AccScience Publishing / IJB / Volume 10 / Issue 6 / DOI: 10.36922/ijb.4454
Submit to IJB
Cite this article
18
Download
453
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
RESEARCH ARTICLE

Fabrication of bacteriorhodopsin-embedded hydrogel construct for biocompatible photosensitive device

Mian Wu1,2,3 ,  Feng Lin1,2,3 ,  Yu Song1,2,3*
Show Less
1 Department of Mechanical Engineering, Tsinghua University, Beijing, China
2 Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing, China
3 Key Laboratory of Advanced Materials Processing Technology of Ministry of Education, Beijing, China
IJB 2024, 10(6), 4454 https://doi.org/10.36922/ijb.4454
Submitted: 6 August 2024 | Accepted: 24 September 2024 | Published: 25 September 2024
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Download PDF
Cite
XML
Abstract

Bacteriorhodopsin (br) is a promising photosensitive material with applications in energy conversion, biosensors, and optoelectronic devices due to its bio-sourced origin and photoelectrical properties. Despite advancements in recent years, the integration of br-based devices necessitates the use of materials with little biocompatibility and fabrication techniques with restricted customizability, limiting potential applications such as optocontrol of cell behavior, implants with 3D patterning for retinal disease treatment, and light-sensitive cell robots. To solve this limitation, this study presents a novel approach by embedding br into a hydrogel matrix. It utilizes an extrusion-based and 3D bioprinting technique, showcasing its light-sensitive characteristics within a fully biocompatible construct. The hydrogel, comprising gelatin and sodium alginate, offers excellent printability for generating structured designs with versatile patterns. Photoelectrical properties of the fabricated br-embedded hydrogel construct, such as differential response, light intensity sensitivity, and br concentration sensitivity, are identified through electrochemical characterization. The temporal and spatial pattern recognition ability, based on the photoelectrical characteristics, is demonstrated through modulated light illumination and different patterns of printed hydrogel construct. Pattern recognition ability was then applied to reconstruct images containing different Latin letters. This research presents a novel method for the fabrication of patterned hydrogel constructs with high biocompatibility and distinctive light-responsive properties, expanding the potential applications of br in bio-related scenarios.  

