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Bacterial cellulose nanofibrous aerogels grafted with citric acid for absorption and separation of protein

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Abstract

The design and construction of high-performance protein absorbents are of great significance for obtaining highly purified proteins in the field of biotechnology and more. In this study, the highly carboxylated absorption media were fabricated for selective absorption of positively charged proteins by using bacterial cellulose (BC) nanofibrous aerogel (NFA) as a substrate material in concert with citric acid (CA). The obtained BC/CA NFAs exhibited highly interconnected open porous structure, surface hydrophilicity, large specific surface area (14.2 m2/g), good elasticity and compression fatigue resistance. BC/CA NFAs displayed a high lysozyme absorption capacity of 868.9 mg/g and fast equilibrium within 2.5 h. A dynamic lysozyme absorption capacity of 655.35 mg/g was achieved under the drive of gravity, meeting the demands of actual applications. Furthermore, BC/CA NFAs exhibited unique absorption selectivity performance, good reusability, as well as acid and alkaline resistance. A successful scale-up of such environmental friendliness, low cost and good reproducibility absorbents could provide a new perspective to develop next generation three-dimensional chromatographic media for substantial bio-separation applications.

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References

  • Amaly N, Ma Y, El-Moghazy AY, Sun G (2020) Copper complex formed with pyridine rings grafted on cellulose nanofibrous membranes for highly efficient lysozyme adsorption. Sep Purif Technol 250:117086

    Article  CAS  Google Scholar 

  • Arabkhani P, Asfaram A (2020) Development of a novel three-dimensional magnetic polymer aerogel as an efficient adsorbent for malachite green removal. J Hazard Mater 384:121394

    Article  CAS  PubMed  Google Scholar 

  • Arbita AA, Paul NA, Cox J, Zhao J (2022) Amino acid sequence of two new milk-clotting proteases from the macroalga Gracilaria edulis. Int J Biol Macromol 211:499–505

    Article  CAS  PubMed  Google Scholar 

  • Beaumont M, Jusner P, Gierlinger N, King AWT, Potthast A, Rojas OJ, Rosenau T (2021a) Unique reactivity of nanoporous cellulosic materials mediated by surface-confined water. Nat Commun 12(1):2513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beaumont M, Nypelo T, Konig J, Zirbs R, Opietnik M, Potthast A, Rosenau T (2016) Synthesis of redispersible spherical cellulose II nanoparticles decorated with carboxylate groups. Green Chem 18(6):1465–1468

    Article  CAS  Google Scholar 

  • Beaumont M, Tardy BL, Reyes G, Koso TV, Schaubmayr E, Jusner P, King AWT, Dagastine RR, Potthast A, Rojas OJ, Rosenau T (2021b) Assembling native elementary cellulose nanofibrils via a reversible and regioselective surface functionalization. J Am Chem Soc 143(41):17040–17046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Sharma SK, Sharma PR, Yeh HD, Johnson K, Hsiao BS (2019) Arsenic(III) removal by nanostructured dialdehyde cellulose-cysteine microscale and nanoscale fibers. ACS Omega 4(26):22008–22020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng P, Liu K, Wan YC, Hu W, Ji CC, Huang P, Guo QH, Xu J, Cheng Q, Wang D (2022) Solution viscosity-mediated structural control of nanofibrous sponge for RNA separation and purification. Adv Funct Mater 32(20):2112023

    Article  CAS  Google Scholar 

  • Chiou BS, Jafri H, Cao T, Robertson GH, Gregorski KS, Imam SH, Glenn GM, Orts WJ (2013) Modification of wheat gluten with citric acid to produce superabsorbent materials. J Appl Polym Sci 129(6):3192–3197

    Article  CAS  Google Scholar 

  • Chiu HT, Lin JM, Cheng TH, Chou SY, Huang CC (2012) Direct purification of lysozyme from chicken egg white using weak acidic polyacrylonitrile nanofiber-based membranes. J Appl Polym Sci 125:E616–E621

