Skip to main content
SpringerLink
Log in

Protoporphyrin IX conjugated bacterial cellulose via diamide spacer arms with specific antibacterial photodynamic inactivation against Escherichia coli

  • Original Paper
  • Published:
Cellulose Aims and scope Submit manuscript

Abstract

Herein, protoporphyrin IX (PPIX) was covalently grafted onto a bacterial cellulose (BC) surface via three diamine spacer arms with different chain lengths. The obtained materials were characterized by spectroscopic (infrared, Raman, UV–Vis diffuse reflectance, electron paramagnetic and fluorescence) and physical (elemental, gravimetric) methods. Antibacterial efficacy was evaluated against Staphylococcus aureus and Escherichia coli, and the PPIX supported BC surface exhibited specific antibacterial photodynamic inactivation against E. coli. The 1,2-bis(2-aminoethoxy)ethane aminated BC immobilized the maximal amount of PPIX, and the resulting photosensitive surface achieved a 99.999% (1st cycle) inactivation efficiency against E. coli, but relatively low efficiency against S. aureus. A mechanism of Gram negative bacterial inactivation was proposed as the positively charged PPIX-conjugated BC surface coupled with sufficient 1O2 generation. Though the reusability of the as-fabricated materials needs to be further enhanced, this work provides a potent strategy for efficient photodynamic inactivation against Gram negative bacteria using neutral photosensitizers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Scheme 1
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abrahamse H, Hamblin MR (2016) New photosensitizers for photodynamic therapy. Biochem J 473:347–364

    Article  CAS  Google Scholar 

  • Brebu M, Uddin MA, Muto A, Sakata Y, Vasile C (2000) Composition of nitrogen-containing compounds in oil obtained from acrylonitrile-butadiene-styrene thermal degradation. Energy Fuels 14:920–928. https://doi.org/10.1021/ef000018v

    Article  CAS  Google Scholar 

  • Carpenter BL, Feese E, Sadeghifar H, Argyropoulos DS, Ghiladi RA (2012) Porphyrin-cellulose nanocrystals: a photobactericidal material that exhibits broad spectrum antimicrobial activity. Photochem Photobiol 88:527–536

    Article  CAS  Google Scholar 

  • Carpenter BL et al (2015) Synthesis, characterization, and antimicrobial efficacy of photomicrobicidal cellulose paper. Biomacromolecules 16:2482–2492. https://doi.org/10.1021/acs.biomac.5b00758

    Article  CAS  Google Scholar 

  • Castriciano MA et al (2017) Poly (carboxylic acid)-cyclodextrin/anionic porphyrin finished fabrics as photosensitizer releasers for antimicrobial photodynamic therapy. Biomacromol 18:1134–1144

    Article  CAS  Google Scholar 

  • Colpa DI, Fraaije MW (2016) High overexpression of dye decolorizing peroxidase TfuDyP leads to the incorporation of heme precursor protoporphyrin IX. J Mol Catal B Enzym 134:372–377. https://doi.org/10.1016/j.molcatb.2016.08.017

    Article  CAS  Google Scholar 

  • Cox GS, Whitten DG (1982) Mechanisms for the photooxidation of protoporphyrin IX in solution. J Am Chem Soc 104:516–521

    Article  CAS  Google Scholar 

  • Dahl T, RobertMiddenand W, Hartman P (1987) Pure singlet oxygen cytotoxicity for bacteria. Photochem Photobiol 46:345–352

    Article  CAS  Google Scholar 

  • Fernandes SC, Oliveira L, Freire CS, Silvestre AJ, Neto CP, Gandini A, Desbriéres J (2009) Novel transparent nanocomposite films based on chitosan and bacterial cellulose. Green Chem 11:2023–2029

    Article  CAS  Google Scholar 

  • Gottenbos B, van der Mei HC, Klatter F, Grijpma DW, Feijen J, Nieuwenhuis P, Busscher HJ (2003) Positively charged biomaterials exert antimicrobial effects on gram-negative bacilli in rats. Biomaterials 24:2707–2710