Graphical abstract
Keywords
Bacteriorhodopsin
Hydrogel construct
Photoelectrical response
Pattern recognition
Funding
Not applicable.
Conflict of interest
The authors declare they have no competing interests.
References
  1. Marin E, Boschetto F, Pezzotti G. Biomaterials and biocompatibility: an historical overview. J Biomed Mater Res A. 2020;108(8):1617-1633. doi: 10.1002/jbm.a.36930
  2. Biswal T, BadJena SK, Pradhan D. Sustainable biomaterials and their applications: a short review. Mater Today Proc. 2020;30:274-282. doi: 10.1016/j.matpr.2020.01.437
  3. Li YT, Tian Y, Tian H, et al. A review on bacteriorhodopsin-based bioelectronic devices. Sensors (Basel). 2018;18(5):1368. doi: 10.3390/s18051368
  4. Shin N, Lee SH, Cho Y, Park TH, Hong S. Bioelectronic skin based on nociceptive ion channel for human-like perception of cold pains. Small. 2020;16(30):2001469. doi: 10.1002/smll.202001469
  5. Kim D, Han SA, Kim JH, Lee JH, Kim SW, Lee SW. Biomolecular piezoelectric materials: from amino acids to living tissues. Adv Mater. 2020;32(14):1906989. doi: 10.1002/adma.201906989
  6. Lanyi JK. Understanding structure and function in the light-driven proton pump bacteriorhodopsin. J Struct Biol. 1998;124(2):164-178. doi: 10.1006/jsbi.1998.4044
  7. Oesterhelt D, Stoeckenius W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat New Biol. 1971;233(39):149-152. doi: 10.1038/newbio233149a0
  8. Lozier RH, Bogomolni RA, Stoeckenius W. Bacteriorhodopsin: a light-driven proton pump in Halobacterium halobium. Biophys J. 1975;15(9):955-962. doi: 10.1016/S0006-3495(75)85875-9
  9. Oesterhelt D. The purple membrane of Halobacterium halobium: a new system for light energy conversion. Ciba Found Symp. 1975;(31):147-167. doi: 10.1002/9780470720134.ch9
  10. Oesterhelt D. Bacteriorhodopsin as an example of a light‐driven proton pump. Angew Chem Int Ed Engl. 1976;15(1):17-24. doi: 10.1002/anie.197600171
  11. Stoeckenius W, Lozier RH, Bogomolni RA. Bacteriorhodopsin and the purple membrane of halobacteria. Biochim Biophys Acta 1979;505(3–4):215-278. doi: 10.1016/0304-4173(79)90006-5
  12. Váró G, Keszthelyi L. Photoelectric signals from dried oriented purple membranes of Halobacterium halobium. Biophys J. 1983;43(1):47-51. doi: 10.1016/S0006-3495(83)84322-7
  13. Kouyama T, Kouyama AN, Ikegami A. Bacteriorhodopsin is a powerful light-driven proton pump. Biophys J. 1987;51(5):839-841. doi: 10.1016/S0006-3495(87)83411-2
  14. Kikukawa T, Araiso T, Mukasa K, Shimozawa T, Kamo N. The molecular motion of bacteriorhodopsin mutant D96N in the purple membrane. FEBS Lett. 1995;377(3): 502-504. doi: 10.1016/0014-5793(95)01408-X
  15. Miyasaka TMT. Design of intelligent optical sensors with organized bacteriorhodopsin films. Jpn J Appl Phys. 1995;34(7S):3920. doi: 10.1143/JJAP.34.3920
  16. Miyasaka T, Koyama K, Itoh I. Quantum conversion and image detection by a bacteriorhodopsin-based artificial photoreceptor. Science. 1992;255(5042):342-344. doi: 10.1126/science.255.5042.342
  17. Lu Z, Wang J, Xiang X, Li R, Qiao Y, Li CM. Integration of bacteriorhodopsin with upconversion nanoparticles for NIR-triggered photoelectrical response. Chem Commun (Camb). 2015;51(29):6373-6376. doi: 10.1039/c5cc00457h
  18. Choi HG, Min J, Choi JW, Lee WH. Molecular photoreceptor consisting of bacteriorhodopsin/flavin complex Langmuir– Blodgett films. Biosensor Bioelectron. 1998;13(10):1069- 1075. doi: 10.1016/S0956-5663(98)00073-6
