Flagella act as Geobacter biofilm scaffolds to stabilize biofilm and facilitate extracellular electron transfer

Liu, Xing; Zhuo, Shiyan; Jing, Xianyue; Yuan, Yong; Rensing, Christopher; Zhou, Shungui

doi:10.1016/j.bios.2019.111748

Cited by 74 publications

(41 citation statements)

References 59 publications

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“…The outer membrane proteins were separated following the previously published method that cells were collected at the late log phase and outer membrane proteins were precipitated by filtration through a membrane with a molecular weight cutoff of 3 kDa (Amicon Ultra centrifugal filter, Merck, Darmstadt, Germany) (Liu et al, ). The extracellular cytochromes in the anode biofilm were extracted together with the extracellular polymeric substances as previously described (Liu, Zhuo, et al, ). Briefly, the anode biofilm was collected and resuspended in 0.9% NaCl.…”

Section: Methodsmentioning

confidence: 99%

Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Liu

Yin

Xiao

et al. 2019

Molecular Microbiology

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The electrically conductive pili (e-pili) of Geobacter species enable extracellular electron transfer to insoluble metallic minerals, electrodes and other microbial species, which confers biogeochemical significance and global prevalence on Geobacter in diverse anaerobic environments. E-pili are constructed by truncated PilA which is considered to have evolved from full-length pilin by gene fission under positive evolutionary selection. However, this hypothesis is based on phylogenetic analysis and has not yet been experimentally confirmed. Here, we reconstructed an ancestral strain of G. sulfurreducens (designated COMB) carrying full-length PilA by combining genes GSU1496 and GSU1497. The results demonstrated that strain COMB expressed and assembled the full-length fused PilA and exhibited an outer membrane c-type cytochrome profile similar to the wild-type strain. Surprisingly, the generated COMB-pili were also conductive, indicating the evolution of truncated PilA did not occur for conductivity. Moreover, strain COMB minimally reduced Fe(III) oxides but maintained its ability to respire electrodes, demonstrating the truncation of pilin enables iron respiration. This study provides the first experimental evidence that the truncation of pilin in Geobacter species confers adaption to Fe(III)-mineral-mediated selective pressures, and suggests an evolutionary event during which the separation of the GSU1497 gene helped Geobacter survive and thrive in natural environments. K E Y W O R D S adaptive evolution, dissimilatory iron reduction, e-pili, Geobacter sulfurreducens, truncated pilin S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Liu X, Ye Y, Xiao K, Rensing C, Zhou S. Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments. Mol Microbiol. 2020;113:783-793.

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Section: Methodsmentioning

confidence: 99%

Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Liu

Yin

Xiao

et al. 2019

Molecular Microbiology

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“…It is known that motility may help bacteria to reach interfaces appropriate for biofilm construction and to penetrate into an existing biofilm and it may also be involved in biofilm spreading over a surface (Houry et al ., 2010). Flagella play an important role in controlling bacterial motility, and thereby maintaining the stability of biofilm and promoting extracellular electron transfer (Liu et al ., 2019b). In addition, flagellum is also recognized as a microbial sensory organelle to sense environmental stresses (Belas, 2014).…”

Section: Discussionmentioning

confidence: 99%

Cadmium sulfide nanoparticle biomineralization and biofilm formation mediate cadmium resistance of the deep‐sea bacterium Pseudoalteromonas sp. MT33b

Sun

2021

Environ Microbiol Rep

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Cadmium (Cd) is a common toxic heavy metal in the environment, and bacteria have evolved different strategies to deal with Cd toxicity. Here, a bacterium designated Pseudoalteromonas sp. MT33b possessing strong Cd resistance was isolated from the Mariana Trench sediments. Supplement of cysteine significantly increased bacterial Cd resistance and removal rate. Biofilm formation was demonstrated to play a positive role toward bacterial Cd resistance. Transcriptome analysis showed the supplement of cysteine effectively prevented Cd 2+ from entering bacterial cells, promoted saccharide metabolism and thereby facilitating energy production, which consists well with bacterial growth trend analysed under the same conditions. Notably, the expressions of many biofilm formation related genes including flagellar assembly, signal transduction, bacterial secretion and TonB-dependent transfer system were significantly upregulated when facing Cd stress, indicating their important roles in determining bacterial biofilm formation and enhancing Cd resistance. Overall, this study indicates the formation of insoluble CdS precipitates and massive biofilm is the major strategy adopted by Pseudoalteromonas sp. MT33b to eliminate Cd stress. Our results provide a good model to investigate how heavy metals impact biofilm formation in the deep-sea ecosystems, which may facilitate a deeper understanding of microbial environmental adaptability and better utilization of these microbes for bioremediation purposes in the future.

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“…The idea of the role of flagella as a mechanical support in a biofilm has been previously suggested in Escherichia coli macrocolony biofilms but was yet to be demonstrated (44). An additional observation to support the possible spatial contribution of flagella is the observation of Geobacter sulfurreducens electrochemical chamber biofilm, using their flagella for cytochromes' spatial arrangement (45). To investigate this possibility, we constructed a P. aeruginosa-flagella knockout (KO) strain.…”

Section: The Possible Structural Importance Of Flagella In a Biofilmmentioning

confidence: 99%

An inside look at a biofilm: Pseudomonas aeruginosa flagella biotracking

et al. 2021

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The opportunistic pathogen, Pseudomonas aeruginosa, a flagellated bacterium, is one of the top model organisms for biofilm studies. To elucidate the location of bacterial flagella throughout the biofilm life cycle, we developed a new flagella biotracking tool. Bacterial flagella were site-specifically labeled via genetic code expansion. This enabled us to track bacterial flagella during biofilm maturation. Live flagella imaging revealed the presence and synthesis of flagella throughout the biofilm life cycle. To study the possible role of flagella in a biofilm, we produced a flagella knockout strain and compared its biofilm to that of the wild-type strain. Results showed a one order of magnitude stronger biofilm structure in the wild type in comparison with the flagella knockout strain. This suggests a possible structural role for flagella in a biofilm, conceivably as a scaffold. Our findings suggest a new model for biofilm maturation dynamic which underscores the importance of direct evidence from within the biofilm.

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Flagella act as Geobacter biofilm scaffolds to stabilize biofilm and facilitate extracellular electron transfer

Cited by 74 publications

References 59 publications

Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Cadmium sulfide nanoparticle biomineralization and biofilm formation mediate cadmium resistance of the deep‐sea bacterium Pseudoalteromonas sp. MT33b

An inside look at a biofilm: Pseudomonas aeruginosa flagella biotracking

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