Au-Interaktion af SLP1 Polymerer og Monolayer fra<em> Lysinibacillus sphaericus</em> JG-B53 - QCM-D, ICP-MS og AFM som Værktøjer til biomolekyle-metal Studies
Summary
To obtain basic information on the sorption and recycling of gold from aqueous systems the interaction of Au(III) and Au(0) nanoparticles on S-layer proteins were investigated. The sorption of protein polymers was investigated by ICP-MS and that of proteinaceous monolayers by QCM-D. Subsequent AFM enables the imaging of the nanostructures.
Abstract
In this publication the gold sorption behavior of surface layer (S-layer) proteins (Slp1) of Lysinibacillus sphaericus JG-B53 is described. These biomolecules arrange in paracrystalline two-dimensional arrays on surfaces, bind metals, and are thus interesting for several biotechnical applications, such as biosorptive materials for the removal or recovery of different elements from the environment and industrial processes. The deposition of Au(0) nanoparticles on S-layers, either by S-layer directed synthesis 1 or adsorption of nanoparticles, opens new possibilities for diverse sensory applications. Although numerous studies have described the biosorptive properties of S-layers 2-5, a deeper understanding of protein-protein and protein-metal interaction still remains challenging. In the following study, inductively coupled mass spectrometry (ICP-MS) was used for the detection of metal sorption by suspended S-layers. This was correlated to measurements of quartz crystal microbalance with dissipation monitoring (QCM-D), which allows the online detection of proteinaceous monolayer formation and metal deposition, and thus, a more detailed understanding on metal binding.
The ICP-MS results indicated that the binding of Au(III) to the suspended S-layer polymers is pH dependent. The maximum binding of Au(III) was obtained at pH 4.0. The QCM-D investigations enabled the detection of Au(III) sorption as well as the deposition of Au(0)-NPs in real-time during the in situ experiments. Further, this method allowed studying the influence of metal binding on the protein lattice stability of Slp1. Structural properties and protein layer stability could be visualized directly after QCM-D experiment using atomic force microscopy (AFM). In conclusion, the combination of these different methods provides a deeper understanding of metal binding by bacterial S-layer proteins in suspension or as monolayers on either bacterial cells or recrystallized surfaces.
Introduction
På grund af den stigende brug af guld til flere applikationer som elektronik, katalysatorer, biosensorer, eller medicinske instrumenter, er efterspørgslen af denne ædle metaller vokset i de seneste få år 6-9. Guld samt mange andre ædel- og tungmetaller frigives i miljøet via industrielt spildevand i fortyndede koncentrationer gennem minedrift, og bortskaffelse 7,8,10, selv om de fleste miljøforurening ved tunge eller ædelmetaller er en løbende proces primært forårsaget af teknologiske aktiviteter. Dette fører til en signifikant interferens af naturlige økosystemer og kan potentielt true menneskers sundhed 9. Kendskab til disse negative resultater fremmer søgningen efter nye teknikker til at fjerne metaller fra forurenede økosystemer og forbedringer i genbrug metaller fra industrispildevand. Veletablerede fysisk-kemiske metoder som udfældning eller ionbytning er ikke så effektive, især i højly fortyndet løsninger 7,8,11. Biosorption, enten med levende eller døde biomasse, er et attraktivt alternativ til spildevandsrensning 10,12. Anvendelsen af sådanne biologiske materialer kan reducere forbruget af giftige kemikalier. Mange mikroorganismer er blevet beskrevet at akkumulere eller immobilisere metaller. For eksempel, celler af Lysinibacillus sphaericus (L. sphaericus) JG-A12 har vist høje bindingskapaciteter for ædelmetaller, f.eks, Pd (II), Pt (II), Au (III), og andre giftige metaller som Pb (II) eller U (VI) 4,13, celler af Bacillus megaterium til Cr (VI) 14, celler af Saccharomyces cerevisiae til Pt (II) og Pd (II) 15 og Chlorella vulgære for Au (III) og U (VI) 16 , 17. Bindingen af metaller som tidligere Au (III), Pd (II), og Pt (II) er også blevet rapporteret for Desulfovibrio desulfuricans 18 og for L. sphaericus JG-B53 19,20. Ikke desto mindre, ikke all mikrober binder store mængder af metaller og deres anvendelse som sorptivt materiale er begrænset 12,21. Endvidere metalbindende Kapaciteten afhænger af forskellige parametre, f.eks cellesammensætning, den anvendte bio-komponent eller miljø- og eksperimentelle betingelser (pH, ionstyrke, temperatur etc.). Undersøgelsen af isolerede cellevægsfragmenter 22,23, som membranlipider, peptidoglycan, proteiner eller andre komponenter, hjælper til at forstå den metalbindende processer komplekse konstrueret helceller 8,21.