    Article  CAS  Google Scholar 

  • Das R, Lindstrom T, Sharma PR, Chi K, Hsiao BS (2022) Nanocellulose for sustainable water purification. Chem Rev 122(9):8936–9031

    Article  CAS  PubMed  Google Scholar 

  • Dou XY, Wang Q, Li ZL, Ju JP, Wang S, Hao LY, Sui KY, Xia YZ, Tan YQ (2019) Seaweed-derived electrospun nanofibrous membranes for ultrahigh protein adsorption. Adv Funct Mater 29(46):1905610

    Article  CAS  Google Scholar 

  • Ebrahimi A, Pazuki G, Mozaffarian M, Ahsaie FG, Abedini H (2023) Separation and purification of C-phycocyanin from spirulina platensis using aqueous two-phase systems based on triblock thermosensitive copolymers. Food Bioprocess Technol. https://doi.org/10.1007/s11947-023-03057-6

    Article  Google Scholar 

  • Fang K, Deng LG, Yin JY, Yang TH, Li JB, He W (2022) Recent advances in starch-based magnetic adsorbents for the removal of contaminants from wastewater: a review. Int J Biol Macromol 218:909–929

    Article  CAS  PubMed  Google Scholar 

  • Fu QX, Duan C, Yan ZS, Si Y, Liu LF, Yu JY, Ding B (2018) Electrospun nanofibrous composite materials: a versatile platform for high efficiency protein adsorption and separation. Compos Commun 8:92–100

    Article  Google Scholar 

  • Fu QX, Liu LF, Si Y, Yu JY, Ding B (2019a) Shapeable, underwater superelastic, and highly phosphorylated nanofibrous aerogels for large-capacity and high-throughput protein separation. ACS Appl Mater Interfaces 11(47):44874–44885

    Article  CAS  PubMed  Google Scholar 

  • Fu QX, Si Y, Duan C, Yan ZS, Liu LF, Yu JY, Ding B (2019b) Highly carboxylated, cellular structured, and underwater superelastic nanofibrous aerogels for efficient protein separation. Adv Funct Mater 29(13):1808234

    Article  Google Scholar 

  • Fu QX, Wang XQ, Si Y, Liu LF, Yu JY, Ding B (2016) Scalable fabrication of electrospun nanofibrous membranes functionalized with citric acid for high-performance protein adsorption. ACS Appl Mater Interfaces 8(18):11819–11829

    Article  CAS  PubMed  Google Scholar 

  • Ge MY, Shen Y, Chen WM, Peng YT, Pan ZY (2019) Adsorption of bovine hemoglobin by sulfonated polystyrene nanospheres. ChemistrySelect 4(10):2874–2880

    Article  CAS  Google Scholar 

  • Ghorpade VS, Yadav AV, Dias RJ, Mali KK (2018) Fabrication of citric acid crosslinked -cyclodextrin/hydroxyethylcellulose hydrogel films for controlled delivery of poorly soluble drugs. J Appl Polym Sci 135(27):4652

    Google Scholar 

  • Ghosh R (2002) Protein separation using membrane chromatography: opportunities and challenges. J Chromatogr A 952(1–2):13–27

    Article  CAS  PubMed  Google Scholar 

  • He XM, Zhu GT, Lu W, Yuan BF, Wang H, Feng YQ (2015) Nickel(II)-immobilized sulfhydryl cotton fiber for selective binding and rapid separation of histidine-tagged proteins. J Chromatogr A 1405:188–192

    Article  CAS  PubMed  Google Scholar 

  • Hu XD, Yang B, Hao M, Chen ZJ, Liu YB, Ramakrishna S, Wang XX, Yao JB (2023) Preparation of high elastic bacterial cellulose aerogel through thermochemical vapor deposition catalyzed by solid acid for oil-water separation. Carbohydr Polym 305:120538

