Membranes and filters are essential devices, both in the laboratory for separation of media, solvent recovery, organic solvent and water filtration purposes, and in industrial scale applications, such as the removal of industrial pollutants, e.g. heavy metal ions, from water.
Trang 1Carbohydrate Polymers 253 (2021) 117273
Available online 27 October 2020
( http://creativecommons.org/licenses/by-nc-nd/4.0/ ).
Fungal chitin-glucan nanopapers with heavy metal adsorption properties
for ultrafiltration of organic solvents and water
Neptun Yousefia, Mitchell Jonesa,b, Alexander Bismarcka,c,d, Andreas Mautnera,*
aInstitute of Materials Chemistry and Research, Polymer and Composite Engineering (PaCE) Group, Faculty of Chemistry, University of Vienna, W¨ahringer Straße 42,
1090 Vienna, Austria
bSchool of Engineering, RMIT University, Bundoora East Campus, PO Box 71, Bundoora 3083, VIC, Australia
cDepartment of Mechanical Engineering, Faculty of Engineering and the Built Environment, University of Johannesburg, South Africa
dDepartment of Chemical Engineering, Imperial College London, South Kensington Campus, London, SW7 2AZ, UK
A R T I C L E I N F O
Keywords:
Fungal chitin
Organic solvent filtration
Water treatment
Copper
Cellulose
A B S T R A C T Membranes and filters are essential devices, both in the laboratory for separation of media, solvent recovery, organic solvent and water filtration purposes, and in industrial scale applications, such as the removal of in-dustrial pollutants, e.g heavy metal ions, from water Due to their solvent stability, biologically sourced and renewable membrane or filter materials, such as cellulose or chitin, provide a low-cost, sustainable alternative to synthetic materials for organic solvent filtration and water treatment Here, we investigated the potential of
fungal chitin nanopapers derived from A bisporus (common white-button mushrooms) as ultrafiltration
mem-branes for organic solvents and aqueous solutions and hybrid chitin-cellulose microfibril papers as high per-meance adsorptive filters Fungal chitin constitutes a renewable, easily isolated, and abundant alternative to crustacean chitin It can be fashioned into solvent stable nanopapers with pore sizes of 10− 12 nm, as determined
by molecular weight cut-off and rejection of gold nanoparticles, that exhibit high organic solvent permeance, making them a valuable material for organic solvent filtration applications Addition of cellulose fibres to pro-duce chitin-cellulose hybrid papers extended membrane functionality to water treatment applications, with considerable static and dynamic copper ion adsorption capacities and high permeances that outperformed other biologically derived membranes, while being simpler to produce, naturally porous, and not requiring cross-linking The simple nanopaper production process coupled with the remarkable filtration properties of the papers for both organic solvent filtration and water treatment applications designates them an environmentally benign alternative to traditional membrane and filter materials
1 Introduction
Filtration membranes and adsorbent filters play a vital role across a
range of filtration applications, from ultrafiltration (UF), nanofiltration
(NF), and solvent recovery to the removal of heavy metals from water,
making it safe to drink (Mautner et al., 2014; Ng, Mohammad, Leo, &
Hilal, 2013) Traditional synthetic membranes are frequently used in
academic or commercial organic solvent or aqueous UF and NF,
rejecting pollutants in the nm scale, or see service in removing harmful
industrial effluents, e.g heavy metal ions, from waste and fresh water
sources in industrialised regions (Marchetti, Jimenez Solomon, Szekely,
& Livingston, 2014; Mohammad et al., 2015; Vandezande, Gevers, &
Vankelecom, 2008) However, despite their efficiency in these
processes, synthetic membranes, most frequently produced from poly-mers, such as polysulfone, polyethylene, polytetrafluoroethylene, or polypropylene, commonly experience problems related to their hydro-phobicity, resulting in biofouling (Baker & Dudley, 1998; Mansouri, Harrisson, & Chen, 2010) Additionally, synthetic membranes manu-factured for applications such as organic solvent filtration typically require complex polymeric structures exhibiting solvent stability Consequently, these membranes are usually expensive and often suffer from low permeance (Marchetti et al., 2014)