    Article  CAS  Google Scholar 

  • Henke P, Kozak H, Artemenko A, Kubát P, Forstová J, Jí Mosinger (2014) Superhydrophilic polystyrene nanofiber materials generating O2 (1Δg): postprocessing surface modifications toward efficient antibacterial effect. ACS Appl Mater Interfaces 6:13007–13014

    Article  CAS  Google Scholar 

  • Isago H (2015) Optical spectra of phthalocyanines and related compounds. Springer, Berlin

    Book  Google Scholar 

  • Jhonsi MA, Nithya C, Kathiravan A (2017) Unravel the interaction of protoporphyrin IX with reduced graphene oxide by vital spectroscopic techniques. Spectrochim Acta A Mol Biomol Spectrosc 178:86–93. https://doi.org/10.1016/j.saa.2017.01.059

    Article  CAS  Google Scholar 

  • Dolanský J, Henke P, Kubát P, Fraix A, Sortino S, Mosinger J (2015) Polystyrene nanofiber materials for visible-light-driven dual antibacterial action via simultaneous photogeneration of NO and O2 (1Δg). ACS Appl Mater Interfaces 7:22980–22989

    Article  Google Scholar 

  • Johnson BJ et al (2016) Porphyrin-modified antimicrobial peptide indicators for detection of bacteria. Sens Bio Sens Res 8:1–7. https://doi.org/10.1016/j.sbsr.2016.02.005

    Article  CAS  Google Scholar 

  • Jori G, Camerin M, Soncin M et al (2011) Antimicrobial photodynamic therapy: basic principles. In: Hamblin MR, Jori G (eds) Photodynamic inactivation of microbial pathogens: Medical and environmental applications. The Royal Sociey of Chemistry, Cambridge, pp 1–18

    Google Scholar 

  • Kim U-J, Kuga S, Wada M, Okano T, Kondo T (2000) Periodate oxidation of crystalline cellulose. Biomacromolecules 1:488–492. https://doi.org/10.1021/bm0000337

    Article  CAS  Google Scholar 

  • Kłodzińska E, Szumski M, Dziubakiewicz E, Hrynkiewicz K, Skwarek E, Janusz W, Buszewski B (2010) Effect of zeta potential value on bacterial behavior during electrophoretic separation. Electrophoresis 31:1590–1596

    Article  Google Scholar 

  • Koyama T, Yamada M, Matsuhashi M (1977) Formation of regular packets of Staphylococcus aureus cells. J Bacteriol 129:1518–1523

    CAS  Google Scholar 

  • Krouit M, Granet R, Krausz P (2009) Photobactericidal films from porphyrins grafted to alkylated cellulose—synthesis and bactericidal properties. Eur Polym J 45:1250–1259. https://doi.org/10.1016/j.eurpolymj.2008.11.036

    Article  CAS  Google Scholar 

  • Le Y, Guo D, Cheng B, Yu J (2013) Bio-template-assisted synthesis of hierarchically hollow SiO2 microtubes and their enhanced formaldehyde adsorption performance. Appl Surf Sci 274:110–116

    Article  CAS  Google Scholar 

  • Li H, Wu B, Mu C, Lin W (2011) Concomitant degradation in periodate oxidation of carboxymethyl cellulose. Carbohydr Polym 84:881–886. https://doi.org/10.1016/j.carbpol.2010.12.026

    Article  CAS  Google Scholar 

  • Li G, Nandgaonkar AG, Wang Q, Zhang J, Krause WE, Wei Q, Lucia LA (2017) Laccase-immobilized bacterial cellulose/TiO2 functionalized composite membranes: evaluation for photo- and bio-catalytic dye degradation. J Membr Sci 525:89–98. https://doi.org/10.1016/j.memsci.2016.10.033

    Article  CAS  Google Scholar 

  • Liu F, Soh Yan Ni A, Lim Y, Mohanram H, Bhattacharjya S, Xing B (2012) Lipopolysaccharide neutralizing peptide–porphyrin conjugates for effective photoinactivation and intracellular imaging of gram-negative bacteria strains. Bioconj Chem 23:1639–1647. https://doi.org/10.1021/bc300203d