  19. Hasegawa H, Sakamoto K, Shomura K, et al. Biomaterial-based biomimetic visual sensors: inkjet patterning of bacteriorhodopsin. ACS Appl Mater Interfaces. 2023;15(38):45137-45145. doi: 10.1021/acsami.3c07540
  20. Okada-Shudo Y, Tanabe T, Mukai T, Kasai K, Zhang Y, Watanabe M. Directionally selective motion detection with bacteriorhodopsin patterned sensor. Synth Met. 2016;222:249-254. doi: 10.1016/j.synthmet.2016.10.020
  21. Lv Y, Yang N, Li S, Lu S, Xiang Y. A novel light-driven pH-biosensor based on bacteriorhodopsin. Nano Energy. 2019;66:104129. doi: 10.1016/j.nanoen.2019.104129
  22. Walczak KA, Bergstrom PL, Friedrich CR. Light sensor platform based on the integration of bacteriorhodopsin with a single electron transistor. Act Passive Electron Compon. 2011;2011:1-7. doi: 10.1155/2011/586924
  23. Chen HM, Jheng KR, Yu AD. Direct, label-free, selective, and sensitive microbial detection using a bacteriorhodopsin-based photoelectric immunosensor. Biosens Bioelectron. 2017;91:24-31. doi: 10.1016/j.bios.2016.12.032
  24. Ahmadi M, Yeow JTW. Fabrication and characterization of a radiation sensor based on bacteriorhodopsin. Biosens Bioelectron. 2011;26(5):2171-2176. doi: 10.1016/j.bios.2010.09.029
  25. Ahmadi M, Osei EK, Yeow JTW. Bacteriorhodopsin for superficial X-ray sensing. Sens Actuat B Chem. 2012;166- 167:177-183. doi: 10.1016/j.snb.2012.02.037
  26. Choi HG, Jung WC, Min J, Lee WH, Choi JW. Color image detection by biomolecular photoreceptor using bacteriorhodopsin-based complex LB films. Biosens Bioelectron. 2001;16(9):925-935. doi: 10.1016/s0956-5663(01)00211-1
  27. Kim JH, Kim DH, So JH, Koo HJ. Toward eco-friendly dye-sensitized solar cells (DSSCs): natural dyes and aqueous electrolytes. Energies. 2021;15(1):219. doi: 10.3390/en15010219
  28. Devi P, Thakur A, Ghosh D, et al. Boosting photoelectrochemical performance of GaN nanowall network photoanode with bacteriorhodopsin. Int J Hydrogen Energy. 2020;45(1):103-111. doi: 10.1016/j.ijhydene.2019.10.184
  29. Wu M, Lin F, Song Y. Engineered bacteriorhodopsin film with oriented patterns for the improvement of the photoelectric response. Int J Mol Sci. 2022;23(24):16079. doi: 10.3390/ijms232416079
  30. Molaeirad A, Rezaeian N. Oriented assembly of bacteriorhodopsin on ZnO nanostructured electrode for enhanced photocurrent generation. Biotechnol Appl Biochem. 2015;62(4):489-493. doi: 10.1002/bab.1294
  31. Renugopalakrishnan V, Barbiellini B, King C, et al. Engineering a robust photovoltaic device with quantum dots and bacteriorhodopsin. J Phys Chem C Nanomater Interfaces. 2014;118(30):16710-16717. doi: 10.1021/jp502885s
  32. Lu S, Guo Z, Xiang Y, Jiang L. Photoelectric frequency response in a bioinspired bacteriorhodopsin/ alumina nanochannel hybrid nanosystem. Adv Mater. 2016;28(44):9851-9856. doi: 10.1002/adma.201603809
  33. Chellamuthu J, Nagaraj P, Chidambaram SG, Sambandam A, Muthupandian A. Enhanced photocurrent generation in bacteriorhodopsin based bio-sensitized solar cells using gel electrolyte. J Photochem Photobiol B. 2016;162:208-212. doi: 10.1016/j.jphotobiol.2016.06.044
  34. Naseri N, Janfaza S, Irani R. Visible light switchable bR/TiO2 nanostructured photoanodes for bio-inspired solar energy conversion. RSC Adv. 2015;5(24): 18642-18646. doi: 10.1039/C4RA16188B
  35. Molaeirad A, Janfaza S, Karimi-Fard A, Mahyad B. Photocurrent generation by adsorption of two main pigments of Halobacterium salinarum on TiO2 nanostructured electrode. Biotechnol Appl Biochem. 2015;62(1):121-125. doi: 10.1002/bab.1244
