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Quantifying the relationship between microbial attachment and mineral surface dynamics using vertical scanning interferometry (VSI)

K. J. Davis^*, and A. Lüttge^*,**

^* Department of Earth Science, Rice University, 6100 Main Street, Houston, Texas 77005, U.S.A
^** Center for Biological and Environmental Nanotechnology, Rice University, Houston, Texas 77005, U.S.A

Corresponding author: K. J. Davis, kjdavis{at}rice.edu

	ABSTRACT

TOP ABSTRACT introduction the application of vsi... experimental methods results and discussion summary and conclusions REFERENCES

 
A major challenge of biogeochemistry is to resolve the precise manner by which microbial activity influences mineral-surface reactions. Although a prerequisite for biological activity at a surface is substrate recognition and attachment, probing the nature of this biological-geological interface is inherently difficult. While atomic force microscopy (AFM) is a powerful high-resolution imaging technique capable of quantifying mineral-surface and microbial cell structure, it suffers from the invasive nature of tip-sample interactions and a limited field of view. A noninvasive imaging technique is needed that can detect the microbe at the surface and quantify any resulting changes in mineral-surface topography, while maintaining both a high spatial resolution and a large field of view. Vertical scanning interferometry (VSI) meets these requirements and enables the measurement of both local dissolution (etch pits) and global dissolution rates (surface normal retreat). Here we use AFM and VSI as complementary techniques to evaluate the influence of mineral-surface dynamics on the surface colonization of carbonate surfaces by Shewanella oneidensis MR-1. It was found that 1) surface colonization occurred more slowly on actively dissolving calcite surfaces than on the less dynamic dolomite and magnesite surfaces; 2) cell attachment reduced calcite dissolution rates by more than 40 percent relative to cell-free controls; 3) surface microtopographical features such as etch pits provide high-energy sites that favor microbial attachment. These results indicate the existence of a complex relationship between microbial surface colonization and mineral-surface dynamics that deserves additional study. Further, this study demonstrates that VSI is an effective method for quantifying mineral-reaction rates in the context of microbial attachment. Direct comparisons with atomic force microscope (AFM) measurements also established VSI as a capable technique for making ex situ measurements of cell and biofilm dimensions on the surface. Accordingly, VSI should be considered a valuable complement to those powerful tools already available to the geomicrobiologist for quantification of processes occurring at the microbe-mineral interface.

	introduction

TOP ABSTRACT introduction the application of vsi... experimental methods results and discussion summary and conclusions REFERENCES

 

Importance of Microbial Attachment in Biogeochemical and Engineered Systems

Over this same period, there has evolved an increasing realization in the earth sciences that many critical geochemical mineral-surface processes are mediated by microbial activity (Banfield and others, 1998; Ehrlich, 1998; Ehrlich, 1999). While microorganisms can modify mineral reaction rates by altering the chemical environment, physical attachment to the mineral-substrate may be of the most direct consequence to surface-controlled processes. Microbes attach to mineral surfaces for a variety of reasons. First, many nutrients tend to concentrate at surfaces (ZoBell, 1943). Surface-associated bacteria are able to utilize these nutrients for growth allowing them to multiply at the solid-water interface under conditions in which they are unable to multiply in the bulk aqueous phase (Marshall, 1996). Secondly, some minerals themselves serve as energy sources for microbial metabolism. The best-known example of this is the coupling of organic carbon oxidation to the dissimilatory reduction of Fe and Mn (Lovely and Phillips, 1988; Nealson and Myers, 1992). Microbial attachment to metal oxide surfaces is often requisite for taking advantage of this metabolic pathway (Arnold and others, 1988; DiChristina and Delong, 1994), although extracellular electron shuttle compounds, such as humics (Lovley and others, 1996; Lovley and Blunt-Harris, 1999) and quinones (Newman and Kolter, 2000; Rosso and others, 2003), also play a role. Additionally, microbes colonize surfaces as a general response to a range of environmental stresses where surface attachment offers protection and the opportunity for synergistic relationships with other cells (Dawson and others, 1981; Kjelleberg and Hermansson, 1984). Whatever the primary cause of microbial attachment, surface colonization generally results in degradation of the mineral surface and a considerable increase in the total reactive surface area. During this process, microbes produce acids, bases, and ligands that interact with the mineral surface, promoting mineral dissolution and the formation of secondary mineral phases (Bennett and others, 1996; Barker and others, 1997; Ehrlich, 1998). Where conditions in the natural environment favor microbial surface colonization, microbial processes can be expected to influence observed mineral dissolution rates.