    Article  CAS  Google Scholar 

  • Lv Y-Y, Wu J, Xu Z-K (2010) Colorimetric and fluorescent sensor constructing from the nanofibrous membrane of porphyrinated polyimide for the detection of hydrogen chloride gas. Sens Actuators B Chem 148:233–239. https://doi.org/10.1016/j.snb.2010.05.029

    Article  CAS  Google Scholar 

  • Lv P, Feng Q, Wang Q, Li G, Li D, Wei Q (2016) Biosynthesis of bacterial cellulose/carboxylic multi-walled carbon nanotubes for enzymatic biofuel cell application. Materials 9:183

    Article  Google Scholar 

  • Lv P et al (2017) Self-assembly of nitrogen-doped carbon dots anchored on bacterial cellulose and their application in iron ion detection. Carbohydr Polym 172:93–101

    Article  CAS  Google Scholar 

  • Mehta A, Zydney AL (2008) Effect of spacer arm length on the performance of charge-modified ultrafiltration membranes. J Membr Sci 313:304–314. https://doi.org/10.1016/j.memsci.2008.01.014

    Article  CAS  Google Scholar 

  • Moan J, Wold E (1979) Detection of singlet oxygen production by ESR. Nature 279:450–451. https://doi.org/10.1038/279450a0

    Article  CAS  Google Scholar 

  • Monier M, Abdel-Latif DA, Abou El-Reash YG (2016) Ion-imprinted modified chitosan resin for selective removal of Pd(II) ions. J Colloid Interface Sci 469:344–354. https://doi.org/10.1016/j.jcis.2016.01.074

    Article  CAS  Google Scholar 

  • Mosinger J, Mosinger B (1995) Photodynamic sensitizers assay: rapid and sensitive iodometric measurement. Experientia 51:106–109

    Article  CAS  Google Scholar 

  • Natarajan P, Raja C (2004) Studies on interpolymer self-organisation behaviour of protoporphyrin IX bound poly(carboxylic acid)s with complimentary polymers by means of fluorescence techniques. Eur Polym J 40:2291–2303. https://doi.org/10.1016/j.eurpolymj.2004.06.003

    Article  CAS  Google Scholar 

  • Ogi T, Kinoshita R, Ito S (2005) Spectroscopic and optical characterization of porphyrin chromophores incorporated into ultrathin polyimide films. J Colloid Interface Sci 286:280–287. https://doi.org/10.1016/j.jcis.2005.01.001

    Article  CAS  Google Scholar 

  • Onem H, Nadaroglu H (2014) Preparation and properties of purified phytase from oakbug milkcap (Lactarius quietus) immobilised on coated chitosan with iron nano particles and investigation of its usability in food industry. J Food Nutr Res 2:938–945

    Article  Google Scholar 

  • Rahimi R, Fayyaz F, Rassa M (2016) The study of cellulosic fabrics impregnated with porphyrin compounds for use as photo-bactericidal polymers. Mater Sci Eng C 59:661–668. https://doi.org/10.1016/j.msec.2015.10.067

    Article  CAS  Google Scholar 

  • Ringot C et al (2011) Triazinyl porphyrin-based photoactive cotton fabrics: preparation, characterization, and antibacterial activity. Biomacromolecules 12:1716–1723. https://doi.org/10.1021/bm200082d

    Article  CAS  Google Scholar 

  • Sharp RE, Diers JR, Bocian DF, Dutton PL (1998) Differential binding of iron (III) and zinc (II) protoporphyrin IX to synthetic four-helix bundles. J Am Chem Soc 120:7103–7104

    Article  CAS  Google Scholar 

  • Shrestha A, Hamblin MR, Kishen A (2014) Photoactivated rose bengal functionalized chitosan nanoparticles produce antibacterial/biofilm activity and stabilize dentin-collagen. Nanomed Nanotechnol Biol Med 10:491–501. https://doi.org/10.1016/j.nano.2013.10.010

    Article  CAS  Google Scholar 

  • Spagnul C, Turner LC, Boyle RW (2015) Immobilized photosensitizers for antimicrobial applications. J Photochem Photobiol B 150:11–30

