Analytical and Bioanalytical Chemistry

, Volume 402, Issue 10, pp 3237–3244 | Cite as

A photosynthetic biosensor with enhanced electron transfer generation realized by laser printing technology

  • Eleftherios Touloupakis
  • Christos Boutopoulos
  • Katia Buonasera
  • Ioanna Zergioti
  • Maria Teresa Giardi
Original Paper

Abstract

One of the limits of current electrochemical biosensors is a lack of methods providing stable and highly efficient junctions between biomaterial and solid-state devices. This paper shows how laser-induced forward transfer (LIFT) can enable efficient electron transfer from photosynthetic biomaterial immobilized on screen-printed electrodes (SPE). The ideal pattern, in terms of photocurrent signal of thylakoid droplets giving a stable response signal with a current intensity of approximately 335 ± 13 nA for a thylakoid mass of 28 ± 4 ng, was selected. It is shown that the efficiency of energy production of a photosynthetic system can be strongly enhanced by the LIFT process, as demonstrated by use of the technique to construct an efficient and sensitive photosynthesis-based biosensor for detecting herbicides at nanomolar concentrations.

Keywords

Laser printing Biosensor Photosynthesis Herbicides 

Notes

Acknowledgements

The work discussed in this paper used technology developed in projects with financial support from the European Commission (e-LIFT FP7 ICT, grant agreement no. 247868; BEEP-C-EN FP 7-SME-2008-01, grant agreement no. 231082, SENSBIOSYN FP 7-SME-2008-01, grant agreement no. 232522), which is gratefully acknowledged.

