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Review Article

Luminescence materials for pH and oxygen sensing in microbial cells – structures, optical properties, and biological applications

, , , &
Pages 723-738 | Received 02 Dec 2015, Accepted 08 May 2016, Published online: 15 Sep 2016

References

  • Quigley H, Colloby SJ, O'brien JT. PET imaging of brain amyloid in dementia: a review. Int J Geriatr Psychiatry. 2011;26:991–999.
  • Wei L, Hu F, Shen Y, et al. Live-cell imaging of alkyne-tagged small biomolecules by stimulated Raman scattering. Nat Methods. 2014;11:410–412.
  • Pimlott SL, Sutherland A. Molecular tracers for the PET and SPECT imaging of disease. Chem Soc Rev. 2011;40:149–162.
  • Knight JC, Edwards PG, Paisey SJ. Fluorinated contrast agents for magnetic resonance imaging; a review of recent developments. Rsc Adv. 2011;1:1415–1425.
  • Shenton ME, Hamoda HM, Schneiderman JS, et al. A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav. 2012;6:137–192.
  • Ortiz SHC, Chiu T, Fox MD. Ultrasound image enhancement: a review. Biomed Signal Proces. 2012;7:419–428.
  • Ebejer N, Guell AG, Lai SCS, et al. Scanning electrochemical cell microscopy: a versatile technique for nanoscale electrochemistry and functional imaging. Annu Rev Anal Chem (Palo Alto, CA). 2013;6:329–351.
  • Takahashi Y, Shevchuk AI, Novak P, et al. Topographical and electrochemical nanoscale imaging of living cells using voltage-switching mode scanning electrochemical microscopy. Proc Natl Acad Sci USA. 2012;109:11540–11545.
  • Ozawa T, Yoshimura H, Kim SB. Advances in fluorescence and bioluminescence imaging. Anal Chem. 2013;85:590–609.
  • Pepperkok R, Ellenberg J. Innovation – High-throughput fluorescence microscopy for systems biology. Nat Rev Mol Cell Biol. 2006;7:690–696.
  • Xia T, Li N, Fang XH. Single-molecule fluorescence imaging in living cells. Annu Rev Phys Chem. 2013;64:459–480.
  • Fu D, Lu FK, Zhang X, et al. Quantitative chemical imaging with multiplex stimulated Raman scattering microscopy. J Am Chem Soc. 2012;134:3623–3626.
  • Klein K, Gigler AM, Aschenbrenner T, et al. Label-free live-cell imaging with confocal Raman microscopy. Biophys J. 2012;102:360–368.
  • Palonpon AF, Sodeoka M, Fujita K. Molecular imaging of live cells by Raman microscopy. Curr Opin Chem Biol. 2013;17:708–715.
  • Han JY, Burgess K. Fluorescent indicators for intracellular pH. Chem Rev. 2010;110:2709–2728.
  • Korostynska O, Arshak K, Gill E, et al. Review on state-of-the-art in polymer based pH sensors. Sensors. 2007;7:3027–3042.
  • Lin J. Recent development and applications of optical and fiber-optic pH sensors. Trac-Trend Anal Chem. 2000;19:541–552.
  • Mcdonagh C, Burke CS, Maccraith BD. Optical chemical sensors. Chem Rev. 2008;108:400–422.
  • Richter A, Paschew G, Klatt S, et al. Review on hydrogel-based pH sensors and microsensors. Sensors. 2008;8:561–581.
  • Wencel D, Abel T, Mcdonagh C. Optical chemical pH sensors. Anal Chem. 2014;86:15–29.
  • Wang XD, Wolfbeis OS. Fiber-optic chemical sensors and biosensors (2008–2012). Anal Chem. 2013b;85:487–508.
  • Wolfbeis OS. Fiber optic chemical sensors and biosensors. Anal Chem. 2000;72:81R–89r.
  • Wolfbeis OS. Fiber-optic chemical sensors and biosensors. Anal Chem. 2002;74:2663–2677.
  • Wolfbeis OS. Fiber-optic chemical sensors and biosensors. Anal Chem. 2004;76:3269–3283.