Critical Questions that Require Further Study

1. How do the properties of the mineral surface influence bacterial attachment? In other words, what are the surface-structural controls on bacterial attachment?

The majority of experimental work has been carried out to discern the environmental and metabolic conditions that favor microbial attachment to various substrates (Grasso and others, 1996). However, little is known about the controls exerted by the microstructure of the surface on surface colonization. Engineering studies have correlated microbial attachment with the surface roughness of industrially significant materials (Scheuerman and others, 1998). Likewise, the degree to which environmental samples are etched has been shown to affect bacterial colonization (Bennett and Hiebert, 1992; Hiebert and Bennett, 1992; Bennett and others, 1996). However, microbial interactions with specific topographic features, especially submicron features, remain largely unresolved. While atomic force microscopy (AFM) has been used with considerable success to measure forces between bacteria and various substrates (Lower and others, 2000, 2001a, 2001b), this technique has only recently been applied to discern attachment forces between bacteria and certain topographic features (Boyd and others, 2002). It is critical that such studies begin to yield a mechanistic understanding of the interaction between microbes and microtopography, so that the precise role that surface microstructure plays in directing bacterial colonization may be resolved.

2. What is the mechanism by which bacterial attachment modifies mineral dissolution rates? What are the consequences of bacterial attachment on the microtopographic features known to control abiotic dissolution rates?

Just as important as understanding microtopographical controls on surface colonization, is determining the manner by which microbial attachment, in turn, modifies the structure and development of the surface. This is especially significant given the known dependence of surface-controlled mineral reaction rates on the microstructure of the surface. Numerous AFM studies have demonstrated the dependence of layer-by-layer growth or dissolution on the formation of growth spirals and etch pits at surface defects (Gratz and others, 1993; Liang and others, 1996; Jordan and Rammensee, 1998; Pina and others, 1998; Teng and others, 1998; Davis and others, 2000; Higgins and others, 2000; Teng and others, 2000; Risthaus and others, 2001; Davis and others, 2004). The more recent use of vertical scanning interferometry (VSI) has successfully correlated observations of etch pit formation with surface normal retreat and global dissolution rates (Lüttge and others, 1999; Arvidson and others, 2003, 2004). A conceptual model for mineral dissolution has been inferred from these interferometric measurements of surface topography (Lasaga and Lüttge, 2001, 2003). The resultant comprehensive dissolution rate theory successfully integrates individual surface reactions into an overall rate. These studies provide a conceptual abiotic framework by which the biological influence on mineral-dissolution rates may be compared.

3. How does the dynamic nature of the actively dissolving mineral surface affect bacterial attachment. For instance, can the dissolving surface retreat beneath the attached bacteria, thereby enhancing the probability of detachment? Additionally, what is the relationship between mineral solubility and the role of microbial surface colonization in weathering reactions?

To date, most investigations have studied microbial attachment to either inert surfaces or slowly dissolving surfaces. The precise role of mineral solubility, and hence dissolution rate, in determining the extent and rate of microbial surface colonization is largely unknown.

