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MR-1 Shewanella Oneidensis Exterior Surface of Omca and Mtrc Are Antibody Recognition Force Microscopy Shows that Outer Membrane Cytochromes OmcA and MtrC Are Expressed on the Exterior Surface of Shewanella oneidensis MR-1 Brian H. Lower, Ruchirej Yongsunthon, Liang Shi, Linda Wildling, Hermann J. Gruber, Nicholas S. Wigginton, Catherine L. Reardon, Grigoriy E. Pinchuk, Timothy C. Droubay, Jean-François Boily and Steven K. Lower Appl. Environ. Microbiol. 2009, 75(9):2931. DOI: 10.1128/AEM.02108-08. Downloaded from Published Ahead of Print 13 March 2009. Updated information and services can be found at: http://aem.asm.org/content/75/9/2931 http://aem.asm.org/ These include: REFERENCES This article cites 28 articles, 8 of which can be accessed free at: http://aem.asm.org/content/75/9/2931#ref-list-1 CONTENT ALERTS Receive: RSS Feeds, eTOCs, free email alerts (when new articles cite this article), more» on August 5, 2014 by guest Information about commercial reprint orders: http://journals.asm.org/site/misc/reprints.xhtml To subscribe to to another ASM Journal go to: http://journals.asm.org/site/subscriptions/ APPLIED AND ENVIRONMENTAL MICROBIOLOGY, May 2009, p. 2931–2935 Vol. 75, No. 9 0099-2240/09/$08.00ϩ0 doi:10.1128/AEM.02108-08 Copyright © 2009, American Society for Microbiology. All Rights Reserved. Antibody Recognition Force Microscopy Shows that Outer Membrane Cytochromes OmcA and MtrC Are Expressed on the Exterior Surface of Shewanella oneidensis MR-1ᰔ Brian H. Lower,1* Ruchirej Yongsunthon,2 Liang Shi,3 Linda Wildling,4 Hermann J. Gruber,4 Nicholas S. Wigginton,5 Catherine L. Reardon,3 Grigoriy E. Pinchuk,3 Timothy C. Droubay,3 Jean-Franc¸ois Boily,6 and Steven K. Lower1 The Ohio State University, Columbus, Ohio 432101; Corning Incorporated, Corning, New York 148312; Pacific Northwest National Laboratory, Richland, Washington 993523; Johannes Kepler University of Linz, A-4040 Linz, Austria4; Ecole Polytechnique Fe´de´rale de Lausanne, CH-1015 Lausanne, Switzerland5; and Umeå University, SE-901 87 Umeå, Sweden6 Downloaded from Received 11 September 2008/Accepted 27 February 2009 Antibody recognition force microscopy showed that OmcA and MtrC are expressed on the exterior surface of living Shewanella oneidensis MR-1 cells when Fe(III), including solid-phase hematite (Fe2O3), was the terminal electron acceptor. OmcA was localized to the interface between the cell and mineral. MtrC displayed a more uniform distribution across the cell surface. Both cytochromes were associated with an extracellular polymeric substance. http://aem.asm.org/ Shewanella oneidensis MR-1 is a dissimilatory metal-reduc- ester of the NHS-PEG-aldehyde linker molecule was then used ing bacterium that is well known for its ability to use a variety to form a covalent linkage between PEG-aldehyde and the of anaerobic terminal electron acceptors (TEAs), including amine groups on the AFM tips (6, 7). Next, anti-MtrC or solid-phase iron oxide minerals, such as goethite and hematite anti-OmcA molecules were covalently tethered to these tips (8, 10). Previous studies suggest that S. oneidensis MR-1 uses via the linker molecule’s aldehyde group. This was accom- outer membrane cytochromes OmcA and MtrC to catalyze the plished by incubating the tips with antibody (0.2 mg/ml) and terminal reduction of Fe(III) through direct contact with the NaCNBH3 as described previously (7). The cantilevers were extracellular iron oxide mineral (2, 8, 10, 15, 16, 20, 21, 23). purchased from Veeco and had spring constant values between on August 5, 2014 by guest However, it has yet to be shown whether OmcA or MtrC is 0.06 and 0.07 N/m, as determined by the thermal method of actually targeted to the external surface of live S. oneidensis Hutter and Bechhoefer (12). MR-1 cells when Fe(III) serves as the TEA. Prior to conducting the Ig-RFM experiments, the specificity In the present study, we used atomic force microscopy of each polyclonal antibody (i.e., anti-OmcA and anti-MtrC) (AFM) to probe the surface of live S. oneidensis MR-1 cells, for OmcA or MtrC was verified by Western blot analysis as using AFM tips that were functionalized with cytochrome- described previously (24, 28). Proteins were resolved by both specific polyclonal antibodies (i.e., anti-OmcA or anti-MtrC). denaturing and nondenaturing polyacrylamide gel electro- This technique, termed antibody recognition force microscopy phoresis (PAGE). Briefly, 2.5 ␮g of purified OmcA or MtrC (Ig-RFM), detects binding events that occur between antibod- (23) was resolved by sodium dodecyl sulfate-PAGE or native ies (e.g., anti-OmcA) on an AFM tip and antigens (e.g., PAGE, transferred to a polyvinylidene difluoride membrane, OmcA) that are exposed on a cell surface. While this is a incubated with either anti-OmcA or anti-MtrC, and then visu- relatively new technique, Ig-RFM has been used to map the alized using the Amersham ECL Plus Western