Cellekomponenterne fokuseret på i denne undersøgelse, er S-lag-proteiner. S-lag-proteiner er dele af den ydre cellekappen af mange bakterier og archaea, og de udgør ca. 15 – 20% af det totale protein masse af disse organismer. Som den første grænseflade til miljøet, disse celle forbindelser stor indflydelse de bakterielle sorptionsegenskaberne 3. S-lag-proteiner med molekylvægte i området fra fyrretil hundredvis af kDa produceres i cellen, men er samlet uden for hvor de er i stand til at danne lag på lipidmembraner eller polymere cellevægsbestanddele. Når isolerede, næsten alle S-lag-proteiner har den iboende egenskab til spontant samle i suspension, ved grænseflader, eller på overflader, der danner plane eller rørlignende strukturer 3. Tykkelsen af proteinet monolag afhænger af bakterier og er inden for en afstand af 5 – 25 nm 24. Generelt kan de dannede S-layer proteinstrukturer har en skrå (p1 eller p2), firkantet (p4) eller sekskantede (P3 eller P6) symmetrisk med gitterkonstanternes på 2,5 til 35 nm 3,24. Gitter formation synes at være i mange tilfælde er afhængige af divalente kationer og hovedsagelig på Ca2 + 25,26, Raff, J. et al. S-lags baserede nanokompositter til industrielle applikationer i protein-baserede Engineered nanostrukturer. (red Tijana Z. Grove & Aitziber L. Cortajarena) (Springer, 2016 (indsendt)). Ikke desto mindre, den fulde reaktionskaskaden af monomer foldning, monomer-monomer interaktion, dannelsen af et gitter, og den rolle, forskellige metaller, især af divalente kationer, såsom Ca2 + og Mg2 +, er endnu ikke fuldt forstået.
Den grampositive stamme L. sphaericus JG-B53 (omdøbt fra Bacillus sphaericus efter nye fylogenetiske klassifikation) 27 blev isoleret fra uranbrydning affald bunke "Haberland" (Johanngeorgenstadt, Sachsen, Tyskland) 4,28,29. Dets funktionelle S-lag protein (SLP1) har en kvadratisk gitter, en molekylvægt på 116 kDa 30, og en tykkelse på ≈ 10 nm på levende bakterieceller 31. I tidligere undersøgelser blev det in vitro dannelse af et lukket og stabilt protein lag med en tykkelse på ca. 10 nm opnås på mindre end 10 min 19. Den relaterede stammen L. sphaericus JG-A12, også et isolat fra "Haberland" bunke, har høj metalbindende kapacitet og dets isolerede S-lag protein har vist en høj kemisk og mekanisk stabilitet og god sorption for ædelmetaller som Au (III), Pt (II), og Pd (II) 4,32,33. Denne binding af ædelmetaller er mere eller mindre specifikke for nogle metaller og afhænger af tilgængeligheden af funktionelle grupper på den ydre og den indre overflade protein af polymeren og i dets porer, ionstyrke og pH-værdien. Relevante funktionelle grupper for interaktion metal ved proteinerne COOH-, NH 2 -, OH-, PO 4 -, SO 4 – og SO-. I princippet metalbindende kapacitet åbner et bredt spektrum af anvendelser, Raff, J. et al. S-lags baserede nanokompositter til industrielle applikationer i protein-baserede Engineered nanostrukturer. (red Tijana Z. Grove & Aitziber L. Cortajarena) (Springer, 2016 (indsendt)). fx som biosorptive komponenter til fjernelse eller nyttiggørelseaf opløste giftige eller værdifulde metaller, skabeloner til syntese eller defineret aflejring af regelmæssigt strukturerede metalliske nanopartikler (NPS) for katalyse, og andre bio-manipuleret materialer som bio-sensorisk lag 3,5,18,33. Regelmæssigt arrangeret NP arrays som Au (0) -NPs kunne bruges til større applikationer spænder fra molekylær elektronik og biosensorer, ultrahøje lagringstæthed enheder og katalysatorer for CO-oxidation 34-37. Udviklingen af sådanne applikationer og smart design af disse materialer kræver en dybere forståelse af de underliggende metal bindende mekanismer.
En forudsætning for udviklingen af sådanne biobaserede materialer er pålidelig gennemførelse af et grænsefladelag mellem biomolekylet og tekniske overflade 38,39. For eksempel, polyelektrolytter samlet med lag-på-lag (LbL) teknik 40,41 er blevet anvendt som et grænsefladelag for omkrystallisation af S-lags proteiner 39 </sup>. En sådan grænseflade tilbyder en relativt nem måde at udføre protein belægning på en reproducerbar og kvantitativ måde. Ved at udføre forskellige eksperimenter med og uden modifikation med selvklæbende initiativtagere, er det muligt at lave udsagn vedrørende belægning kinetik, lag stabilitet og samspillet mellem metaller med biomolekyler 19,42, Raff, J. et al. S-lags baserede nanokompositter til industrielle applikationer i protein-baserede Engineered nanostrukturer. (red Tijana Z. Grove & Aitziber L. Cortajarena) (Springer, 2016 (indsendt)). Imidlertid er kompleks mekanisme af proteinet adsorption og protein-overfladeinteraktion ikke helt forstået. Især oplysninger om kropsbygning, mønster orientering, og coating tætheder mangler stadig.