    Article  CAS  PubMed  Google Scholar 

  • Huang JY, Zhao M, Hao Y, Wei QF (2022) Recent advances in functional bacterial cellulose for wearable physical sensing applications. Adv Mater Technol 7(1):2100617

    Article  CAS  Google Scholar 

  • Jain P, Sun L, Dai JH, Baker GL, Bruening ML (2007) High-capacity purification of his-tagged proteins by affinity membranes containing functionalized polymer brushes. Biomacromol 8(10):3102–3107

    Article  CAS  Google Scholar 

  • Janusz W, Skwarek E, Sternik D, Pikus S, Pawlak D, Parus JL, Mikolajczak R (2020) Synthesis of yttrium citrate from yttrium carbonate hydroxide and citric acid. Mater Chem Phys 250:123113

    Article  CAS  Google Scholar 

  • Jiang Y, Lu J, Guo L (2023) Fabrication of highly carboxylated thermoplastic nanofibrous membranes for efficient absorption and separation of protein. Colloid Surf A 665:131203

    Article  CAS  Google Scholar 

  • Kluszczynska K, Peczek L, Rozanski A, Czernek L, Duchler M (2022) U6/miR-211 expression ratio as a purity parameter for HEK293 cell-derived exosomes. Acta Biochim Pol 69(2):409–415

    CAS  PubMed  Google Scholar 

  • Leitch ME, Li CK, Ikkala O, Mauter MS, Lowry GV (2016) Bacterial nanocellulose aerogel membranes: novel high-porosity materials for membrane distillation. Environ Sci Technol Lett 3(3):85–91

    Article  CAS  Google Scholar 

  • Li C, Ding YW, Hu BC, Wu ZY, Gao HL, Liang HW, Chen JF, Yu SH (2020) Temperature-invariant superelastic and fatigue resistant carbon nanofiber aerogels. Adv Mater 32(2):1904331

    Article  CAS  Google Scholar 

  • Li GT, Li TT, Li YL, An LB, Li W, Zhang ZM (2017) Preparation of pH-controllable nanofibrous membrane functionalized with lysine for selective adsorption of protein. Colloid Surf A 531:173–181

    Article  CAS  Google Scholar 

  • Li Y, Wen YA, Wang LH, He JX, Al-Deyab SS, El-Newehy M, Yu JY, Ding B (2015) Simultaneous visual detection and removal of lead(II) ions with pyromellitic dianhydride-grafted cellulose nanofibrous membranes. J Mater Chem A 3(35):18180–18189

    Article  CAS  Google Scholar 

  • Lu JW, Jiang YG, Xiao R, Jacob KI, Tao L, Li SJ, Guo L (2022) Chemical vapor deposition based superelastic and superhydrophoboic thermoplastic polymeric nanofibrous aerogels for water purification. J Inorg Organomet Poly 32(8):2975–2985

    Article  CAS  Google Scholar 

  • Lu JW, Li Y, Song W, Losego MD, Monikandan R, Jacob KI, Xiao R (2020) Atomic layer deposition onto thermoplastic polymeric nanofibrous aerogel templates for tailored surface properties. ACS Nano 14(7):7999–8011

    Article  CAS  PubMed  Google Scholar 

  • Lu JW, Xu DD, Wei JK, Yan S, Xiao R (2017) Superoleophilic and flexible thermoplastic polymer nanofiber aerogels for removal of oils and organic solvents. ACS Appl Mater Interfaces 9(30):25533–25541

    Article  CAS  PubMed  Google Scholar 

  • Lv H, Wang XQ, Fu QX, Si Y, Yin X, Li XR, Sun G, Yu JY, Ding B (2017) A versatile method for fabricating ion-exchange hydrogel nanofibrous membranes with superb biomolecule adsorption and separation properties. J Colloid Interface Sci 506:442–451

    Article  CAS  PubMed  Google Scholar 

  • Ma JC, Wang XQ, Fu QX, Si Y, Yu JY, Ding B (2015) Highly carbonylated cellulose nanofibrous membranes utilizing maleic anhydride grafting for efficient lysozyme adsorption. ACS Appl Mater Interfaces 7(28):15658–15666