blotting detec- nanoscale spatial location of single molecules in complex tion kit. Anti-OmcA bound exclusively to OmcA, anti-MtrC biological structures under physiological conditions (5, 9, bound exclusively to MtrC, and neither antibody showed cross- 11, 13). reactivity with the other cytochrome. Antibody specificities of Anti-MtrC or anti-OmcA molecules were covalently coupled anti-OmcA and anti-MtrC were also validated by immunoblot to silicon nitride (Si3N4) cantilevers (Veeco or Olympus) via a analysis of S. oneidensis whole-cell lysate (28). flexible, heterofunctional polyethylene glycol (PEG) linker To determine if MtrC or OmcA was expressed on the ex- molecule. The PEG linker consists of an NHS (N-hydroxysuc- ternal surface of live bacteria when Fe(III) served as the TEA, cinimide) group at one end and an aldehyde group at the other Ig-RFM was conducted on wild-type versus ⌬omcA ⌬mtrC end (i.e., NHS-PEG-aldehyde). AFM tips were functionalized double mutant cells. For these experiments, bacteria were cul- with amine groups, using ethanolamine (6, 7). The active NHS tivated anaerobically with Fe(III), in the form of Fe(III) che- lated to nitrilotriacetic acid (NTA), serving as the TEA (19, 23). Growth conditions have been described elsewhere (3, 15) * Corresponding author. Mailing address: School of Environment and were based on previous studies (3, 15, 16, 18) that suggest and Natural Resources, The Ohio State University, 210 Kottman Hall, S. oneidensis 2021 Coffey Rd., Columbus, OH 43210. Phone: (614) 247-1676. Fax: that MR-1 targets OmcA and MtrC to the cell (614) 292-7432. E-mail: [email protected]. surface when Fe(III) serves as the TEA. ᰔ Published ahead of print on 13 March 2009. An Asylum Research MFP-3D-BIO AFM or a Digital In- 2931 2932 LOWER ET AL. APPL.ENVIRON.MICROBIOL. struments Bioscope AFM (16, 17) was used for these experi- ments. The z-piezoelectric scanners were calibrated as de- scribed previously (17). Cells were deposited on a hydrophobic glass coverslip and immersed in imaging buffer (i.e., phos- phate-buffered saline [pH 7.4]). The hydrophobic glass cover- slips were made as described previously (17) using a self-as- sembling silane compound called octadecyltrichlorosilane (OTS; Sigma-Aldrich). S. oneidensis MR-1 cells readily ad- sorbed onto OTS glass coverslips and remained attached to the coverslips during the entire experiment. No lateral cell move- ment was observed during the experiment, consistent with pre- vious studies that used OTS glass to immobilize bacteria (15, 17, 18, 27). The AFM tip was brought into contact with the surface of a bacterium, and the antibody-functionalized tip was repeatedly Downloaded from brought into and out of contact with the sample, “fishing” for a binding reaction with cytochrome molecules that were ex- posed on the external cell surface. Binding events were ob- served upon separating anti-OmcA- or anti-MtrC-functional- ized tips from wild-type S. oneidensis MR-1 cells (Fig. 1). For the wild-type cells, we observed both nonspecific and specific interactions (Fig. 1). The distinction between “specific” and “nonspecific” adhe- http://aem.asm.org/ sion is made by observing the change in slope of the force curve during the retraction process (26). During specific binding (Fig. 1C), the cantilever is initially relaxed as it is pulled away from the sample. Upon further retraction, the ligand-receptor complex becomes stretched and unravels, resulting in a non- linear force profile as noted in references 26 and 16. On the other hand, nonspecific adhesion (Fig. 1C) maintains the same slope during the retraction process because only the cantilever on August 5, 2014 by guest flexes (26). FIG. 1. Retraction force curves for anti-MtrC-functionalized tips Figure 2 summarizes the frequency or probability of observ- (A) and anti-OmcA-functionalized tips (B) that are being pulled away ing a binding event for both anti-OmcA and anti-MtrC tips. ⌬ ⌬ from the surface of living omcA mtrC double mutant (gray dotted Each bar in Fig. 2 represents one experiment in which 500 to line) or wild-type (solid black line) S. oneidensis MR-1. These bacteria were adsorbed onto OTS glass coverslips. (C) Retraction curves ex- 1,000 force curves were collected between one AFM tip and hibiting nonspecific binding, specific binding, or no binding between two to four live bacterial cells. This figure does not make a the AFM tip and the cell surface. distinction between specific and nonspecific binding. It simply shows the frequency of observing an attractive interaction as the antibody-functionalized tip was pulled away from the sur- face of S. oneidensis MR-1. Binding events occurred with roughly the same frequency when wild-type S. oneidensis MR-1 FIG. 2. Histograms showing the frequency of observing a binding event for anti-MtrC-functionalized (blue) or anti-OmcA-functionalized (red) AFM tips on live wild-type S.
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