Kvartskrystalmikrovægt med spredning overvågning (QCM-D) teknik har tiltrukket sig opmærksomhed i de senere år som et redskab til at studere proteinadsorption, belægning kinetik, og interaktion proprocesser på nanometer skala 19,43-45. Denne teknik giver mulighed for detaljeret påvisning af masse adsorption i realtid, og kan anvendes som en indikator for proteinet selvsamlende proces og kobling af funktionelle molekyler på protein gitre 19,20,42,46-48. Desuden QCM-D målinger åbner mulighed for at studere interaktion metal processer med det proteinholdige lag under naturlige biologiske forhold. I en nylig undersøgelse, interaktionen af S-fase-protein med udvalgte metaller som Eu (III), Au (III), Pd (II), og Pt (II) er blevet undersøgt med QCM-D 19,20. Det adsorberede protein lag kan tjene som en forenklet model af en cellevæg grampositive bakterier. Undersøgelsen af denne enkelt komponent kan bidrage til en dybere forståelse af samspillet metal. Men alene QCM-D forsøg, der ikke tillader udsagn om overfladestrukturer og påvirkninger af metaller til protein. Andre teknikker er nødvendige for at indhente disse oplysninger. Én posligheden for billedbehandling bio-nanostrukturer og indhente oplysninger om strukturelle egenskaber er den atomare kraft mikroskopi (AFM).
Formålet med den præsenterede undersøgelse var at undersøge sorptionen af guld (Au (III) og Au (0) -NPs) til S-lag-proteiner, navnlig SLP1 L. sphaericus JG-B53. Eksperimenter blev udført med suspenderede proteiner på batch målestok i et pH-område på 2,0 – 5.0 ved hjælp af ICP-MS og med immobiliserede S-lag ved hjælp af QCM-D. Desuden blev indflydelsen af metalsalt løsning på gitteret stabilitet undersøgt med efterfølgende AFM undersøgelser. Kombinationen af disse teknikker bidrager til en bedre forståelse af in vitro-interaktion metal processer som et redskab til at lære mere om bindende begivenheder på hele bakterieceller vedrørende specifikke metal tilhørsforhold. Denne viden er ikke kun afgørende for udviklingen af gældende filtermaterialer til udvinding af metaller til miljøbeskyttelse og bevarelse af rekilder 49, men også for udviklingen af arrays af stærkt bestilt metalliske NP'er til forskellige tekniske applikationer.
Protocol
Representative Results
Discussion
I dette arbejde studeret binding af Au til S-lag-proteiner blev undersøgt under anvendelse af en kombination af forskellige analysemetoder. Især bindingen af Au er meget attraktiv, ikke kun anvendes til genindvinding af Au fra minedrift farvande eller procesløsninger, men også til konstruktion af materialer, f.eks sensoriske overflader. For undersøgelser af Au interaktion (Au (III) og Au (0) -NPs) med suspenderet og omkrystalliseres monolag af SLP1, havde protein, der skal isoleres. Derfor har denne unders…
Divulgations
The authors have nothing to disclose.
Acknowledgements
Den nuværende arbejde blev delvist finansieret af IGF-projektet "S-Sieve" (490 ZBG / 1) finansieret af BMWi og BMBF-projektet "Aptasens" (BMBF / DLR 01RB0805A). Særlig tak til Tobias J. Günther for hans værdifulde hjælp under AFM undersøgelser og til Erik V. Johnstone til aflæsning af manuskriptet som en indfødt engelsktalende. Desuden vil forfatteren af dette papir takke Aline Ritter og Sabrina Gurlit (fra Institute for Resource Økologi om bistand i ICP-MS-målinger), Manja Vogel, Nancy Unger, Karen E. Viacava og gruppen bioteknologi af Helmholtz-Instituttet Freiberg for Resource Technology.