Quantifying Microbe-Mineral Interactions –A Challenge

vertical scanning interferometry (vsi)

Vertical scanning interferometry (VSI) is a type of interferometry that is optimized for the wide dynamic range needed to image rough surfaces. It typically uses a white light illumination source, which allows for large vertical scans (up to 100 µm with better than 2 nm resolution). Since the coherence length is short due to the wide spectral bandwidth of the white-light source, good contrast fringes are only obtained when the two path lengths of the interferometer are closely matched in length. Therefore, the interferometer is aligned so that the interference intensity distribution along the vertical scanning direction has its peak (best contrast fringes) at the best focus position. While many algorithms are employed to analyze white light interferograms, all of them generally detect the coherence peak.

Although VSI is primarily used for non-destructive testing of semiconductors, it has also been used with considerable success to measure mineral-surface kinetics (Lüttge and others, 1999, 2003; Arvidson and others, 2003, 2004). This success stems from the speed, precision and versatility by which VSI produces quantitative topographic maps of the mineral surface. Images made at 50x magnification using white-light illumination provide a lateral resolution of 0.5 µm, while maintaining a vertical resolution on the order of 1 to 2 nm. The scan size at this magnification is 165 x 125 µm, a little larger than the maximum AFM scan size of 130 x 130 µm. However, interference objectives can be easily switched via a turret providing, for instance, 10x magnification with a field of view of 845 x 630 µm. When larger scan areas are needed, a "stitching" procedure can be employed in which a number of overlapping measurements are combined into one surface profile using an automated positioning stage and sub-pixel registration techniques. VSI employs a 2 µm/s vertical scan rate allowing for extremely fast data acquisition. For instance, a surface area of 1 mm² with 20 µm of surface relief can be quantified in less than ten seconds.

Since interferometry measures relative surface height, absolute changes in mineral-surface topography must be measured relative to a reference surface. This is achieved by placing an inert mask on the surface. By measuring the average height difference between the reacted and unreacted surfaces, an absolute value of surface normal retreat may be determined. Thus, during dissolution, changes in average height made at time intervals t yields a surface normal retreat velocity, _[hkl]:

Dividing this velocity by the molar volume (cm³/mol) gives a global dissolution rate in the familiar units of moles per unit area per unit time:

This approach allows a simple and straightforward calculation of surface-area retreat or advance rates from measurements of average surface heights () (Lüttge and others, 1999). In addition to these global dissolution rates, local dissolution rates at etch pits can be quantified by monitoring changes in the volume and density of etch pits across the surface over time.

The key to achieving accurate measurements of mineral-reaction rates using this masking technique is the large vertical scan range and field of view available using VSI. For instance, AFM can in principal be used to measure surface retreat rates relative to a masked reference surface. However, the relatively small vertical scan range (7 µm) and lateral scan size of AFM makes it impossible to achieve accurate measurements of surface reaction rates. Even using VSI it is clear that the 10x objective provides a much more accurate measurement of surface normal retreat than is determined using the 50x objective. This is because the limited field of view provided by the 50x objective is more sensitive to influences from local dissolution features and reaction artifacts associated with the mask edge.

	the application of vsi to the quantification of mineral surface dynamics in the context of microbial attachment

TOP ABSTRACT introduction the application of vsi... experimental methods results and discussion summary and conclusions REFERENCES

 
While VSI is becoming a standard technique for the quantification of mineral-surface reactions in inorganic systems, its application to microbial systems has not been fully evaluated. Only one previous study has attempted to use VSI to investigate microbe-mineral interactions (Lüttge and Conrad, 2004). In this work, surface colonization by Shewanella oneidensis MR-1 was observed to prevent the opening of etch pits on the calcite surface, despite undersaturated solution conditions. The authors hypothesized that this dissolution mechanism was dependent upon both the biomass to surface area ratio and the rate at which the etch pits opened. Unfortunately, these experiments used a high cell titer and small reaction volume, thereby precluding any possibility of large-scale calcite dissolution from occurring. Yet, this study raises an interesting question: what is the relationship between microbial surface colonization and the dynamics of the surface (that is dissolution rate)? If microbial attachment influences the dissolution of the surface, can surface dissolution, in turn, affect microbial attachment?