Tackling the disadvantages associated with these synthetic materials, biologically derived membranes and filters based on cellulose, chitosan,
or chitin have experienced increased academic interest due to their low costs, and utilisation of abundant, sustainable resources (Shaheen, Eissa,
* Corresponding author
E-mail address: andreas.mautner@univie.ac.at (A Mautner)
Contents lists available at ScienceDirect Carbohydrate Polymers journal homepage: www.elsevier.com/locate/carbpol
https://doi.org/10.1016/j.carbpol.2020.117273
Received 17 February 2020; Received in revised form 14 October 2020; Accepted 15 October 2020
Trang 2Ghanem, El-Din, & Al Anany, 2013) In particular nano-sized fibres of
these biopolymers constitute a promising approach to size-exclusion
filtration in both the NF and UF range (Gustafsson et al., 2019;
Janesch et al., 2020; Liu, Zhu, & Mathew, 2019; Manukyan, Padova, &
Mihranyan, 2019; Mautner, 2020; Metreveli et al., 2014), coupled with
excellent solvent stability for organic solvent filtration in the case of
nanocellulose (Mautner et al., 2014) Furthermore, chitin, and its
deacetylated derivative chitosan, have received significant attention due
to their high affinity toward metal ions, resulting from their many free
hydroxyl and acetamide groups (chitin) or amine groups (chitosan),
making these renewable sorbents particularly effective for water
treat-ment (Dragan & Dinu, 2020; Ghaee, Shariaty-Niassar, Barzin, &
Mat-suura, 2010; Khalil, Elhusseiny, El-dissouky, & Ibrahim, 2020; Preethi,
Prabhu, & Meenakshi, 2017; Rostamian, Firouzzare, & Irandoust, 2019;
Shaheen et al., 2013; Vold, Vårum, Guibal, & Smidsrød, 2003) Chitin
can be readily sourced from the environment, where it occurs as an
abundant linear macromolecule in the exoskeleton of arthropods (
Pau-lino, Santos, & Nozaki, 2008; Rostamian et al., 2019) and fungal cell
walls, in which it occurs as native nano-sized material, well suited to
nanopaper preparation with no requirement for high-energy mechanical
disintegration (Nawawi, Lee, Kontturi, Bismarck, & Mautner, 2020;
Zhang, Zeng, & Cheng, 2016) These natural materials are ecologically
beneficial compared with traditional membrane manufacturing
pro-cesses, in particular for organic solvent filtration (Honda, Miyata, &
Iwahori, 2002), while also offering adsorption capacities competitive
with or even higher than traditional (synthetic) sorbent materials
Chitin and chitosan are, by definition, distinguished from each other
only by solubility differences in various media (Pillai, Paul, & Sharma,
2009) Solvent stable filtration membranes are subsequently
preferen-tially manufactured using chitin rather than chitosan The use of chitin
as opposed to chitosan also accelerates nanopaper production since
time-consuming deacetylation procedures are not required Membranes
from animal-derived chitin are usually prepared by film casting
methods, since simple papermaking utilising chitin fibrils extracted
from this source results in papers with poor mechanical properties
(Nawawi, Jones et al., 2019) due to the lack of glucan covalently bound
to chitin macromolecules, which would otherwise act as a matrix and
facilitate film formation properties (King & Watling, 1997; Nawawi, Lee,
Kontturi, Murphy, & Bismarck, 2019, 2020) Crustacean chitin is also
dependent on seasonal and regional variation and requires harsh acid
and alkaline treatments for purification and demineralisation, as well as
high-energy defibrillation in case that nanofibrils are desired (Di Mario,
Rapana, Tomati, & Galli, 2008; Hassainia, Satha, & Boufi, 2018) In
contrast, chitin derived from fungal cell walls constitutes a native
ar-chitecture of nanofibrils that are easily isolated using low-energy
me-chanical disintegration (Nawawi, Jones et al., 2019) In this natural
composite, glucan acts as a flexible matrix with chitin fibrils responsible
for strength This enables the preparation of strong and stiff nanopapers
from fungal chitin nanofibrils (FChNF) FChNF nanopapers should