Materials
| equiment and software | |||
| Bioreactor, Steam In Place 70L Pilot System | Applikon Biotechnology, Netherlands | Z6X | Including dO2, pH sensors of Applikon Biotechnology and BioXpert software V2 |
| Noninvasive Biomass Monitor BugEye 2100 | BugLab, Concord (CA), USA | Z9X | — |
| Spectrometer Ultrospec 1000 | Amersham Pharmacia Biotech, Great Britain | 80-2109-10 | Company now GE Healthcare Life Sciences |
| MiniStar micro centrifuge | VWR, Germany | 521-2844 | For centrifugation of cultivation samples |
| Research system microscope BX-61 | Olympus Germany LLC, Germany | 037006 | Microscope in combination with imaging software |
| Cell^P (version 3.1) | Olympus Soft Imaging Solutions LLC, Münster, Germany | — | together with microscope |
| Powerfuge Pilot Separation System Serie 9010-S | Carr Centritech, Florida, USA | 9010PLT | For biomasse harvesting |
| T18 basic Ultra Turrax | IKA Labortechnik, Germany | 431-2601 | For flagella removal and sample homogenization |
| Sorvall Evolution RC Superspeed Centrifuge | Thermo Fisher Scientific, USA | 728411 | Used within protein isolation |
| Mobile high shear fluid processor, M-110EH-30 Pilot | Microfluidics, Massachusetts, USA | M110EH30K | Used for cell rupture |
| Alpha 1-4 LSC Freeze dryer | Martin Christ Freeze dryers LLC, Osterode, Germany | 102041 | — |
| UV-VIS spectrophotometry (NanoDrop 2000c) | Thermo Fisher Scientific, USA | 91-ND-2000C-L | For determination of protein concentration |
| Mini-PROTEAN vertical electrophoresis chamber | Bio-Rad Laboratories GmbH, Munich, Germany | 165-3322 | For SDS-PAGE |
| VersaDoc Imaging System 3000 | Bio-Rad Laboratories GmbH, Munich, Germany | 1708030 | Used for imaging of SDS-PAGE gels |
| ICP-MS Elan 9000 | PerkinElmer, Waltham (MA), USA | N8120536 | For determination of metal concentration |
| Zetasizer Nano ZS | Malvern Instruments, Worcestershire United Kingdom | ZEN3600 | For determination of nanoparticle size |
| Q-Sense E4 device | Q-Sense AB, Gothenburg, Sweden | QS-E4 | ordered via LOT quantum design (software included with E4 platform) |
| Q-Soft 401 (data recording) | Q-Sense AB, Gothenburg, Sweden | ||
| Q-Tools 3 (data evaluation and modelling) | Q-Sense AB, Gothenburg, Sweden | ||
| QCM-D flow modules QFM 401 | Q-Sense AB, Gothenburg, Sweden | QS-QFM401 | ordered via LOT quantum design |
| QSX 303 SiO2 piezoelectric AT-cut quartz sensors | Q-Sense AB, Gothenburg, Sweden | QS-QSX303 | ordered via LOT quantum design |
| Ozone cleaning chamber | Bioforce Nanoscience, Ames (IA), USA | QS-ESA006 | ordered via LOT quantum design |
| Atomic Force Microscope MFP-3D Bio AFM | Asylum Research, Santa Barbara (CA), USA | MFP-3DBio | AFM measurements and imaging software |
| Asylum Research AFM Software AR Version 120804+1223 | Asylum Research, Santa Barbara (CA), USA | — | imaging software included in Cat. No. MFP-3DBio |
| Igor Version Pro 6.3.2.3 Software | WaveMetrics, Inc., USA | — | imaging software included in Cat. No. MFP-3DBio |
| BioHeater | Asylum Research, Santa Barbara (CA), USA | Bioheater | Sample heater for AFM measurements |
| Biolever mini cantilever, BL-AC40TS-C2 | Olympus Germany LLC, Germany | BL-AC40TS-C2 | Prefered cantilever for AFM measurements |
| WSxM 5.0 Develop 6.5 (2013) | Nanotec Electronica S.L. , Spain | freeware | Software for AFM analysis |
| Name | Company | Catalog Number | Comments |
| Detergents and other equiment | |||
| Calcium chloride Dihydrate (CaCl2 ∙ 2H2O) | Merck KGaA | 1.02382 | — |
| acidic acid, 100 %, p.A. | CARL ROTH GmbH+CO.KG | 3738.5 | Danger, flammable and corrosive liquid and vapour. Causes severe skin burns and eye damage. |
| Antifoam 204 | Sigma-Aldrich Co. LLC. | A6426 | For foam suppression |
| bromophenol blue, sodium salt | Sigma-Aldrich Co. LLC. | B5525 | — |
| Coomassie Brilliant Blue R (C45H44N3NaO7S2) | CARL ROTH GmbH+CO.KG | 3862.1 | — |
| Deoxyribonuclease II from porcine spleen | Sigma-Aldrich Co. LLC. | D4138 | Typ IV , 2,000-6,000 Kunitz units/mg protein |
| Ethanol, 95% | VWR, Germany | 20827.467 | Danger, flammable |
| glycerine, p.A. | CARL ROTH GmbH+CO.KG | 3783.1 | — |