Here we further investigate the relationship between microbial surface colonization and mineral-surface dynamics by examining three key interactions:

1. The rate of cell attachment as a function of carbonate dissolution rate
   
2. Calcite dissolution rate in the presence of microbial cells versus a cell-free control
   
3. The role of mineral-surface topography in determining cell attachment
   

A second goal of this paper is to further evaluate the applicability of VSI to the quantitative study of mineral-surface reactions in the context of microbial attachment. To this end, VSI measurements of cell and biofilm dimensions will be directly compared to those obtained using the more commonly used quantitative imaging technique, AFM.

	experimental methods

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Mineral-Surface Selection and Preparation

Shewanella Culture Preparation and Controls

Shewanella oneidensis MR-1 cultures were obtained from Kenneth Nealson’s lab (University of Southern California) and aerobically cultured in a pH 7.4, low-nutrient medium, prepared to 1L using: 200 mg yeast extract, 100 mg peptone, 10 mL 1M HEPES, 10 mL 0.2M bicarbonate and 20 mL 1M lactate. The culture was allowed to enter stationary phase as monitored by spectrophotometric absorbance measurements, with a final A600 reading of 0.15, corresponding to a cell titer of 3x10⁸ cells/mL. Two portions of this culture were used as control solutions. The first control was a cell-free extract that was prepared through centrifugation of the culture at 9000 rpm for 30 min. The supernatant was decanted from the pellet and the centrifugation step repeated twice more. Following this procedure, the spectrophotometric absorbance A600 of the solution fell to 0. A second dead-cell control was prepared by heat-killing the cells through incubation above 45°C and below 55°C for 2.5 hours and then allowing the culture to cool and repeating the cycle two more times. The measured spectroscopic absorbance A600 of the solution fell to 0.12 during this procedure. Viability of the dead-cell control was assessed by counting the number of colony-forming units (cfu) per volume plated on Luria-Bertani (LB) agar plates. It was determined that less than 1 bacterial cell per mL of culture was microbiologically viable.

Reaction Conditions

VSI And AFM Imaging and Measurements

Measurements of cell densities on the carbonate surfaces were made by counting the number of cells per area in randomly selected images or portions of images. Averages of at least 20 separate counts are reported in tables 1 and 2. When available, AFM observations were found to confirm the VSI cell density measurements. Global dissolution rates were measured after 35 hours for at least two masks per mineral species and for at least two crystals for each mineral species. At least ten transects were measured along each mask, paying careful attention to taking transects along a single continuous terrace to avoid error from natural surface steps.

	results and discussion

TOP ABSTRACT introduction the application of vsi... experimental methods results and discussion summary and conclusions REFERENCES

 

Surface Colonization on Carbonate Surfaces

View larger version (72K): [in this window] [in a new window]   Fig. 1. 3D plots of VSI data sets showing progressive surface colonization by Shewanella on dolomite over 35 hours. (A) honeycomb morphology after 9 hours; (B) beginning of monolayer surface coverage after 18 hours of exposure; (C) after 25 hours, most of the central regions of the crystal surface were covered by a continuous monolayer of cells. (All images were captured using a 50x interferometric objective yielding image sizes of 165 x 125 µm.)

View larger version (59K): [in this window] [in a new window]   Fig. 2. 2D VSI image of Shewanella surface colonization on a magnesite surface after 9 hours. This early biofilm consists of taller (bright-yellow) cells and associated lower (dark yellow) organic material.

View larger version (29K): [in this window] [in a new window]   Fig. 3. Cross-section measurements of a single Shewanella cell on a dolomite surface and its associated organic material. Here, the cell is 650 nm in diameter, 3 microns long, and the associated organic material rises 200 nm above the crystal surface.

View larger version (67K): [in this window] [in a new window]   Fig. 4. 2D VSI image of entrenched cells on calcite following the removal of associated organic material. (9 hours exposure to Shewanella culture.)