subsequently be ideal candidates for membrane and filtration
applica-tions in both organic and aqueous environments due to their native
nanoscale structure, lacking in crustacean chitin, and their higher
sol-vent stability compared to chitosan
Agaricus bisporus (white button mushroom) is an edible mushroom
that is not only nutritious but also a functional food due to its free radical
scavenging and antioxidant activities (Guan, Fan, & Yan, 2013; Lin
et al., 2017; Lindequist, Niedermeyer, & Jülich, 2005) It primarily
comprises a chitin, glucan, and protein-based cell wall, non-structural
polysaccharides, and soluble proteins (Hammond, 1979) with a
distinct odour that is ascribed to flavour volatiles such as 8-carbon atom
compounds (Noble, Dobrovin-Pennington, Hobbs, Pederby, & Rodger,
2009), e.g 1-octen-3-ol (Dong, Zhang, Lu, Sun, & Xu, 2012) Additional
secondary compounds also have the potential to promote human health,
with cytostatic, antimutagenic, and genoprotective activity reported for
A bisporus, resulting from the presence of compounds such as lectins and
the enzyme tyrosinase (Lindequist et al., 2005; Shi, James, Benzie, &
Buswell, 2004; Yu, Fernig, Smith, Milton, & Rhodes, 1993) Large-scale
production of A bisporus also makes it abundant and relatively stable in
composition and properties and subsequently an ideal model system for investigation of fungal chitin-glucan nanofibrils and products
We utilised native nano-sized chitin-glucan fibrils and investigated
the potential of FChNF nanopapers derived from A bisporus for
ultra-filtration of organic solvents, e.g ethanol and tetrahydrofuran, and water with additional investigation into the removal of heavy metal ions, such as copper, from aqueous solution also performed A mild alkaline treatment was utilised for extraction of FChNF Nanopapers of various grammages were then prepared from this FChNF extract The physico-chemical properties of these nanopapers were characterised in addition to the permeance of both organic solvents and water and the nanopaper pore size was characterised by the molecular weight cut-off Hybrid papers comprising varying quantities of cellulose sludge fibres and FChNF were also trialled in order to increase the porosity and thus permeance of the filters
2 Materials and methods
2.1 Materials
Common white button mushrooms were purchased from a local su-permarket (origin: B Fungi Kft., Ocsa, Hungary) Shrimp shell chitin flakes (Sigma-Aldrich, C9213, practical grade) were used for reference purposes NaOH (Sigma), NH3 solution (25 %, analytical grade, Sigma- Aldrich), ethylenediaminetetraacetic acid disodium salt dihydrate (EDTA) (0.1 M, analytical grade, Roth), murexide (Fluka), NH4Cl (Roth), and Cu(NO3)2⋅6 H2O (Honeywell Fluka) were used for the extraction of FChNF and complexometric titration of copper ions For carbohydrate analysis, Sugar Recovery Standards (SRS) were prepared from D-(+)-xylose (Merck 108689), D-(+)-glucosamine hydrochloride (Sigma-Aldrich G4875), L-(+)-rhamnose (Merck R3875), L -(+)-arabi-nose (Merck 101492), D-(+)-mannose (Merck 4440), D-(+)-galactose (Merck 3455), and D-(+)-glucose (VWR 10117 HV) Deionised water, ethanol (Sigma-Aldrich), and tetrahydrofuran (THF, 98 %, Fisher Chemicals) were used for permeance and solvent stability tests Acetone (Sigma-Aldrich) was used to test solvent stability Polyethylene glycol (PEG) standards with molecular weights (Mw) of 2, 20, and 50 kDa (Polymer Laboratories) and polystyrene (PS) standards with 2.5, 20, and
50 kDa (Fluka) were used to determine the molecular weight cut-off (MWCO) Cellulose sludge microfibres, with a cellulose and hemicellu-lose content of 95 % and 4.75 %, respectively, a charge content of approx 0.04 mmol g− 1, and diameters of 5–20μm (Mautner et al.,
2015) were kindly provided by Processum AB (Domsj¨o, Sweden) 10 nm gold nanoparticles (OD 1, stabilised suspension in citrate puffer) were purchased from Sigma-Aldrich All chemicals were used as received Deionised water was used for all experiments except for adsorption ex-periments for which Type 1 Milli-Q® ultrapure water was used
2.2 FChNF extraction and nanopaper preparation
The extraction of fungal chitin nanofibrils (FChNF) and preparation