| Gold(III) chloride trihydrate (HAuCl4 ∙ 3H2O) | Sigma-Aldrich Co. LLC. | 520918 | Danger |
| Guanidine hydrochloride (GuHCl) | CARL ROTH GmbH+CO.KG | 0037.1 | — |
| Hellmanex III | Hellma GmbH & Co. KG | 9-307-011-4-507 | — |
| Hydrochloric acid (HCl) (37%) | CARL ROTH GmbH+CO.KG | 4625.2 | Danger; Corrosive, used for pH adjustment |
| Lysozyme from chicken egg white | Sigma-Aldrich Co. LLC. | L6876 | Lyophilized powder, protein =90 %, =40,000 units/mg protein (Sigma) |
| Magnesium chloride Hexahydrate (MgCl2 ∙ 6H2O) | Merck KGaA | 1.05833 | — |
| Magnetic stirrer with heating, MR 3000K | Heidolph Instruments GmbH & Co.KG, Germany | 504.10100.00 | Standard stirrer within experiment |
| NB-Media DM180 | Mast Diagnostica GmbH | 121800 | — |
| Nitric acid (HNO3) | CARL ROTH GmbH+CO.KG | HN50.1 | Danger; Oxidizing, Corrosing |
| PageRuler Unstained Protein Ladder | ThermoScientific-Pierce | 26614 | — |
| Poly(sodium 4-styrenesulfonat) (PSS) | Sigma-Aldrich Co. LLC. | 243051 | Average Mw ~70,000 |
| Polyethylenimine (PEI), branched | Sigma-Aldrich Co. LLC. | 408727 | Warning; Harmful, Irritant, Dangerous for the environment; average Mw ~25,000 |
| Potassium carbonate anhydrous (K2CO3) | Sigma-Aldrich Co. LLC. | 60108 | Warning; Harmful |
| Ribonuclease A from bovine pancreas | Sigma-Aldrich Co. LLC. | R5503 | Type I-AS, 50-100 Kunitz units/mg protein |
| Sodium azide (NaN3) | Merck KGaA | 106688 | Danger; very toxic and Dangerous for the environment |
| Sodium chloride (NaCl) | CARL ROTH GmbH+CO.KG | 3957.2 | — |
| Sodium dodecyl sulfate (SDS) | Sigma-Aldrich Co. LLC. | L-5750 | Danger; toxic |
| Sodium hydroxide (NaOH) | CARL ROTH GmbH+CO.KG | 6771.1 | Danger; Corrosive, used for pH regulation within cultivation and pH adjustment |
| Spectra/Por 6, Dialysis membrane, MWCO 50,000 | CARL ROTH GmbH+CO.KG | 1893.1 | — |
| Sulfuric acid (H2SO4) | CARL ROTH GmbH+CO.KG | HN52.2 | Danger; Corrosive, used for pH regulation within cultivation |
| Tannic acid (C76H52O46) | Sigma-Aldrich Co. LLC. | 16201 | — |
| TRIS HCl (C4H11NO3HCl) | CARL ROTH GmbH+CO.KG | 9090.2 | — |
| Tri-sodium citrate dihydrate (C6H5Na3O7 ∙ 2H2O) | CARL ROTH GmbH+CO.KG | 3580.2 | — |
| Triton X-100 | CARL ROTH GmbH+CO.KG | 3051.3 | Warning; Harmful, Dangerous for the environment |
| VIVASPIN 500, 50.000 MWCO Ultrafiltration tubes | Sartorius AG | VS0132 | — |
| β-mercaptoethanol | Sigma-Aldrich Co. LLC. | M6250 | Danger, toxic |
References
- Merroun, M. L., Rossberg, A., Hennig, C., Scheinost, A. C., Selenska-Pobell, S. Spectroscopic characterization of gold nanoparticles formed by cells and S-layer protein of Bacillus sphaericus JG-A12. Mater. Sci. Eng. C. 27 (1), 188-192 (2007).
- Raff, J., Soltmann, U., Matys, S., Selenska-Pobell, S., Bottcher, H., Pompe, W. Biosorption of uranium and copper by biocers. Chem. Mat. 15 (1), 240-244 (2003).
- Sleytr, U. B., Schuster, B., Egelseer, E. M., Pum, D. S-Layers: Principles and Applications. FEMS Microbiol. Rev. , (2014).
- Pollmann, K., Raff, J., Merroun, M., Fahmy, K., Selenska-Pobell, S. Metal binding by bacteria from uranium mining waste piles and its technological applications. Biotechnol. Adv. 24 (1), 58-68 (2006).
- Raff, J., Selenska-Pobell, S. Toxic avengers. Nucl. Eng. Int. 51, 34-36 (2006).
- Tsuruta, T. Biosorption and recycling of gold using various microorganisms. J. Gen. Appl. Microbiol. 50 (4), 221-228 (2004).
- Sathishkumar, M., Mahadevan, A., Vijayaraghavan, K., Pavagadhi, S., Balasubramanian, R. Green Recovery of Gold through Biosorption, Biocrystallization, and Crystallization. Ind. Eng. Chem. Res. 49 (16), 7129-7135 (2010).
- Das, N. Recovery of precious metals through biosorption – A review. Hydrometallurgy. 103 (1-4), 180-189 (2010).
- Volesky, B. Biosorption and me. Water Res. 41 (18), 4017-4029 (2007).
- Vilar, V. J. P., Botelho, C. M. S., Boaventura, R. A. R., Atimtay, T. A., Sikdar, S. K. Environmental Friendly Technologies for Wastewater Treatment: Biosorption of Heavy Metals Using Low Cost Materials and Solar Photocatalysis. Security of Industrial Water Supply and Management.NATO Science for Peace and Security Series C-Environmental Security. , 159-173 (2010).