View larger version (51K): [in this window] [in a new window]   Fig. 5. The removal of associated organic material revealed the clear presence of Shewanella microcolonies on the calcite surface. The initial stages of surface colonization were often characterized by microcolony formation. (A) 2D VSI image; (B) 3D reconstruction of microcolonies in the context of natural surface topography. (8 hours of exposure to Shewanella cultures.)

View larger version (84K): [in this window] [in a new window]   Fig. 6. The role of mineral-surface microtopography in determining cell attachment on calcite. This image is a 3D representation of a VSI data set that was generated using the SPIP 3.0 software package (www.imagemet.com). The bright-yellow peaks are bacterial cells. Two cells are attached lengthwise along a macrostep; one cell is attached to the center of an etch pit; one cell is attached to a flat terrace. The etch pits are between 75 and 142 nm deep. The macrostep is 230 nm tall. The microbe in the center of the etch pit is 560 nm tall and 3.5 microns in length. The microbe attached to the surface is 325 nm tall and 2.0 microns in length. The two cells attached lengthwise to the step are between 475 and 525 nm in height and 2.0 to 2.75 microns in length. This image indicates that while cell alignment may occur along energetically favorable attachment sites, the availability of such sites did not limit surface colonization.

While bacterial cell dimensions are near the lateral resolution limits of the 50X interferometric objective used in VSI, higher-resolution AFM imaging provided concise images of microbes at the mineral-surface (figs. 7 and 8A). In fact cell structures such as flagella are easily resolved using AFM (fig. 8B). However, despite the resolution difference between the two techniques, VSI measurements of cell diameter and length (fig. 9) were found to be very comparable to those measured using AFM. This is an interesting result given that the lower resolution of VSI causes the shape outline of the cells to appear somewhat diffuse. Fortunately, the optical nature of VSI that is responsible for such limitations in lateral resolution also confers certain advantages to VSI over AFM. The noninvasive nature of VSI imaging does not suffer from the tip-sample interactions inherent to AFM imaging that can cause bacterial cells to dislodge from the surface during imaging. Further, the large field of view and fast data acquisition allows VSI to quickly assess attached cell density over the entire crystal surface. Although not studied here, the large vertical scan range characteristic of VSI may even allow for the quantification of developing biofilm structures up to 100 µm above the surface. These capabilities make VSI a strong complement to the in situ high-resolution imaging abilities of AFM. The coupling of these two techniques allows for mineral-surface reactions and cell-mineral interface processes to be quantified at multiple length-scales.

View larger version (67K): [in this window] [in a new window]   Fig. 7. FM images of Shewanella surface colonization on a dolomite surface after 35 hours. (A) height image; (B) deflection (amplitude) plot.

View larger version (51K): [in this window] [in a new window]   Fig. 8. High-resolution deflection AFM images of Shewanella cells on a dolomite surface. (A) A recently divided cell; (B) a rare example of a flagellum that is still attached to a Shewanella cell.

View larger version (31K): [in this window] [in a new window]   Fig. 9. Cross-section of a recently divided cell on a calcite surface. The individual cells measure 400 and 440 nm in diameter and 2.5 microns in length. VSI measurements such as these can yield accurate measurements of cell dimensions that compare favorably with those obtained using more common ex situ AFM techniques.

View larger version (47K): [in this window] [in a new window]   Fig. 10. Images showing the extent of dissolution between masked and unmasked areas of a calcite crystal following 4 hours of reaction in the cell-free control solutions. Both images show portions of the same masked area with the only difference being the magnification of the interferometric objective used. The previously masked portion of the calcite surface is apparent as the smooth (unetched) surface in the upper-left quadrant of the image.

View larger version (47K): [in this window] [in a new window]   Fig. 11. Images showing the masked and unmasked regions of a dolomite crystal surface following 4 hours of exposure to Shewanella cells. These VSI images reveal that no dolomite dissolution occurred during the reaction period. Instead, a number of Shewanella cells have deposited on the surface along with a thin organic film. The unreacted surface (previously masked) is apparent as the smooth surface on the left side of these images.