    Article  CAS  PubMed  Google Scholar 

  • Ogata M, Sakamoto M, Yamauchi N, Nakazawa M, Koizumi A, Anazawa R, Kurumada K, Hidari KIPJ, Kono H (2022) Optimization of the conditions for the immobilization of glycopolypeptides on hydrophobic silica particulates and simple purification of lectin using glycopolypeptide-immobilized particulates. Carbohydr Res 519:108624

    Article  CAS  PubMed  Google Scholar 

  • Orr V, Zhong LY, Moo-Young M, Chou CP (2013) Recent advances in bioprocessing application of membrane chromatography. Biotechnol Adv 31(4):450–465

    Article  CAS  PubMed  Google Scholar 

  • Przybycien TM, Pujar NS, Steele LM (2004) Alternative bioseparation operations: life beyond packed-bed chromatography. Curr Opin Biotechnol 15(5):469–478

    Article  CAS  PubMed  Google Scholar 

  • Qian LW, Yang MX, Chen HN, Xu Y, Zhang SF, Zhou QS, He B, Bai Y, Song WQ (2019) Preparation of a poly(ionic liquid)-functionalized cellulose aerogel and its application in protein enrichment and separation. Carbohydr Polym 218:154–162

    Article  CAS  PubMed  Google Scholar 

  • Qiao LZ, Liao YX, Wang XW, Wang SS, Du KF (2022) Double-emulsion templated macroporous cellulose microspheres as a high-performance chromatographic media for protein separation. Cellulose 29(13):7263–7276

    Article  CAS  Google Scholar 

  • Rajesh S, Crandall C, Schneiderman S, Menkhaus TJ (2018) Cellulose-graft-polyethyleneamidoamine anion-exchange nanofiber membranes for simultaneous protein adsorption and virus filtration. ACS Appl Nano Mater 1(7):3321–3330

    Article  CAS  Google Scholar 

  • Sharma PR, Chattopadhyay A, Sharma SK, Hsiao BS (2017) Efficient removal of UO22+ from water using carboxycellulose nanofibers prepared by the nitro-oxidation method. Ind Eng Chem Res 56(46):13885–13893

    Article  CAS  Google Scholar 

  • Sharma PR, Sharma SK, Antoine R, Hsiao BS (2019) Efficient removal of arsenic using zinc oxide nanocrystal-decorated regenerated microfibrillated cellulose scaffolds. ACS Sustain Chem Eng 7(6):6140–6151

    Article  CAS  Google Scholar 

  • Sharma PR, Sharma SK, Lindstrom T, Hsiao BS (2020) Nanocellulose-enabled membranes for water purification: perspectives. Adv Sustain Syst 4(5):1900114

    Article  CAS  Google Scholar 

  • Si Y, Fu QX, Wang XQ, Zhu J, Yu JY, Sun G, Ding B (2015) Superelastic and superhydrophobic nanofiber-assembled cellular aerogels for effective separation of oil/water emulsions. ACS Nano 9(4):3791–3799

    Article  CAS  PubMed  Google Scholar 

  • Si Y, Wang XQ, Li Y, Chen K, Wang JQ, Yu JY, Wang HJ, Ding B (2014) Optimized colorimetric sensor strip for mercury(II) assay using hierarchical nanostructured conjugated polymers. J Mater Chem A 2(3):645–652

    Article  CAS  Google Scholar 

  • Spinella S, Maiorana A, Qian Q, Dawson NJ, Hepworth V, McCallum SA, Ganesh M, Singer KD, Gross RA (2016) Concurrent cellulose hydrolysis and esterification to prepare a surface-modified cellulose nanocrystal decorated with carboxylic acid moieties. ACS Sustain Chem Eng 4(3):1538–1550