of FChNF nanopapers followed the protocol described earlier by Nawawi, Lee et al (2019, 2020) Briefly, A bisporus mushrooms were
soaked and washed in water to remove dirt and other impurities and blended (JB 3060, Braun) The slurry (1 % w/v) thus prepared was then heated to 85◦C for 30 min, cooled, and centrifuged at 7000 rpm for
15 min The supernatant was discarded, and the precipitate resuspended
in aqueous NaOH solution (1 mol L− 1) at 65◦C for 3 h The suspension was cooled and neutralised (pH 7) by repeated centrifugation and re-dispersion of the precipitate in water, yielding FChNF extract Nanopapers were produced from FChNF extract by suspending pre-determined amounts of FChNF extract in water followed by me-chanical blending (JB 3060, Braun) These suspensions were then vac-uum filtered, and the filter cakes cold pressed for 5 min between blotting
Trang 3Carbohydrate Polymers 253 (2021) 117273
papers to remove excess water Two blotting paper lined metal plates
and a 5 kg mass were then utilised to press this sandwich, which was
oven dried for 3 h at 120◦C Nanopaper grammages ranged from 10 to
110 g m− 2
2.3 FChNF + cellulose hybrid filter preparation
Hybrid filters comprising FChNF and cellulose microfibres were
produced as has been described earlier by Janesch et al (2020) Briefly,
50 g m− 2 (gsm) nanopapers in weight ratios of 80:20, 60:40, 50:50,
40:60, and 20:80 were prepared using a 0.1 wt.% dispersion of cellulose
microfibres (0.08 %) formed by mixing 1.0 g of cellulose sludge
microfibres (water content 50 %) with 270 mL of water This dispersion
was blended to achieve a homogenous suspension before the FChNF
extract was added, the desired consistency set, and blending continued
for an additional 2 min The FChNF + cellulose hybrid papers were then
pressed and oven dried as previously described
2.4 Analysis of the molecular structure of the FChNF extracts
The molecular structure of dried extracts was assessed by Attenuated
Total Reflection-Fourier-transform-infrared (ATR-FT-IR) spectroscopy
across the full accessible range from 4000 to 400 cm− 1 (Carry 630 FT-IR,
Agilent) with a single reflection diamond ATR-module and KBr optics
(beam splitter) Three spectra from different regions of each sample
were recorded to verify homogeneity Carbon, hydrogen, nitrogen, and
oxygen elemental analysis was performed with 2 mg samples in
dupli-cate using an elemental analyser (EA 1108 CHNS-O, Carlo Erba)
High performance anion exchange chromatography (HPAEC) was
performed to analyse the sugar composition of the carbohydrates as
described earlier by Janesch et al (2020) Briefly, freeze-dried samples
and SRS were dispersed in conc H2SO4, subsequently diluted with water
and placed in an autoclave The acid hydrolysate was analysed using
HPAEC on a Dionex ICS3000 chromatograph equipped with a CarboPac
PA20 column
2.5 Morphology and physical properties of the nanopapers
Nanopaper surface morphology was examined by Scanning Electron
Microscopy (SEM) using a Zeiss Supra 55 V P Scanning Electron
Mi-croscope Nanopapers were initially coated (Leica EM SCD 050) with
10 nm of gold before being imaged at an accelerating voltage of 2 kV
Fibril diameters were analysed for 10 replicate measurements using the
Fiji distribution of ImageJ (version 1.51a)
The nanopaper skeletal density ρskeletal was determined by helium
gas displacement pycnometry (Micromeritics AccuPyc II 1340) with a
chamber volume of 1 cm3
The nanopaper grammage G (Eq 1), mass m, thickness d, envelope
density ρenvelope (Eq 2), and porosity Φ (Eq 3) of the nanopapers were
determined following the procedure established earlier by Janesch et al
(2020)
G (g m− 2) = m (g)
ρenvelope(kg m− 3) =G (kg m− 2)
Φ (%) =
(
1 − ρenvelope(kg m− 3)
ρskeletal(kg m− 3)
)
2.6 Surface properties of the nanopapers
The surface charge as expressed by the ζ-potential of the nanopapers
was analysed with an electrokinetic analyser (Anton Paar SurPASS,
Graz, Austria) as a function of pH in an adjustable gap cell (100μm)
1 mM KCl electrolyte solution was pumped through the cell at pressures steadily increased to 300 mbar and the pH controlled by titrating 0.05 mol L− 1 KOH and 0.05 mol L− 1 HCl, respectively, into the elec-trolyte solution The ζ-potential was determined from the streaming current