View larger version (63K): [in this window] [in a new window]   Fig. 12. VSI images showing differences in Shewanella surface colonization on calcite, dolomite and magnesite surfaces after 8 and 35 hours of exposure to microbial cultures. Average measured cell densities for the respective crystal surfaces are given in table 1. Here, only images that have had most of the associated organic material removed are shown. Counts were primarily conducted on crystal surfaces that had only undergone the initial standardized washing procedure, although no statistical difference in cell density measurements was observed following the second washing procedure. (All images are 125 x 165 µm.)

View larger version (99K): [in this window] [in a new window]   Fig. 13. VSI image of Shewanella surface colonization on the calcite surface after 35 hours. The majority of cells were found to occupy the rims of large etch pits, indicating that microbial attachment may be less favorable near dissolution centers where the surface is most dynamic.

View larger version (72K): [in this window] [in a new window]   Fig. 14. VSI data of calcite dissolution relative to masked portions of the crystal surface after 35 hours of exposure to cell-free controls and Shewanella cell cultures. 10X and 50X images of the same masked region are shown for comparison. Average measurements of calcite dissolution for the two systems are given in table 3. Here the unreacted portions of the surface occupy the left side of the images.

View larger version (70K): [in this window] [in a new window]   Fig. 15. VSI images of surface colonization on barite and dolomite surfaces after 4 hours. Attached cell density was significantly higher on the pre-etched surfaces than on the pristine cleavages surfaces. Average measurements of attached cell densities are given in table 2. (All images are 125 x 165 µm).

View larger version (88K): [in this window] [in a new window]   Fig. 16. AFM image of pre-etched dolomite surface revealing extremely rough surface steps that are not observable using VSI.

View larger version (145K): [in this window] [in a new window]   Fig. 17. AFM images of cell attachment on pre-etched dolomite and barite surfaces. Dissolution features like those shown in figure 16 are not visible in these images because of the much greater vertical scale employed to accommodate both bacterial cells and surface features (A) height image of dolomite surface; (B) corresponding deflection (amplitude) plot; (C) height image of barite surface; (D) corresponding deflection (amplitude) plot.

	summary and conclusions

TOP ABSTRACT introduction the application of vsi... experimental methods results and discussion summary and conclusions REFERENCES

In this study, AFM and VSI were used in synergistic fashion to achieve a beginning understanding of the interplay between mineral-surface dynamics and microbial attachment. Our results indicate that when the dissolution rate of the surface is comparable to the rate of surface colonization, surface dynamics may be a significant factor in determining cell attachment. This was found to be the case for calcite where significant surface retreat resulted in reduced Shewanella surface colonization. In further support of this finding, the most dynamic areas of the surface (etch pits) were found to provide additional local barriers to cell attachment. However, the cells that did attach to the calcite surface affected surface dynamics by reducing the overall far from equilibrium dissolution rate. In contrast to the findings for calcite, dissolution features on the slower-dissolving dolomite and barite surfaces actually resulted in faster surface colonization rates by providing energetically favorable sites for cell attachment. This complicated relationship between surface colonization and mineral-surface development reinforces the central theme of biogeochemistry that the evolution of geological surfaces and biological systems are intertwined. However, the significance of these relationships to biogeochemical and engineered systems requires further investigation.

	acknowledgments

 
The authors wish to thank Kenneth Nealson and Randa Abboud (University of Southern California) for generously providing the Shewanella cultures used in this study. The authors also gratefully acknowledge support for this study from the Department of Energy (grant#DE-FG03-02ER63427), and the Nanoscale Science and Engineering Initiative of the National Science Foundation under NSF Award Number EEC-0118007 (to A. Lüttge). In addition, the authors would like to thank Catherine Skinner, Javiera Cervini-Silva, and Rob Rye, for extremely helpful and insightful reviews of this manuscript.

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