References

  1. 1.
    Luong JHT, Male KB, Glennon JD (2008) Biosensor technology: technology push versus market pull. Biotechnol Adv 26(5):492–500CrossRefGoogle Scholar
  2. 2.
    Rodriguez-Mozaz S, Lopez de Alda MJ, Barceló D (2006) Biosensors as useful tools for environmental analysis and monitoring. Anal Bioanal Chem 386:1025–1041CrossRefGoogle Scholar
  3. 3.
    Giardi MT, Pace E (2005) Photosynthetic proteins for technological applications. Trends Biotechnol 23(5):257–263CrossRefGoogle Scholar
  4. 4.
    Gant E (1996) Pigment protein complexes and the concept of the photosynthetic unit: chlorophyll complexes and phycobilisomes. Photosynth Res 48:47–53CrossRefGoogle Scholar
  5. 5.
    Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342CrossRefGoogle Scholar
  6. 6.
    Oettmeier W (2003) In: Plimmer JR (ed) Encyclopedia of agrochemicals vol. 2. John Wiley & Sons, Inc, HobokenGoogle Scholar
  7. 7.
    Ackerman F (2007) The economics of atrazine. Int J Occup Environ Health 13:441–449Google Scholar
  8. 8.
    Shitanda I, Takamatsu S, Watanabe K, Itagaki M (2009) Amperometric screen-printed algal biosensor with flow injection analysis system for detection of environmental toxic compounds. Electrochim Acta 54:4933–4936CrossRefGoogle Scholar
  9. 9.
    Li J, Wei X, Peng T (2005) Fabrication of herbicide biosensors based on the inhibition of enzyme activity that catalyzes the scavenging of hydrogen peroxide in a thylakoid membrane. Anal Sci 21:1217–1222CrossRefGoogle Scholar
  10. 10.
    Rouillon R, Boucher N, Gingras Y, Carpentier R (2000) Immobilization of photosystem II submembrane fractions in poly(vinylalcohol) bearing styrylpyridium groups. Application to the detection of heavy metals. J Chem Technol Biotechnol 75:1003–1007CrossRefGoogle Scholar
  11. 11.
    Rodriquez M, Sanders CA, Greenbaum E (2002) Biosensors for rapid monitoring of primary-source drinking water using naturally occurring photosynthesis. Biosens Bioelectron 17:843–849CrossRefGoogle Scholar
  12. 12.
    Podola B, Melkonian M (2003) A long-term operating algal biosensor for the rapid detection of volatile toxic compounds. J Appl Phycol 15:415–424CrossRefGoogle Scholar
  13. 13.
    Moreno-Garrido I (2008) Microalgae immobilization: current techniques and uses. Bioresour Technol 99:3949–3964CrossRefGoogle Scholar
  14. 14.
    Touloupakis E, Giannoudi L, Piletsky SA, Guzzella L, Pozzoni F, Giardi MT (2005) A multi-biosensor based on immobilized photosystem II on screen-printed electrodes for the detection of herbicides in river water. Biosens Bioelectron 20:1984–1992CrossRefGoogle Scholar
  15. 15.
    Bettazzi F, Laschi S, Mascini M (2007) One-shot screen-printed thylakoid membrane-based biosensor for the detection of photosynthetic inhibitors in discrete samples. Anal Chim Acta 589:14–21CrossRefGoogle Scholar
  16. 16.
    Campàs M, Carpentier R, Rouillon R (2008) Plant tissue-and photosynthesis-based biosensors. Biotechnol Adv 26(4):370–378CrossRefGoogle Scholar
  17. 17.
    Avramescu A, Rouillon R, Carpentier R (1999) Potential for use of a cyanobacterium Synechocystis sp. immobilized in poly(vinylalcohol): application to the detection of pollutants. Biotechnol Tech 13:559–562CrossRefGoogle Scholar
  18. 18.
    Koblitzek M, Maly J, Masojidek J, Komenda J, Kucera T, Giardi MT, Mattoo AK, Pilloton R (2002) A biosensor for the detection of triazine and phenylurea herbicides designed using photosystem II coupled to a screen-printed electrode. Biotechnol Bioeng 78:110–116CrossRefGoogle Scholar
  19. 19.
    Maly J, Krejci J, Ilie M, Jakubka L, Masojídek J, Pilloton R, Sameh K, Steffan P, Stryhal Z, Sugiura M (2005) Monolayers of photosystem II on gold electrodes with enhanced sensor response–effect of porosity and protein layer arrangement. Anal Bioanal Chem 381(8):1558–1567CrossRefGoogle Scholar
  20. 20.
    Bhalla V, Zazubovich V (2011) Self-assembly and sensor response of photosynthetic reaction centers on screen-printed electrodes. Anal Chim Acta 707(1–2):184–190CrossRefGoogle Scholar
  21. 21.
    Rouillon R, Tocabens M, Carpentier R (1999) A photoelectrochemical cell for detecting pollutant-induced effects on the activity of immobilized cyanobacterium Synechococcus sp. PCC 7942. Enzyme Microb Technol 25:230–235CrossRefGoogle Scholar
  22. 22.
    Giardi MT, Guzzella L, Euzet P, Rouillon R, Esposito D (2005) Detection of herbicide subclasses by an optical multibiosensor based on an array of photosystem II mutants. Environ Sci Technol 39:5378–5384CrossRefGoogle Scholar
  23. 23.
    Barthelmebs L, Carpentier R, Rouillon R (2011) Physical and chemical immobilization methods of photosynthetic materials. Methods Mol Biol 684:247–256CrossRefGoogle Scholar
  24. 24.
    Shitanda I, Takada K, Sakai Y, Tatsuma T (2005) Compact amperometric algal biosensors for the evaluation of water toxicity. Anal Chim Acta 530:191–197CrossRefGoogle Scholar
  25. 25.
    Ringeisen BR, Wu PK, Kim H, Piqué A, Auyeung RYC, Young HD, Chrisey DB, Krizman DB (2002) Picoliter-scale protein microarrays by laser direct write. Biotechnol Prog 18:1126–1129CrossRefGoogle Scholar
  26. 26.
    Wu PK, Ringeisen BR, Krizman DB, Frondoza CG, Brooks M, Bubb DM, Auyeung RCY, Pique A, Spargo B, McGill RA, Chrisey DB (2003) Laser manipulation of biomaterials: Matrix-Assisted Pulsed-Laser Evaporation (MAPLE) and MAPLE - Direct Write (MDW). Rev Sci Instrum 74:2546–2557CrossRefGoogle Scholar
  27. 27.
    Karaiskou A, Zergioti I, Fotakis C, Kapsetaki M, Kafetzopoulos D (2003) Microfabrication of biomaterials by the sub-ps laser-induced forward transfer process. Appl Surf Sci 245:208–209Google Scholar
  28. 28.
    Serra P, Fernandez Pradas JM, Colina M, Duocastella M, Dominguez J, Morenza JL (2006) Laser-induced forward transfer: a direct-writing technique for biosensors preparation. J Laser Micro Nanoeng 1:236–242CrossRefGoogle Scholar
  29. 29.
    Guillemot F, Souquet A, Catros S, Guillotin B, Lopez J, Faucon M, Pippenger B, Bareille R, Rémy M, Bellance S, Chabassier P, Fricain JC, Amédée J (2010) High-throughput laser printing of cells and biomaterials for tissue engineering. Acta Biomater 6:2494–2500CrossRefGoogle Scholar
  30. 30.
    Boutopoulos C, Touloupakis E, Pezzotti I, Giardi MT, Zergioti I (2011) Direct laser immobilization of photosynthetic material on screen printed electrodes for amperometric biosensor. Appl Phys Lett 98:093703CrossRefGoogle Scholar
  31. 31.
    Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156CrossRefGoogle Scholar
  32. 32.
    Boutopoulos C, Andreakou P, Kafetzopoulos D, Chatzandroulis S, Zergioti I (2008) Direct laser printing of biotin microarrays on low temperature oxide on Si substrates. Phys Status Solidi A 205:2505–2508CrossRefGoogle Scholar
  33. 33.
    Boutopoulos C, Pandis C, Giannakopoulos K, Pissis P, Zergioti I (2010) Polymer/carbon nanotube composite patterns via laser induced forward transfer. Appl Phys Lett 96:041104CrossRefGoogle Scholar
  34. 34.
    Deegan R, Bakajin O, Dupont T, Huber G (1997) Capillary flow as the cause of ring stains from dried liquid drops. Nature 389:827–829CrossRefGoogle Scholar
  35. 35.
    Duocastella M, Fernández-Pradas JM, Serra P, Morenza JL (2008) Jet formation in the laser forward transfer of liquids. Appl Phys A 93:453–456CrossRefGoogle Scholar
  36. 36.
    Deng T, Varanasi KK, Hsu M, Bhate N, Keimel C, Stein J, Blohm M (2009) Nonwetting of impinging droplets on textured surfaces. Appl Phys Lett 94:133109CrossRefGoogle Scholar
  37. 37.
    Wakabayashi K, Böger P (2002) Target sites for herbicides: entering the 21st century. Pest Manag Sci 58:1149–1154CrossRefGoogle Scholar
  38. 38.
    Maly J, Masojidek J, Masci A, Ilie M, Cianci E, Foglietti V, Vastarella W, Pilloton R (2005) Direct mediatorless electron transport between the monolayer of photosystem II and poly(mercapto-p-benzoquinone) modified gold electrode-new design of biosensor for herbicide detection. Biosens Bioelectron 21:923–932CrossRefGoogle Scholar
  39. 39.
    Buck RP, Lindner E (1994) Recommendations for nomenclature of ionselective electrodes (IUPAC Recommendations 1994). Pure Appl Chem 66:2527–2536CrossRefGoogle Scholar
  40. 40.
    Vittadello M, Gorbunov MY, Mastrogiovanni DT, Wielunski LS, Garfunkel EL, Guerrero F, Kirilovsky D, Sugiura M, Rutherford AW, Safari A, Falkowski PG (2010) Photoelectron generation by photosystem II core complexes tethered to gold surfaces. ChemSusChem 3:471–475CrossRefGoogle Scholar
  41. 41.
    Kaniber S, Frolov L, Simmel FC, Holleitner AW, Carmeli C, Carmeli I (2009) Covalently binding the photosystem I to carbon nanotubes. Nano Lett 1:133–134Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Eleftherios Touloupakis
    • 1
    • 2
  • Christos Boutopoulos
    • 3
  • Katia Buonasera
    • 1
  • Ioanna Zergioti
    • 3
  • Maria Teresa Giardi
    • 1
  1. 1.Institute of CrystallographyNational Research CouncilRomeItaly
  2. 2.Biosensor srlRomeItaly
  3. 3.Department of PhysicsNational Technical University of AthensAthensGreece

Personalised recommendations