Atomic force microscopy measurements of bacterial adhesion and biofilm formation onto clay-sized particles

Huang, Qiaoyun; Wu, Huayong; Cai, Peng; Fein, Jeremy B.; Chen, Wenli

doi:10.1038/srep16857

Cited by 134 publications

(107 citation statements)

References 52 publications

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“…38,39 The goethite is a kind of nanoparticle mineral and the goethite-coated surface may be unsuitable for cell growth (Figs. 3, 4).…”

Section: Discussionmentioning

confidence: 99%

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Bacillus subtilis biofilm development in the presence of soil clay minerals and iron oxides

Peng

Walker

et al. 2017

npj Biofilms Microbiomes

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Clay minerals and metal oxides, as important parts of the soil matrix, play crucial roles in the development of microbial communities. However, the mechanism underlying such a process, particularly on the formation of soil biofilm, remains poorly understood. Here, we investigated the effects of montmorillonite, kaolinite, and goethite on the biofilm formation of the representative soil bacteria Bacillus subtilis. The bacterial biofilm formation in goethite was found to be impaired in the initial 24 h but burst at 48 h in the liquid–air interface. Confocal laser scanning microscopy showed that the biofilm biomass in goethite was 3–16 times that of the control, montmorillonite, and kaolinite at 48 h. Live/Dead staining showed that cells had the highest death rate of 60% after 4 h of contact with goethite, followed by kaolinite and montmorillonite. Atomic force microscopy showed that the interaction between goethite and bacteria may injure bacterial cells by puncturing cell wall, leading to the swarming of bacteria toward the liquid–air interface. Additionally, the expressions of abrB and sinR, key players in regulating the biofilm formation, were upregulated at 24 h and downregulated at 48 h in goethite, indicating the initial adaptation of the cells to minerals. A model was proposed to describe the effects of goethite on the biofilm formation. Our findings may facilitate a better understanding of the roles of soil clays in biofilm development and the manipulation of bacterial compositions through controlling the biofilm in soils.

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“…38,39 The goethite is a kind of nanoparticle mineral and the goethite-coated surface may be unsuitable for cell growth (Figs. 3, 4).…”

Section: Discussionmentioning

confidence: 99%

“…39 Briefly, 0.4 mL of the ultrasound mineral suspensions (1 g L −1 ) were pipetted onto the circle coverslips and the minerals onto the glass substrate were boiled at 120 °C for 20 min. Then deionized water was used to rinse the coverslips and dried at 60 °C.…”

Section: Methodsmentioning

confidence: 99%

Bacillus subtilis biofilm development in the presence of soil clay minerals and iron oxides

Peng

Walker

et al. 2017

npj Biofilms Microbiomes

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“…The deflection sensitivity, α s , of the cantilever was recorded on bare glass to calculate the applied normal force, F n , usingwhere K n is the cantilever stiffness (0.046 ± 0.002 N m −1 ; average over 26 cantilevers) and V n is the voltage output from the AFM photodiode due to cantilever deflection. Bacteria were immobilized on the tipless cantilevers (NPO, Bruker AFM Probes, Camarillo, CA, USA) via electrostatic interaction with poly-L-lysine (PLL; Sigma-Aldrich, USA) using a micromanipulator (Narishige Groups, Tokyo, Japan) 35 . The far end of the cantilever was dipped in a droplet of PLL for 1 min and dried in air (2 min), followed by 1 min immersion in a droplet of greatly diluted, bacterial suspension (3 × 10 6 bacteria mL −1 ) to let a bacterium adhere.…”

Section: Methodsmentioning

confidence: 99%

Detachment and successive re-attachment of multiple, reversibly-binding tethers result in irreversible bacterial adhesion to surfaces

Sjollema

Mei

Hall

et al. 2017

Sci Rep

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Bacterial adhesion to surfaces occurs ubiquitously and is initially reversible, though becoming more irreversible within minutes after first contact with a surface. We here demonstrate for eight bacterial strains comprising four species, that bacteria adhere irreversibly to surfaces through multiple, reversibly-binding tethers that detach and successively re-attach, but not collectively detach to cause detachment of an entire bacterium. Arguments build on combining analyses of confined Brownian-motion of bacteria adhering to glass and their AFM force-distance curves and include the following observations: (1) force-distance curves showed detachment events indicative of multiple binding tethers, (2) vibration amplitudes of adhering bacteria parallel to a surface decreased with increasing adhesion-forces acting perpendicular to the surface, (3) nanoscopic displacements of bacteria with relatively long autocorrelation times up to several seconds, in absence of microscopic displacement, (4) increases in Mean-Squared-Displacement over prolonged time periods according to tα with 0 < α ≪ 1, indicative of confined displacement. Analysis of simulated position-maps of adhering particles using a new, in silico model confirmed that adhesion to surfaces is irreversible through detachment and successive re-attachment of reversibly-binding tethers. This makes bacterial adhesion mechanistically comparable with the irreversible adsorption of high-molecular-weight proteins to surfaces, mediated by multiple, reversibly-binding molecular segments.

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“…The AFM morphology measurements were made following Huang et al . (). NanoScope Analysis software (version 1.5, Bruker Corporation, Karlsruhe, Germany) was used to process the image data.…”

Section: Methodsmentioning

confidence: 97%

Copper adsorption on composites of goethite, cells of Pseudomonas putida and humic acid

Lin

Chen

et al. 2017

European J Soil Science

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In the soil environment, iron oxides co‐occur commonly with different types of organic constituents to produce iron oxide–organic composites that play an important role in the biogeochemical cycling of trace metals. We investigated copper (Cu) adsorption on synthetic goethite, Pseudomonas putida (CCTCC M209319) bacterial cells, humic acid (HA) and their binary and ternary composites with batch adsorption experiments coupled with isothermal titration calorimetry (ITC). Morphological characterizations show that the three components can form closely combined and heterogeneous aggregates with one another. The kinetics of sorption of Cu to these composite materials conforms to the pseudo‐second‐order model, whereas the Cu sorptivities deviate from linear additivity. Specifically, Cu sorptivities on the binary goethite–P. putida and P. putida–HA and ternary goethite–P. putida–HA composites are less than expected assuming additivity, whereas the opposite is seen for the binary goethite–HA composite. There is considerable masking of adsorption sites in the ternary goethite–P. putida–HA system, but the binding sites on bacteria are not completely covered, as shown by the adsorption enthalpy and entropy (19.60 kJ mol−1 and 120.9 J mol−1 K−1, respectively) for the ternary composite. We conclude that the binding affinity of Cu for the binary goethite–humic acid composite is larger than that for the bacterial composites with goethite or humic acid, or both. This research indicates that bacteria, iron oxide and humic substances exhibit different behaviour in the sequestration of heavy metals when they form various binary and ternary complexes in natural environments. Highlights How does mineral–organic interaction affect the binding behaviour of trace elements? First investigation of Cu sorption to goethite–bacteria–humic acid composites. Goethite–HA shows enhanced Cu adsorption, whereas the opposite is true for bacterial complexes. Various bacteria–iron oxide–humic substance composites behave differently in metal sequestration.

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Atomic force microscopy measurements of bacterial adhesion and biofilm formation onto clay-sized particles

Cited by 134 publications

References 52 publications

Bacillus subtilis biofilm development in the presence of soil clay minerals and iron oxides

Bacillus subtilis biofilm development in the presence of soil clay minerals and iron oxides

Detachment and successive re-attachment of multiple, reversibly-binding tethers result in irreversible bacterial adhesion to surfaces

Copper adsorption on composites of goethite, cells of Pseudomonas putida and humic acid

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