  36. Mohammadpour R, Janfaza S. Efficient nanostructured biophotovoltaic cell based on bacteriorhodopsin as biophotosensitizer. ACS Sustain Chem Eng. 2015;3(5):809- 813. doi: 10.1021/sc500617w
  37. Guo Z, Liang D, Rao S, Xiang Y. Heterogeneous bacteriorhodopsin/gold nanoparticle stacks as a photovoltaic system. Nano Energy. 2015;11:654-661. doi: 10.1016/j.nanoen.2014.11.026
  38. Hug H, Bader M, Mair P, Glatzel T. Biophotovoltaics: natural pigments in dye-sensitized solar cells. Appl Energy. 2014;115:216-225. doi: 10.1016/j.apenergy.2013.10.055
  39. Kumara NTRN, Ekanayake P, Lim A, et al. Layered co-sensitization for enhancement of conversion efficiency of natural dye sensitized solar cells. J Alloys Compoun. 2013;581:186-191. doi: 10.1016/j.jallcom.2013.07.039
  40. Yen CW, Hayden SC, Dreaden EC, Szymanski P, El-Sayed MA. Tailoring plasmonic and electrostatic field effects to maximize solar energy conversion by bacteriorhodopsin, the other natural photosynthetic system. Nano Lett. 2011;11(9):3821-3826. doi: 10.1021/nl2018959
  41. Thavasi V, Lazarova T, Filipek S, et al. Study on the feasibility of bacteriorhodopsin as bio-photosensitizer in excitonic solar cell: a first report. J Nanosci Nanotech. 2009;9(3): 1679-1687. doi: 10.1166/jnn.2009.si07
  42. Li R, Hu F, Bao Q, et al. Enhancement of photoelectric response of bacteriorhodopsin by multilayered WO3·H2O nanocrystals/PVA membrane. Chem Commun. 2010;46(5):689-691. doi: 10.1039/b923354g
  43. Zabut B, Elkahlout K, Yücel M, Gunduz U, Turker L, Eroglu I. Hydrogen gas production by combined systems of Rhodobacter sphaeroides O.U.001 and Halobacterium salinarum in a photobioreactor. Int J Hydrogen Energy. 2006;31:1553-1562. doi: 10.1016/j.ijhydene.2006.06.023
  44. Chen F, Qing Y, Wu H, Hou X. Optical storage characters of bacteriorhodopsin molecule film. Proc SPIE. 2002;4536. doi: 10.1117/12.409233
  45. Yu X, Yao B, Lei M, Gao P, Ma B. Femtosecond laser-induced permanent anisotropy in bacteriorhodopsin films and applications in optical data storage. J Modern Optic. 2013;60(4):309-314. doi: 10.1080/09500340.2013.774067
  46. Yao B, Lei M, Ren L, et al. Polarization multiplexed write-once–read-many optical data storage in bacteriorhodopsin films. Opt Lett. 2005;30(22):3060-3062. doi: 10.1364/ol.30.003060
  47. Chen F, Hou X, Li BF, Jiang L, Hammp N. Optical information storage of bacteriorhodopsin molecule film: experimental study. Mater Sci Eng B. 2000;76(1):76-78. doi: 10.1016/S0921-5107(00)00399-8
  48. Hampp NA, Neebe M, Seitz A. Printing inks containing the photochromic protein bacteriorhodopsin. In: Optical Security and Counterfeit Deterrence Techniques III. SPIE, 2000;3973:118-125. doi: 10.1117/12.382181
  49. Hampp N, Neebe M. Bacteriorhodopsin-based multilevel optical security features. In: Optical Security and Counterfeit Deterrence Techniques VI. SPIE, 2006;6075:256-264. doi: 10.1117/12.642627
  50. Ostrovsky MA, Smitienko OA, Bochenkova AV, Feldman TB. Similarities and differences in photochemistry of Type I and Type II rhodopsins. Biochem Moscow. 2023;88(10): 1528-1543. doi: 10.1134/S0006297923100097
  51. Sabari Girisun TC, Jeganathan C, Pavithra N, Anandan S. Structurally modified bacteriorhodopsin as an efficient bio-sensitizer for solar cell applications. Eur Biophys J. 2019;48(1):61-71. doi: 10.1007/s00249-018-1331-1