- Lovley, D. R., Lloyd, J. R. Microbes with a mettle for bioremediation. Nat. Biotechnol. 18 (6), 600-601 (2000).
- Schiewer, S., Volesky, B., Lovely, D. R. . Environmental Microbe-Metal Interactions. , 329-362 (2000).
- Raff, J., Berger, S., Selenska-Pobell, S. Uranium binding by S-layer carrying isolates of the genus Bacillus. Annual Report 2006 Institute of Radiochemistry. , (2006).
- Srinath, T., Verma, T., Ramteke, P. W., Garg, S. K. Chromium (VI) biosorption and bioaccumulation by chromate resistant bacteria. Chemosphere. 48 (4), 427-435 (2002).
- Godlewska-Zylkiewicz, B. Biosorption of platinum and palladium for their separation/preconcentration prior to graphite furnace atomic absorption spectrometric determination. Spectroc. Acta Pt. B-Atom. Spectr. 58 (8), 1531-1540 (2003).
- Hosea, M., et al. Accumulation of elemental gold on the alga Chlorella-vulgaris. Inorg. Chim. A-Bioinor. 123 (3), 161-165 (1986).
- Vogel, M., et al. Biosorption of U(VI) by the green algae Chlorella vulgaris. in dependence of pH value and cell activity. Sci. Total Environ. 409 (2), 384-395 (2010).
- Creamer, N., Baxter-Plant, V., Henderson, J., Potter, M., Macaskie, L. Palladium and gold removal and recovery from precious metal solutions and electronic scrap leachates by Desulfovibrio desulfuricans. Biotechnol Lett. 28 (18), 1475-1484 (2006).
- Suhr, M., et al. Investigation of metal sorption behavior of Slp1 from Lysinibacillus sphaericus. JG-B53 – A combined study using QCM-D, ICP-MS and AFM. Biometals. 27 (6), 1337-1349 (2014).
- Suhr, M. . Isolierung und Charakterisierung von Zellwandkomponenten der gram-positiven Bakterienstämme Lysinibacillus sphaericus JG-A12 und JG-B53 und deren Wechselwirkungen mit ausgewählten relevanten Metallen und Metalloiden. , (2015).
- Spain, A., Alm, E. Implications of Microbial Heavy Metal Tolerance in the Environment. Reviews in Undergraduate Research. 2, 1-6 (2003).
- Ledin, M. Accumulation of metals by microorganisms – processes and importance for soil systems. Earth-Sci. Rev. 51 (1-4), 1-31 (2000).
- Maruyama, T., et al. Proteins and Protein-Rich Biomass as Environmentally Friendly Adsorbents Selective for Precious Metal Ions. Environ. Sci. Technol. 41 (4), 1359-1364 (2007).
- Sara, M., Sleytr, U. B. S-layer proteins. J. Bacteriol. 182 (4), 859-868 (2000).
- Baranova, E., et al. SbsB structure and lattice reconstruction unveil Ca2+ triggered S-layer assembly. Nature. 487 (7405), 119-122 (2012).
- Teixeira, L. M., et al. Entropically Driven Self-Assembly of Lysinibacillus sphaericus S-Layer Proteins Analyzed Under Various Environmental Conditions. Macromol. Biosci. 10 (2), 147-155 (2010).
- Ahmed, I., Yokota, A., Yamazoe, A., Fujiwara, T. Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Int. J. Syst. Evol. Microbiol. 57 (5), 1117-1125 (2007).
- Panak, P., et al. Bacteria from uranium mining waste pile: interactions with U(VI). J. Alloy. Compd. 271, 262-266 (1998).
- Selenska-Pobell, S., Kampf, G., Flemming, K., Radeva, G., Satchanska, G. Bacterial diversity in soil samples from two uranium waste piles as determined by rep-APD, RISA and 16S rDNA retrieval. Antonie Van Leeuwenhoek. 79 (2), 149-161 (2001).
- Lederer, F. L., et al. Identification of multiple putative S-layer genes partly expressed by Lysinibacillus sphaericus JG-B53. Microbiology. 159 ( Pt 6), 1097-1108 (2013).
- Günther, T. J., Suhr, M., Raff, J., Pollmann, K. Immobilization of microorganisms for AFM studies in liquids. RSC Advances. 4, 51156-51164 (2014).
- Fahmy, K., et al. Secondary Structure and Pd(II) Coordination in S-Layer Proteins from Bacillus sphaericus. Studied by Infrared and X-Ray Absorption Spectroscopy. Biophys. J. 91 (3), 996-1007 (2006).
- Pollmann, K., Merroun, M., Raff, J., Hennig, C., Selenska-Pobell, S. Manufacturing and characterization of Pd nanoparticles formed on immobilized bacterial cells. Lett. Appl. Microbiol. 43 (1), 39-45 (2006).
- Corti, C., Holliday, R. . Gold : science and applications. , (2010).
- Daniel, M. C., Astruc, D. Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. Chem. Rev. 104 (1), 293-346 (2004).