    Article  CAS  Google Scholar 

  • Wang FF, Zhang Y, Shi J, Sun L, Ullah A, Zhu CH, Kim IS (2023) Bioinspired and biodegradable functionalized graphene oxide/deacetylated cellulose acetate composite janus membranes for water evaporation-induced electricity generation. ACS Sustain Chem Eng 11(26):9792–9803

    Article  CAS  Google Scholar 

  • Wang P, Yin YK, Xu J, Chen SH, Wang H (2020) Facile synthesis of Cu2+-immobilized imprinted cotton for the selective adsorption of bovine hemoglobin. Cellulose 27(2):867–877

    Article  CAS  Google Scholar 

  • Wang XL, Fu QX, Wang XQ, Si Y, Yu JY, Wang XL, Ding B (2015) In situ cross-linked and highly carboxylated poly(vinyl alcohol) nanofibrous membranes for efficient adsorption of proteins. J Mater Chem B 3(36):7281–7290

    Article  CAS  PubMed  Google Scholar 

  • Yi SX, Dai FY, Ma Y, Yan TS, Si Y, Sun G (2017) Ultrafine silk-derived nanofibrous membranes exhibiting effective lysozyme adsorption. ACS Sustain Chem Eng 5(10):8777–8784

    Article  CAS  Google Scholar 

  • Yi SX, Dai FY, Wu YH, Zhao CY, Si Y, Sun G (2018) Scalable fabrication of sulfated silk fibroin nanofibrous membranes for efficient lipase adsorption and recovery. Int J Biol Macromol 111:738–745

    Article  CAS  PubMed  Google Scholar 

  • Yu LL, Sun Y (2013) Protein adsorption to poly(ethylenimine)-modified Sepharose FF: II. Effect of ionic strength. J Chromatogr A 1305:85–93

    Article  CAS  PubMed  Google Scholar 

  • Zhan CB, Li YX, Sharma PR, He HR, Sharma SK, Wang RF, Hsiao BS (2019) A study of TiO2 nanocrystal growth and environmental remediation capability of TiO2/CNC nanocomposites. RSC Adv 9(69):40565–40576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Zhang Y, Lu CH, Deng YL (2012) Aerogels from crosslinked cellulose nano/micro-fibrils and their fast shape recovery property in water. J Mater Chem 22(23):11642–11650

    Article  CAS  Google Scholar 

  • Zhang YD, Zhang LQ, Hu JN, Wang ZW, Meng DM, Li H, Zhou ZK, Yang R (2023) The structural characterization and color stabilization of the pigment protein-phycoerythrin glycosylated with oligochitosan. Food Hydrocolloid 136:108241

    Article  CAS  Google Scholar 

  • Zhao L, Wang H, Fu J, Wu X, Liang XY, Liu XY, Wu X, Cao LL, Xu ZY, Dong M (2022) Microfluidic-based exosome isolation and highly sensitive aptamer exosome membrane protein detection for lung cancer diagnosis. Biosens Bioelectron 214:114487

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Jiangsu University was acknowledged to provide characterization.

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Authors and Affiliations

  1. School of Materials Science and Engineering, Jiangsu University, Zhenjiang, 212013, China

    Jianwei Lu, Yangang Jiang, Zihao Wen, Zhengjin Luo, Yufei Qiao & Li Guo

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  1. Jianwei Lu
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  2. Yangang Jiang
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  3. Zihao Wen
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  4. Zhengjin Luo
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  5. Yufei Qiao
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  6. Li Guo
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Contributions

JL conceptualized the work, analyzed data, and wrote the manuscript; YJ, ZW, ZL and YQ prepared bacterial cellulose nanofibrous aerogels and carried out protein absorption experiments; LG provided resources and guidance. All authors reviewed the manuscript.

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Correspondence to Jianwei Lu or Li Guo.

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Lu, J., Jiang, Y., Wen, Z. et al. Bacterial cellulose nanofibrous aerogels grafted with citric acid for absorption and separation of protein. Cellulose 31, 349–361 (2024). https://doi.org/10.1007/s10570-023-05621-x

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