  52. Janfaza S, Molaeirad A, Mohamadpour R, Khayati M, Mehrvand J. Efficient bio-nano hybrid solar cells via purple membrane as sensitizer. BioNanoSci. 2014;4(1):71-77. doi: 10.1007/s12668-013-0118-1
  53. Das S, Wu C, Song Z, et al. Bacteriorhodopsin enhances efficiency of perovskite solar cells. ACS Appl Mater Interfaces. 2019;11(34):30728-30734. doi: 10.1021/acsami.9b06372
  54. Jeganathan C, Sabari Girisun TC, Vijaya S, Anandan S. Bacteriorhodopsin-sensitized preferentially oriented one-dimensional TiO2 nanorod polymorphs as efficient photoanodes for high-performance bio-sensitized solar cells. Appl Nanosci. 2019;9(2):189-208. doi: 10.1007/s13204-018-0905-7
  55. Yao B, Wang Y, Lei M, Zheng Y. Characteristics and mechanisms of the two types of photoelectric differential response of bacteriorhodopsin-based photocell. Biosens Bioelectron. 2003;19(4):283-287. doi: 10.1016/S0956-5663(03)00211-2
  56. Wang Y, Wu J, Ma D, Ding J. Preparation of a cross-linked gelatin/bacteriorhodopsin film and its photochromic properties. Sci China Chem. 2011;54(2):405-409. doi: 10.1007/s11426-010-4213-7
  57. Ma D, Zhao Y, Wu J, Cui T, Ding J. A block-copolymer hydrogel encapsulates bacteriorhodopsin and produces the longest photochromic response of the membrane protein under high water content conditions. Soft Matter. 2009;5(23):4635-4637. doi: 10.1039/b917438a
  58. Hsieh FY, Han HW, Chen XR, Yang CS, Wei Y, Hsu SH. Non-viral delivery of an optogenetic tool into cells with self-healing hydrogel. Biomaterials. 2018;174:31-40. doi: 10.1016/j.biomaterials.2018.05.014
  59. Ma Y, Zhang Y, Cai S, et al. Flexible hybrid electronics for digital healthcare. Adv Mater. 2020;32(15):1902062. doi: 10.1002/adma.201902062
  60. Wang L, Xu T, Zhang X. Multifunctional conductive hydrogel-based flexible wearable sensors. TrAC Trends Anal Chem. 2021;134:116130. doi: 10.1016/j.trac.2020.116130
  61. Ling Y, An T, Yap LW, Zhu B, Gong S, Cheng W. Disruptive, soft, wearable sensors. Adv Mater. 2020;32(18):1904664. doi: 10.1002/adma.201904664
  62. Han F, Xie X, Wang T, et al. Wearable hydrogel‐based epidermal sensor with thermal compatibility and long term stability for smart colorimetric multi‐signals monitoring. Adv Healthc Mater. 2023;12(3):2201730. doi: 10.1002/adhm.202201730
  63. Persaud A, Maus A, Strait L, Zhu D. 3D bioprinting with live cells. Eng Regen. 2022;3(3):292-309. doi: 10.1016/j.engreg.2022.07.002
  64. Dey M, Ozbolat IT. 3D bioprinting of cells, tissues and organs. Sci Rep. 2020;10(1):14023. doi: 10.1038/s41598-020-70086-y
  65. Gai K, Yang M, Chen W, et al. Development of neural cells and spontaneous neural activities in engineered brain-like constructs for transplantation. Adv Healthc Mater. 2024;2401419. doi: 10.1002/adhm.202401419
  66. Lien SM, Ko LY, Huang TJ. Effect of crosslinking temperature on compression strength of gelatin scaffold for articular cartilage tissue engineering. Mater Sci Eng C. 2010;30(4):631-635. doi: 10.1016/j.msec.2010.02.019
  67. Chu LK, Yen CW, El-Sayed MA. Bacteriorhodopsin-based photo-electrochemical cell. Biosens Bioelectron. 2010;26(2):620-626. doi: 10.1016/j.bios.2010.07.01
  68. Liu W, Liu F, Zhang T. An optoelectronic device based on bacteriorhodopsin with modulated photocurrent waveform. Opt Mater. 2022;133:112937. doi: 10.1016/j.optmat.2022.112937

 

 

 

 

Share
Back to top
International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept