proteins of the EET chain in C. ferrireducens differ significantly from their previously described counterparts of Geobacter , Shewanella , and Thermincola species ( Figure 7 and Supplementary Figure S6 ).…”

Characterization of the genome fromGeobacter anodireducens, a strain with enhanced current production in bioelectrochemical systems

“…Similar to most members of the genus Geobacter, all four strains can utilize both soluble and insoluble Fe(III) as the sole electron acceptor coupled with the oxidation of acetate, [25][26][27]53 and are capable of producing current on the anode of MFCs (Table 1). 11,26,54 3.2 Physiological comparison of Geobacter anodireducens to G. sulfurreducens and G. metallireducens Due to the in depth characterization and completed genome sequences of G. sulfurreducens PCA and G. metallireducens GS-15, further physiological comparisons with these species were done in order to uncover potential mechanisms used for enhanced EET in high salinity environments. As previous research has shown, G. anodireducens SD-1 grew fastest of the three strains with soluble Fe(III) citrate provided as the electron acceptor.…”

“…Similar to other characterized Geobacter species, G. anodireducens appears to excel at its ability to exchange electrons with the extracellular environment. 26 Numerous studies have iden-tied c-type cytochromes that are involved in extracellular electron transfer to or from such substrates as Fe(III) oxide, Fe(III) citrate, Mn(IV) oxide, electrodes, Fe(0), Fe(III) containing sediments, and other microorganisms in such organisms as G. sulfurreducens, 33,37,[77][78][79] G. metallireducens, 32,40 G. soli, 54 and G. uraniireducens. 35 The G. anodireducens genome has 87 genes that could potentially code for c-type cytochrome proteins (ESI Table S2 †).…”

“…94,95 OmcS also appears to be involved in electron transfer to insoluble Fe(III) oxide and anodes by G. soli. 54 G. anodireducens also has a homolog for OmcS (Ga0133348_111108) with amino acid sequence identity of 95.16%. However, omcS homologs are not present in genomes from G. metallireducens or most other Geobacter species (Table 3, ESI Table S2 †).…”

The electrically conductive pili ofGeobacter soli

“…The physiological 78 properties of G. soli are different from those of G. sulfurreducens, and these 79 properties determine its special environmental significance, although both strains are 80 highly similar based on phylogenetic analysis (20). For example, G. soli can 81 anaerobically oxidize aromatic compounds, including phenol, benzoate and 82 benzaldehyde, while G. sulfurreducens cannot (20,21). In addition, G. soli has faster 83 Fe(III) oxide reduction and higher current production than G. sulfurreducens (Fig.…”