- Tang, J., et al. Fabrication of Highly Ordered Gold Nanoparticle Arrays Templated by Crystalline Lattices of Bacterial S-Layer Protein. Chem. Phys. Chem. 9 (16), 2317-2320 (2008).
- Haruta, M. Size- and support-dependency in the catalysis of gold. Catal. Today. 36 (1), 153-166 (1997).
- Habibi, N., et al. Nanoengineered polymeric S-layers based capsules with targeting activity. Colloids and surfaces. B, Biointerfaces. 88 (1), 366-372 (2011).
- Toca-Herrera, J. L., et al. Recrystallization of Bacterial S-Layers on Flat Polyelectrolyte Surfaces and Hollow Polyelectrolyte Capsules. Small. 1 (3), 339-348 (2005).
- Decher, G., Lehr, B., Lowack, K., Lvov, Y., Schmitt, J. New nanocomposite films for biosensors – Layer-by-Layer adsorbed films of polyelectrolytes, proteins or DNA. Biosens. Bioelectron. 9 (9-10), 677-684 (1994).
- Decher, G., Schmitt, J. Fine-tuning of the film thickness of ultrathin multilayer films composed of consecutively alternating layers of anionic and cationic polyelectrolytes. Progress in Colloid & Polymer Science. 89 Trends in Colloid and Interface Science VI, (1992).
- Günther, T. J. . S-Layer als Technologieplattform – Selbstorganisierende Proteine zur Herstellung funktionaler Beschichtungen. , (2015).
- Delcea, M., et al. Thermal stability, mechanical properties and water content of bacterial protein layers recrystallized on polyelectrolyte multilayers. Soft Matter. 4 (7), 1414-1421 (2008).
- Roach, P., Farrar, D., Perry, C. C. Interpretation of Protein Adsorption: Surface-Induced Conformational Changes. J. Am. Chem. Soc. 127 (22), 8168-8173 (2005).
- Zeng, R., Zhang, Y., Tu, M., Zhou, C. R., et al. Protein Adsorption Behaviors on PLLA Surface Studied by Quartz Crystal Microbalance with Dissipation Monitoring (QCM-D). Materials Science Forum. 610-613, 1219-1223 (2009).
- Bonroy, K., et al. Realization and Characterization of Porous Gold for Increased Protein Coverage on Acoustic Sensors. Anal. Chem. 76 (15), 4299-4306 (2004).
- Pum, D., Toca-Herrera, J. L., Sleytr, U. B. S-layer protein self-assembly. Int. J. Mol. Sci. 14 (2), 2484-2501 (2013).
- Weinert, U., et al. S-layer proteins as an immobilization matrix for aptamers on different sensor surfaces. Eng. Life Sci. , (2015).
- Umeda, H., et al. Recovery and Concentration of Precious Metals from Strong Acidic Wastewater. Mater. Trans. 52 (7), 1462-1470 (2011).
- Engelhardt, H., Saxton, W. O., Baumeister, W. 3-Dimensional structure of the tetragonal surface-layer of Sporosarcina-urea. J. Bacteriol. 168 (1), 309-317 (1986).
- Sprott, G. D., Koval, S. F., Schnaitman, C. A. . Methods for general and molecular bacteriology. , 72-103 (1994).
- Laemmli, U. K. Cleavage of Structural Proteins during Assembly of Head Bacteriophage T4. Nature. 227 (5259), 680-685 (1970).
- Stoscheck, C., Deutscher, M. P. [6] Quantitation of protein. Methods in Enzymology. 182, 50-68 (1990).
- Sleytr, U. B., Messner, P., Pum, D. Analysis of Crystalline Bacterial Surface-Layers by Freeze-Etching Metal Shadowing, Negative Staining and Ultra-Thin Sectioning. Method Microbiol. 20, 29-60 (1988).
- PerkinElmer. . ICP Mass Spectrometry – The 30-Min to ICP-MS. , (2001).
- Mühlpfordt, H. The preparation of colloidal Gold Nanoparticles using tannic-acid as an additional reducing agent. Experientia. 38 (9), 1127-1128 (1982).
- Hayat, M. A. . Colloidal Gold – Principles, Methods and Applications. , (1989).
- Amendola, V., Meneghetti, M. Size Evaluation of Gold Nanoparticles by UV−vis Spectroscopy. The Journal of Physical Chemistry C. 113 (11), 4277-4285 (2009).
- Schurtenberger, P., Newman, M. E., Buffle, J., van Leeuwen, H. P. . Characterization of biological and environmental particles using static and dynamic light scattering in Environmental Particles. 2, 37-115 (1993).
- Jain, R., et al. Extracellular Polymeric Substances Govern the Surface Charge of Biogenic Elemental Selenium Nanoparticles. Environmental Science & Technology. 49 (3), 1713-1720 (2015).
- Harewood, K., Wolff, J. S. Rapid electrophoretic procedure for detection of SDS-released oncorna-viral RNA using polyacrylamide-agarose gels. Anal. Biochem. 55 (2), 573-581 (1973).
- Penfold, J., Staples, E., Tucker, I., Thomas, R. K. Adsorption of mixed anionic and nonionic surfactants at the hydrophilic silicon surface. Langmuir. 18 (15), 5755-5760 (2002).
- Krozer, A., Rodahl, M. X-ray photoemission spectroscopy study of UV/ozone oxidation of Au under ultrahigh vacuum conditions. J. Vac. Sci. Technol. A-Vac. Surf. Films. 15 (3), 1704-1709 (1997).
- Vig, J. R. UV ozone cleaning of surfaces. J. Vac. Sci. Technol. 3 (3), 1027-1034 (1985).
- Sauerbrey, G. Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur Mikrowägung. Zeitschrift Fur Physik. 155 (2), 206-222 (1959).
- Q-Sense – Biolin Scientific. . Introduction and QCM-D Theory – Q-Sense Basic Training. , (2006).
- Edvardsson, M., Rodahl, M., Kasemo, B., Höök, F. A dual-frequency QCM-D setup operating at elevated oscillation amplitudes. Anal. Chem. 77 (15), 4918-4926 (2005).
- Hovgaard, M. B., Dong, M. D., Otzen, D. E., Besenbacher, F. Quartz crystal microbalance studies of multilayer glucagon fibrillation at the solid-liquid interface. Biophys. J. 93 (6), 2162-2169 (2007).
- Liu, S. X., Kim, J. T. Application of Kelvin-Voigt Model in Quantifying Whey Protein Adsorption on Polyethersulfone Using QCM-D. Jala. 14 (4), 213-220 (2009).
- Reviakine, I., Rossetti, F. F., Morozov, A. N., Textor, M. Investigating the properties of supported vesicular layers on titanium dioxide by quartz crystal microbalance with dissipation measurements. J. Chem. Phys. 122 (20), (2005).
- Voinova, M. V., Rodahl, M., Jonson, M., Kasemo, B. Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces: Continuum mechanics approach. Phys. Scr. 59 (5), 391-396 (1999).
- Fischer, H., Polikarpov, I., Craievich, A. F. Average protein density is a molecular-weight-dependent function. Protein Sci. 13 (10), 2825-2828 (2004).
- Schuster, B., Pum, D., Sleytr, U. B. S-layer stabilized lipid membranes (Review). Biointerphases. 3 (2), FA3-FA11 (2008).
- Malmström, J., Agheli, H., Kingshott, P., Sutherland, D. S. Viscoelastic Modeling of Highly Hydrated Laminin Layers at Homogeneous and Nanostructured Surfaces: Quantification of Protein Layer Properties Using QCM-D and SPR. Langmuir. 23 (19), 9760-9768 (2007).
- Vörös, J. The Density and Refractive Index of Adsorbing Protein Layers. Biophys. J. 87 (1), 553-561 (2004).
- Hillier, A. C., Bard, A. J. ac-mode atomic force microscope imaging in air and solutions with a thermally driven bimetallic cantilever probe. Rev. Sci. Instrum. 68 (5), 2082-2090 (1997).
- Horcas, I., et al. WSXM: A software for scanning probe microscopy and a tool for nanotechnology. Rev. Sci. Instrum. 78 (1), 013705 (2007).
- Merroun, M. L., Rossberg, A., Scheinost, A. C., Selenska-Pobell, S. XAS characterization of gold nanoclusters formed by cells and S-layer sheets of B. sphaericus JG-A12. Annual Report Forschungszentrum Rossendorf – Institute for Radiochemistry. , (2005).
- Jankowski, U., Merroun, M. L., Selenska-Pobell, S., Fahmy, K. S-Layer protein from Lysinibacillus sphaericus. JG-A12 as matrix for Au III sorption and Au-nanoparticle formation. Spectroscopy. 24 (1), 177-181 (2010).
- Selenska-Pobell, S., et al. Magnetic Au nanoparticles on archaeal S-Layer ghosts as templates. Nanomater. nanotechnol. 1 (2), 8-16 (2011).
- Caruso, F., Furlong, D. N., Kingshott, P. Characterization of ferritin adsorption onto gold. J. Colloid Interface Sci. 186 (1), 129-140 (1997).
- Ward, M. D., Buttry, D. A. In situ interfacial mass detection with piezoelectric transducers. Science. 249 (4972), 1000-1007 (1990).
- Höök, F., et al. Variations in coupled water, viscoelastic properties, and film thickness of a Mefp-1 protein film during adsorption and cross-linking: A quartz crystal microbalance with dissipation monitoring, ellipsometry, and surface plasmon resonance study. Anal. Chem. 73 (24), 5796-5804 (2001).
- Wahl, R. . Reguläre bakterielle Zellhüllenproteine als biomolekulares Templat. , (2003).
- Jennings, T., Strouse, G. . Past, present, and future of gold nanoparticles in Bio-Applications of Nanoparticles. , 34-47 (2007).
- Beveridge, T., Fyfe, W. Metal fixation by bacterial cell walls. Can. J. Earth Sci. 22 (12), 1893-1898 (1985).
