Identification of Multicomponent Histidine-Aspartate Phosphorelay System Controlling Flagellar and Motility Gene Expression in Geobacter Species

Ueki, Toshiyuki; Leang, Ching; Inoue, Kengo; Lovley, Derek R.

doi:10.1074/jbc.m112.345041

Cited by 20 publications

(24 citation statements)

References 40 publications

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“…PgcA could potentially function in this manner while still being held in the extracellular matrix, but the recovery of PgcA in cell supernatants suggests that it may function as an electron shuttle. The lower abundance of transcripts for genes involved in flagellum function in JS-1 than in KN400 (see Table S2 in the supplemental material) further supports this conclusion because previous studies have suggested that flagellum-mediated motility is most necessary when cells need to directly contact Fe(III) oxides (34)(35)(36). Presumably, once Fe(III) oxide is reduced in one location, the cell must move to a fresh Fe(III) oxide source.…”

Section: Resultssupporting

confidence: 66%

“…This has been attributed to its greater production of electrically conductive pili, which confer higher biofilm conductivity (27,33). Furthermore, KN400 is motile, whereas DL-1 is not, which can be attributed to a regulatory defect in DL-1 (34). Motility is beneficial for Fe(III) oxide reduction because once the Fe(III) in one microenvironment is reduced it is necessary for cells to find a fresh source of electron acceptor (35).…”

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confidence: 99%

“…Restoring the capacity for motility enhanced the rates of Fe(III) oxide reduction by DL-1 (36). Genetically eliminating motility in KN400 (34) or Geobacter metallireducens (36) decreased the capacity for Fe(III) oxide reduction.…”

mentioning

confidence: 99%

“…Initial studies demonstrated that KN400 reduced Fe(III) oxides faster than DL-1 (34). To evaluate the potential role of increased pilus production in this phenotype, a strain in which pilA was deleted was constructed.…”

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confidence: 99%

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Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1

Smith

Tremblay

Shrestha

et al. 2014

Appl Environ Microbiol

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Previous studies have suggested that the conductive pili of Geobacter sulfurreducens are essential for extracellular electron transfer to Fe(III) oxides and for optimal long-range electron transport through current-producing biofilms. The KN400 strain of G. sulfurreducens reduces poorly crystalline Fe(III) oxide more rapidly than the more extensively studied DL-1 strain. Deletion of the gene encoding PilA, the structural pilin protein, in strain KN400 inhibited Fe(III) oxide reduction. However, low rates of Fe(III) reduction were detected after extended incubation (>30 days) in the presence of Fe(III) oxide. After seven consecutive transfers, the PilA-deficient strain adapted to reduce Fe(III) oxide as fast as the wild type. Microarray, whole-genome resequencing, proteomic, and gene deletion studies indicated that this adaptation was associated with the production of larger amounts of the c-type cytochrome PgcA, which was released into the culture medium. It is proposed that the extracellular cytochrome acts as an electron shuttle, promoting electron transfer from the outer cell surface to Fe(III) oxides. The adapted PilA-deficient strain competed well with the wild-type strain when both were grown together on Fe(III) oxide. However, when 50% of the culture medium was replaced with fresh medium every 3 days, the wild-type strain outcompeted the adapted strain. A possible explanation for this is that the necessity to produce additional PgcA, to replace the PgcA being continually removed, put the adapted strain at a competitive disadvantage, similar to the apparent selection against electron shuttle-producing Fe(III) reducers in many anaerobic soils and sediments. Despite increased extracellular cytochrome production, the adapted PilA-deficient strain produced low levels of current, consistent with the concept that long-range electron transport through G. sulfurreducens biofilms is more effective via pili.

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Section: Resultssupporting

confidence: 66%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1

Smith

Tremblay

Shrestha

et al. 2014

Appl Environ Microbiol

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“…Specifically, binding profiles of s H and s N were obtained from cells under heat shock stress and nitrogen limitation, respectively. s F was excluded from this study as the 32 flagella genes controlled by this s factor were found to be usually silent 15,16 . Although several conditions were assayed for s E , no suitable condition could be obtained to induce its expression.…”

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confidence: 99%

Characterizing the interplay between multiple levels of organization within bacterial sigma factor regulatory networks

et al. 2013

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Bacteria contain multiple sigma factors, each targeting diverse, but often overlapping sets of promoters, thereby forming a complex network. The layout and deployment of such a sigma factor network directly impacts global transcriptional regulation and ultimately dictates the phenotype. Here we integrate multi-omic data sets to determine the topology, the operational, and functional states of the sigma factor network in Geobacter sulfurreducens, revealing a unique network topology of interacting sigma factors. Analysis of the operational state of the sigma factor network shows a highly modular structure with s N being the major regulator of energy metabolism. Surprisingly, the functional state of the network during the two most divergent growth conditions is nearly static, with sigma factor binding profiles almost invariant to environmental stimuli. This first comprehensive elucidation of the interplay between different levels of the sigma factor network organization is fundamental to characterize transcriptional regulatory mechanisms in bacteria.

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The unphosphorylated form of the PilR two-component system regulates pilA gene expression in Geobacter sulfurreducens

Hernández-Eligio

Andrade

Soto

et al. 2016

Environ Sci Pollut Res

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In Geobacter sulfurreducens, metal reduction and generation of bioelectricity require the participation of several elements, and among them, the type IV pili has an essential role. The pilus is composed of multiple PilA monomers. Expression of pilA gene depends mainly on the σ54 factor and the response regulator protein PilR. In this work, we characterized the role of the PilS-PilR two-component system in the regulation of the pilA gene expression. Experimental evidence indicates that PilS is autophosphorylated at the His-334 residue, which in turn is transferred to the conserved Asp-53 in PilR. Contrary to other PilS-PilR systems, substitution D53N in PilR resulted in higher activation of the pilA gene. By using a pilA::luxCDABE fusion with different promoter fragments and in vitro DNA-binding assays, we demonstrated the existence of multiple functional PilR binding sites. A regulatory model in which the non-phosphorylated PilR protein directs activation of pilA expression by binding to two sites in the promoter region of this gene is presented.

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Identification of Multicomponent Histidine-Aspartate Phosphorelay System Controlling Flagellar and Motility Gene Expression in Geobacter Species

Cited by 20 publications

References 40 publications

Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1

Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1

Characterizing the interplay between multiple levels of organization within bacterial sigma factor regulatory networks

The unphosphorylated form of the PilR two-component system regulates pilA gene expression in Geobacter sulfurreducens

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