    Article  CAS  Google Scholar 

  • Stanley SL, Scholle F, Zhu J, Lu Y, Zhang X, Situ X, Ghiladi RA (2016) Photosensitizer-embedded polyacrylonitrile nanofibers as antimicrobial non-woven textile. Nanomaterials 6:77

    Article  Google Scholar 

  • Tirapattur S, Belletête M, Drolet N, Leclerc M, Durocher G (2003) Steady-state and time-resolved studies of 2, 7-carbazole-based conjugated polymers in solution and as thin films: determination of their solid state fluorescence quantum efficiencies. Chem Phys Lett 370:799–804

    Article  CAS  Google Scholar 

  • Vallapa N, Wiarachai O, Thongchul N, Pan J, Tangpasuthadol V, Kiatkamjornwong S, Hoven VP (2011) Enhancing antibacterial activity of chitosan surface by heterogeneous quaternization. CarbohydR Polym 83:868–875. https://doi.org/10.1016/j.carbpol.2010.08.075

    Article  CAS  Google Scholar 

  • Vu TT et al (2009) New hindered BODIPY derivatives: solution and amorphous state fluorescence properties. J Phys Chem C 113:11844–11855

    Article  CAS  Google Scholar 

  • Wen X, Zhang X, Szewczyk G, El-Hussein A, Huang Y-Y, Sarna T, Hamblin MR (2017) Potassium iodide potentiates antimicrobial photodynamic inactivation mediated by Rose Bengal: in vitro and in vivo studies. AAC 61:00467–00417

    Article  Google Scholar 

  • Wu J, Meredith JC (2014) Assembly of Chitin Nanofibers into Porous Biomimetic Structures via Freeze Drying. ACS Macro Lett 3:185–190. https://doi.org/10.1021/mz400543f

    Article  CAS  Google Scholar 

  • Zhao G et al (2017) Co-porphyrin/carbon nitride hybrids for improved photocatalytic CO2 reduction under visible light. Appl Catal B 200:141–149

    Article  CAS  Google Scholar 

  • Zhou Z, Xiao Y, Hatton TA, Chung T-S (2009) Effects of spacer arm length and benzoation on enantioseparation performance of β-cyclodextrin functionalized cellulose membranes. J Membr Sci 339:21–27. https://doi.org/10.1016/j.memsci.2009.04.015

    Article  CAS  Google Scholar 

  • Zhu J, Sun G (2012) Preparation and photo-oxidative functions of poly(ethylene-co-methacrylic acid) (PE-co-MAA) nanofibrous membrane supported porphyrins. J Mater Chem 22:10581–10588. https://doi.org/10.1039/C2JM16703D

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge to International Joint Research Laboratory for Advanced Functional Textile Materials for helping with instruments operation and helpful discussions. We thank the financial support from the 111 Project (B17021), Recruitment Program of Foreign Experts (B; JSB2017016), National Natural Science Foundation (51641303) of China, Natural Science for Youth Foundation (51603090), the Priority Academic Program Development of Jiangsu Higher Education Institutions, the Top-notch Academic Programs Project of Jiangsu Higher Education Institutions, the Natural Science Foundation of Jiangsu Province (BK20150155), and the Fundamental Research Funds for the Central Universities (JUSRP51621A).

Author information

Authors and Affiliations

  1. Key Laboratory of Eco-Textiles, Ministry of Education, Jiangnan University, Wuxi, 214122, China

    Jiancheng Dong, Qingqing Wang, Yibing Cai & Qufu Wei

  2. Department of Chemistry, North Carolina State University, Raleigh, NC, 27695, USA

    Reza A. Ghiladi

Authors
  1. Jiancheng Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reza A. Ghiladi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qingqing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yibing Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qufu Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qufu Wei.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 2812 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, J., Ghiladi, R.A., Wang, Q. et al. Protoporphyrin IX conjugated bacterial cellulose via diamide spacer arms with specific antibacterial photodynamic inactivation against Escherichia coli. Cellulose 25, 1673–1686 (2018). https://doi.org/10.1007/s10570-018-1697-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10570-018-1697-3

Keywords

Search

Navigation