  • Wolfbeis OS. Fiber-optic chemical sensors and biosensors. Anal Chem. 2006;78:3859–3873.
  • Wolfbels OS. Fiber-optic chemical sensors and biosensors. Anal Chem. 2008;80:4269–4283.
  • Wolfbeis OS. Materials for fluorescence-based optical chemical sensors. J Mater Chem. 2005;15:2657–2669.
  • Wang XD, Wolfbeis OS. Optical methods for sensing and imaging oxygen: materials, spectroscopies and applications. Chem Soc Rev. 2014b;43:3666–3761.
  • Steiner MS, Duerkop A, Wolfbeis OS. Optical methods for sensing glucose. Chem Soc Rev. 2011;40:4805–4839.
  • Pickup JC, Hussain F, Evans ND, et al. Fluorescence-based glucose sensors. Biosens Bioelectron. 2005;20:2555–2565.
  • Wu ZY, Fang H, Xu WF. Progress in boronic acid-based fluorescent glucose sensors. Chin J Org Chem. 2007;27:830–836.
  • Fang H, Kaur G, Wang BH. Progress in boronic acid-based fluorescent glucose sensors. J Fluoresc. 2004;14:481–489.
  • Carter KP, Young AM, Palmer AE. Fluorescent sensors for measuring metal ions in living systems. Chem Rev. 2014;114:4564–4601.
  • Domaille DW, Que EL, Chang CJ. Synthetic fluorescent sensors for studying the cell biology of metals. Nat Chem Biol. 2008;4:168–175.
  • Lidstrom ME, Konopka MC. The role of physiological heterogeneity in microbial population behavior. Nat Chem Biol. 2010;6:705–712.
  • Kim J, Hegde M, Kim SH, et al. A microfluidic device for high throughput bacterial biofilm studies. Lab Chip. 2012;12:1157–1163.
  • Wu FB, Dekker C. Nanofabricated structures and microfluidic devices for bacteria: from techniques to biology. Chem Soc Rev. 2016;45:268–280.
  • Ungerbock B, Charwat V, Ertl P, et al. Microfluidic oxygen imaging using integrated optical sensor layers and a color camera. Lab Chip. 2013;13:1593–1601.
  • Padan E, Bibi E, Ito M, et al. Alkaline pH homeostasis in bacteria: new insights. Biochim Biophys Acta. 2005;1717:67–88.
  • Krulwich TA, Sachs G, Padan E. Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol. 2011;9:330–343.
  • Miller WM, Blanch HW, Wilke CR. A kinetic-analysis of hybridoma growth and metabolism in batch and continuous suspension-culture – effect of nutrient concentration, dilution rate, and pH. Biotechnol Bioeng. 1988;32:947–965.
  • Ozturk SS, Palsson BO. Effects of dissolved-oxygen on hybridoma cell-growth, metabolism, and antibody-production kinetics in continuous culture. Biotechnol Prog. 1990;6:437–446.
  • Schmid G, Blanch HW, Wilke CR. Hybridoma growth, metabolism, and product formation in hepes-buffered medium. 2. Effect of pH. Biotechnol Lett. 1990;12:633–638.
  • Booth IR. Regulation of cytoplasmic Ph in bacteria. Microbiol Rev. 1985;49:359–378.
  • Booth IR, Kroll RG. Regulation of cytoplasmic Ph (pH1) in bacteria and its relationship to metabolism. Biochem Soc Trans. 1983;11:70–72.
  • Billinton N, Knight AW. Seeing the wood through the trees: a review of techniques for distinguishing green fluorescent protein from endogenous autofluorescence. Anal Biochem. 2001;291:175–197.
  • Padan E, Zilberstein D, Schuldiner S. pH homeostasis in bacteria. Biochim Biophys Acta. 1981;650:151–166.
  • Hakansson A, Bentley CC, Shakhnovic EA, et al. Cytolysin-dependent evasion of lysosomal killing. Proc Natl Acad Sci USA. 2005;102:5192–5197.
  • Pethe K, Swenson DL, Alonso S, et al. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc Natl Acad Sci USA. 2004;101:13642–13647.
  • Fernandes R, Tsao CY, Hashimoto Y, et al. Magnetic nanofactories: localized synthesis and delivery of quorum-sensing signaling molecule autoinducer-2 to bacterial cell surfaces. Metab Eng. 2007;9:228–239.
  • Heo J, Thomas KJ, Seong GH, et al. A microfluidic bioreactor based on hydrogel-entrapped E. coli: cell viability, lysis, and intracellular enzyme reactions. Anal Chem. 2003;75:22–26.
  • Johnson I, Spence MTZ. (2010). A guide to fluorescent probes and labeling technologies: The Molecular Probes® handbook. 11th ed. Waltham, MA: Thermo Fisher Scientific Inc.
  • Breeuwer P, Drocourt JL, Bunschoten N, et al. Characterization of uptake and hydrolysis of fluorescein diacetate and carboxyfluorescein diacetate by intracellular esterases in Saccharomyces cerevisiae, which result in accumulation of fluorescent product. Appl Environ Microb. 1995;61:1614–1619.
  • Breeuwer P, Drocourt JL, Rombouts FM, et al. A novel method for continuous determination of the intracellular pH in bacteria with the internally conjugated fluorescent probe 5 (and 6-)-carboxyfluorescein succinimidyl ester. Appl Environ Microb. 1996;62:178–183.
  • Wan SL, Zheng Y, Shen J, et al. “NS and its bioimaging applications” switchable sensor: a fluorescent spiropyran responds to extreme pH conditions and its bioimaging. Acs Appl Mater Interfaces. 2014;6:19515–19519.
  • Xu Y, Jiang Z, Xiao Y, et al. A new fluorescent pH probe for extremely acidic conditions. Anal Chim Acta. 2014;820:146–151.
  • Breeuwer P, Drocourt JL, Rombouts FM, et al. Energy-dependent, carrier-mediated extrusion of carboxyfluorescein from Saccharomyces cerevisiae allows rapid assessment of cell viability by flow-cytometry. Appl Environ Microb. 1994;60:1467–1472.
  • Hunter RC, Beveridge TJ. Application of a pH-sensitive fluoroprobe (C-SNARF-4) for pH microenvironment analysis in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol. 2005;71:2501–2510.
  • Tian Y, Su F, Weber W, et al. A series of naphthalimide derivatives as intra and extracellular pH sensors. Biomaterials. 2010b;31:7411–7422.
  • Tsujimoto K, Semadeni M, Huflejt M, et al. Intracellular pH of Halobacteria can be determined by the fluorescent dye 2',7'-bis(carboxyethyl)-5(6)-carboxyfluorescein. Biochem Biophys Res Commun. 1988;155:123–129.
  • Aono R, Ito M, Machida T. Contribution of the cell wall component teichuronopeptide to pH homeostasis and alkaliphily in the alkaliphile Bacillus lentus C-125. J Bacteriol. 1999;181:6600–6606.
  • Dunn KW, Mayor S, Myers JN, et al. Applications of ratio fluorescence microscopy in the study of cell physiology. FASEB J. 1994;8:573–582.
  • Molenaar D, Bolhuis H, Abee T, et al. The efflux of a fluorescent-probe is catalyzed by an Atp-driven extrusion system in Lactococcus lactis. J Bacteriol. 1992;174:3118–3124.
  • Awaji T, Hirasawa A, Shirakawa H, et al. Novel green fluorescent protein-based ratiometric indicators for monitoring pH in defined intracellular microdomains. Biochem Biophys Res Commun. 2001;289:457–462.
  • Wilks JC, Slonczewski JL. pH of the cytoplasm and periplasm of Escherichia coli: rapid measurement by green fluorescent protein fluorimetry. J Bacteriol. 2007;189:5601–5607.
  • Modi S, Nizak C, Surana S, et al. Two DNA nanomachines map pH changes along intersecting endocytic pathways inside the same cell. Nat Nanotechnol. 2013;8:459–467.
  • Yang M, Jalloh AS, Wei W, et al. Biocompatible click chemistry enabled compartment-specific pH measurement inside E. coli. Nat Commun. 2014;5:4981
  • Smith JL. The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J Food Protect. 2003;66:1292–1303.
  • Small P, Blankenhorn D, Welty D, et al. Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J Bacteriol. 1994;176:1729–1737.
  • Jin Y, Tian Y, Zhang W, et al. Tracking bacterial infection of macrophages using a novel red-emission pH sensor. Anal Bioanal Chem. 2010;398:1375–1384.
  • Hidalgo G, Burns A, Herz E, et al. Functional tomographic fluorescence imaging of pH microenvironments in microbial biofilms by use of silica nanoparticle sensors. Appl Environ Microb. 2009;75:7426–7435.
  • Wang XD, Meier RJ, Wolfbeis OS. Fluorescent pH-sensitive nanoparticles in an agarose matrix for imaging of bacterial growth and metabolism. Angew Chem Int Ed Engl. 2013a;52:406–409.
  • Wang FL, Raval Y, Chen HY, et al. Development of luminescent pH sensor films for monitoring bacterial growth through tissue. Adv Healthc Mater. 2014a;3:197–204.
  • Aragones J, Fraisl P, Baes M, et al. Oxygen sensors at the crossroad of metabolism. Cell Metab. 2009;9:11–22.
  • Ward JPT. Oxygen sensors in context. Biochim Biophys Acta. 2008;1777:1–14.
  • Potzkei J, Kunze M, Drepper T, et al. Real-time determination of intracellular oxygen in bacteria using a genetically encoded FRET-based biosensor. BMC Biol. 2012;10:28
  • Ernst JF, Tielker D. Responses to hypoxia in fungal pathogens. Cell Microbiol. 2009;11:183–190.
  • Hassett DJ, Sutton MD, Schurr MJ, et al. Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol. 2009;17:130–138.
  • Rustad TR, Sherrid AM, Minch KJ, et al. Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol. 2009;11:1151–1159.
  • Schobert M, Tielen P. Contribution of oxygen-limiting conditions to persistent infection of Pseudomonas aeruginosa. Future Microbiol. 2010;5:603–621.
  • Coates JD, Anderson RT. Emerging techniques for anaerobic bioremediation of contaminated environments. Trends Biotechnol. 2000;18:408–412.
  • Karakashev D, Thomsen AB, Angelidaki I. Anaerobic biotechnological approaches for production of liquid energy carriers from biomass. Biotechnol Lett. 2007;29:1005–1012.
  • Loffler FE, Edwards EA. Harnessing microbial activities for environmental cleanup. Curr Opin Biotechnol. 2006;17:274–284.
  • Mckinlay JB, Harwood CS. Photobiological production of hydrogen gas as a biofuel. Curr Opin Biotechnol. 2010;21:244–251.
  • Fercher A, Borisov SM, Zhdanov AV, et al. Intracellular O-2 sensing probe based on cell-penetrating phosphorescent nanoparticles. ACS Nano. 2011;5:5499–5508.
  • Wang XD, Stolwijk JA, Lang T, et al. Ultra-small, highly stable, and sensitive dual nanosensors for imaging intracellular oxygen and pH in cytosol. J Am Chem Soc. 2012;134:17011–17014.
  • Xu H, Aylott JW, Kopelman R, et al. A real-time ratiometric method for the determination of molecular oxygen inside living cells using sol-gel-based spherical optical nanosensors with applications to rat C6 glioma. Anal Chem. 2001;73:4124–4133.
  • Ji J, Rosenzweig N, Jones I, et al. Novel fluorescent oxygen indicator for intracellular oxygen measurements. J Biomed Opt. 2002;7:404–409.
  • Koo YEL, Cao YF, Kopelman R, et al. Real-time measurements of dissolved oxygen inside live cells by organically modified silicate fluorescent nanosensors. Anal Chem. 2004;76:2498–2505.
  • Mcnamara KP, Rosenzweig Z. Dye-encapsulating liposomes as fluorescence-based oxygen nanosensors. Anal Chem. 1998;70:4853–4859.
  • O'riordan TC, Fitzgerald K, Ponomarev GV, et al. Sensing intracellular oxygen using near-infrared phosphorescent probes and live-cell fluorescence imaging. Am J Physiol Regul Integr Comp Physiol. 2007;292:R1613–R1620.
  • Saito T, Asakura N, Kamachi T, et al. Oxygen concentration imaging in a single living cell using phosphorescence lifetime of Pt-porphyrin. J Porphyr Phthalocya. 2007;11:160–164.
  • O'donovan C, Hynes J, Yashunski D, et al. Phosphorescent oxygen-sensitive materials for biological applications. J Mater Chem. 2005;15:2946–2951.
  • Su FY, Alam R, Mei Q, et al. Nanostructured oxygen sensor-using micelles to incorporate a hydrophobic platinum porphyrin. PLoS One. 2012;7:e33390
  • Borisov SM, Mayr T, Klimant I. Poly(styrene-block-vinylpyrrolidone) beads as a versatile material for simple fabrication of optical nanosensors. Anal Chem. 2008;80:573–582.
  • Zhdanov AV, Ogurtsov VI, Taylor CT, et al. Monitoring of cell oxygenation and responses to metabolic stimulation by intracellular oxygen sensing technique. Integr Biol (Camb). 2010;2:443–451.
  • Wang XD, Gorris HH, Stolwijk JA, et al. Self-referenced RGB color imaging of intracellular oxygen. Chem Sci. 2011;2:901–906.
  • Brasuel M, Kopelman R, Aylott JW, et al. Production, characteristics and applications of fluorescent PEBBLE nanosensors: potassium, oxygen, calcium and pH imaging inside live cells. Sensor Mater. 2002;14:309–338.
  • Garcia JR, Cha HJ, Rao G, et al. Microbial NAR-GFP cell sensors reveal oxygen limitations in highly agitated and aerated laboratory-scale fermentors. Microb Cell Fact. 2009;8:6
  • Borisov SM, Fischer R, Saf R, et al. Exceptional oxygen sensing properties of new blue light-excitable highly luminescent europium(III) and gadolinium(III) complexes. Adv Funct Mater. 2014;24:6548–6560.
  • Lehner P, Staudinger C, Borisov SM, et al. Ultra-sensitive optical oxygen sensors for characterization of nearly anoxic systems. Nat Commun. 2014;5:4460
  • Zhang GQ, Palmer GM, Dewhirst M, et al. A dual-emissive-materials design concept enables tumour hypoxia imaging. Nat Mater. 2009;8:747–751.
  • Esipova TV, Karagodov A, Miller J, et al. Two new “application in tumor imaging” oxyphors for biological oximetry: properties and application in tumor. Anal Chem. 2011;83:8756–8765.
  • Lecoq J, Parpaleix A, Roussakis E, et al. Simultaneous two-photon imaging of oxygen and blood flow in deep cerebral vessels. Nat Med. 2011;17:893–898.
  • Sakadzic S, Roussakis E, Yaseen MA, et al. Two-photon high-resolution measurement of partial pressure of oxygen in cerebral vasculature and tissue. Nat Methods. 2010;7:755–759.
  • Pang H-L, Kwok N-Y, Chow LM-C, et al. ORMOSIL oxygen sensors on polystyrene microplate for dissolved oxygen measurement. Sensor Actuat B. 2007;123:120–126.
  • Tian Y, Shumway BR, Gao W, et al. Influence of matrices on oxygen sensing of three sensing films with chemically conjugated platinum porphyrin probes and preliminary application for monitoring of oxygen consumption of Escherichia coli (E. coli). Sens Actuators B. 2010a;150:579–587.
  • Cywinski PJ, Moro AJ, Stanca SE, et al. Ratiometric porphyrin-based layers and nanoparticles for measuring oxygen in biosamples. Sensor Actuat B. 2009;135:472–477.
  • Staal M, Borisov SM, Rickelt LF, et al. Ultrabright planar optodes for luminescence life-time based microscopic imaging of O-2 dynamics in biofilms. J Microbiol Methods. 2011;85:67–74.
  • Kuhl M. Optical microsensors for analysis of microbial communities. Methods Enzymol. 2005;397:166–199.
  • Kuhl M, Rickelt LF, Thar R. Combined imaging of bacteria and oxygen in biofilms. Appl Environ Microbiol. 2007;73:6289–6295.
  • Kang DK, Ali MM, Zhang K, et al. Rapid detection of single bacteria in unprocessed blood using integrated comprehensive droplet digital detection. Nat Commun. 2014;5:5427
  • Yoshimoto N, Kida A, Jie X, et al. An automated system for high-throughput single cell-based breeding. Sci Rep. 2013;3:1191
  • Konopka MC, Strovas TJ, Ojala DS, et al. Respiration response imaging for real-time detection of microbial function at the single-cell level. Appl Environ Microbiol. 2011;77:67–72.
  • Molter TW, Mcquaide SC, Suchorolski MT, et al. A microwell array device capable of measuring single-cell oxygen consumption rates. Sens Actuators B Chem. 2009;135:678–686.
  • Kelbauskas L, Ashili SP, Houkal J, et al. Method for physiologic phenotype characterization at the single-cell level in non-interacting and interacting cells. J Biomed Opt. 2012;17:037008
  • Maruyama H, Matsuda Y, Niimi T, et al. Measurement of photosynthesis activity using single synecocystis SP. PCC 6803 on microchambers having gas barrier wall and fluorescence oxygen sensor. Paper presented at: 2012 International Symposium on Date of Conferenceon Micro-NanoMechatronics and Human Science (MHS); 4–7 Nov. 2012; Nagoya, Japan: Nagoya University; 2012; p. 476–478.
  • Vasylevska GS, Borisov SM, Krause C, et al. Indicator-loaded permeation-selective microbeads for use in fiber optic simultaneous sensing of pH and dissolved oxygen. Chem Mater. 2006;18:4609–4616.
  • Lu HG, Jin YG, Tian YQ, et al. New ratiometric optical oxygen and pH dual sensors with three emission colors for measuring photosynthetic activity in cyanobacteria. J Mater Chem. 2011;2011:19293–19301.
  • Schroder CR, Polerecky L, Klimant I. Time-resolved pH/pO2 mapping with luminescent hybrid sensors. Anal Chem. 2007;79:60–70.
  • Kocincova AS, Nagl S, Arain S, et al. Multiplex bacterial growth monitoring in 24-well microplates using a dual optical sensor for dissolved oxygen and pH. Biotechnol Bioeng. 2008;100:430–438.
  • Meier RJ, Schreml S, Wang XD, et al. Simultaneous photographing of oxygen and pH in vivo using sensor films. Angew Chem Int Ed Engl. 2011;50:10893–10896.
  • Zhou X, Su F, Tian Y, et al. Dually fluorescent core-shell microgels for ratiometric imaging in live antigen-presenting cells. PLoS One. 2014;9:e88185
  • Borchert NB, Ponomarev GV, Kerry JP, et al. O(2)/pH multisensor based on one phosphorescent dye. Anal Chem. 2011;83:18–22.
  • Ray A, Koo Lee YE, Epstein T, et al. Two-photon nano-PEBBLE sensors: subcellular pH measurements. Analyst. 2011;136:3616–3622.
  • Lim CS, Cho BR. Two-photon probes for biomedical applications. BMB Rep. 2013;46:188–194.
  • Aigner D, Borisov SM, Petritsch P, et al. Novel near infrared fluorescent pH sensors based on 1-aminoperylene bisimides covalently grafted onto poly(acryloylmorpholine). Chem Commun (Camb). 2013;49:2139–2141.
  • Hutter LH, Muller BJ, Koren K, et al. Robust optical oxygen sensors based on polymer-bound NIR-emitting platinum(II)-benzoporphyrins. J Mater Chem C. 2014;2:7589–7598.
  • Borisov SM, Seifner R, Klimant I. A novel planar optical sensor for simultaneous monitoring of oxygen, carbon dioxide, pH and temperature. Anal Bioanal Chem. 2011;400:2463–2474.

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