2.7 Water permeance, pore size, and solvent stability of nanopapers
The permeance of the nanopapers was determined in analogy to the procedure described earlier by Mautner et al (2014) by passing water, ethanol, and tetrahydrofuran, respectively, through the samples in a dead-end cell with an effective filtration diameter of 43 mm (Sterlitech HP4750) Nanopaper discs (49 mm diameter) were placed on a sintered stainless-steel support structure and water or organic solvents, respec-tively, passed through them using a nitrogen head pressure of 5 bar and
1 bar for hybrid papers, respectively The permeance was in turn calculated from the volume of liquid passed through the nanopaper per unit time, unit area, and unit pressure (L h− 1m− 2MPa− 1)
The molecular weight cut-off (MWCO) (See Toh, Loh, Li, Bismarck, & Livingston, 2007) of the nanopapers was determined using three PEG standards (2, 20, 50 kDa) dissolved in ultrapure water in equal con-centrations, with a total concentration of 1 g L− 1 Three PS standards (2.5, 20, 50 kDa) were also used, dissolved in tetrahydrofuran with a total concentration of 1.5 g L− 1 Permeance tests were initially per-formed as described above and the permeate fractions analysed by gel permeation chromatography for PS in THF (Waters 515 HPLC pump, Waters 2410 RI detector) and PEG in aqueous solution (Viscotek GPCmax VE2001, VE3580 RI detector) Similarly, 20 mL of a suspension (diluted with deionized water in a ratio of 1:10) of 10 nm gold nano-particles was passed through CG nanopaper and the reduction in the intensity of the red colour analysed by UV–vis spectroscopy (Agilent 8453) with relative concentrations calculated from the absorbance at a wavelength of 520 nm (Janesch et al., 2020)
The solvent stability of the nanopapers was tested in acetone, deionised water, ethanol, and tetrahydrofuran Nanopaper specimens,
~16 mg in mass, were placed in a small glass flask and submerged in
50 mL of each respective solvent The flask was then sealed with par-afilm and left for 5 weeks, after which time the solvent was removed and the nanopapers weighed again Solvent stability was assessed as weight loss (WL) based on the mass difference (Δm) between the initial mass (m0) and the final mass after 5 weeks soaking in the respective solvent (m5w)
WL(wt%) = Δm (g)
m0(g)∙100 =
m0(g) − m5w(g)
2.8 Adsorption properties of FChNF and papers
Static adsorption of Cu2+ions on FChNF was analysed with Cu(NO3)2 solutions as earlier described by Janesch et al (2020) Suspensions of the FChNF extracts (50 mg aliquots) were allowed various periods of interaction (1, 3, 20, 30, and 60 min) with several concentrations of
Cu2+ions (0.2, 0.5, 1.0, 5.0, and 10.0 mM) before being filtered The concentration of copper in the filtrate (c) was determined by com-plexometric titration with EDTA Briefly, 5 mg of NH4Cl and 12 drops (~0.6 mL) of NH3 (25 %) were added to the test samples to attain a pH of
10 Titrations were completed with 5 mM (molar concentration) EDTA (cEDTA) and 5 mg of murexide used as an indicator of the transition point, a colour change of yellow-orange to pink Concentrations of the filtrate were then related to those of a reference sample that had not been exposed to FChNF This relation enabled calculation of the quantity
of Cu2+ions adsorbed on FChNF (q) c was plotted with respect to q and the Freundlich (1906) and Langmuir (1918) equations (Eqs 5 and 6) applied to model static adsorption isotherms for each contact time
N Yousefi et al
Trang 4q = qmc
with qm being the maximum adsorption amount per unit mass of
adsorbent in order to form a complete monolayer coverage on the
sur-face and KL the Langmuir constant
KF is the adsorption coefficient and n the Freundlich parameter The
Gibbs Free Energy of adsorption (ΔG0) was calculated according to Eq
7
Dynamic adsorption experiments for hybrid papers were performed
using discs (diameter =49 mm) in a dead-end cell (Sterlitech HP4750)
A total of 2 L of a 2 mM copper solution was deposited onto the disc and
a nitrogen head pressure of 1 bar applied An aliquot of each permeate
fraction (Vfraction) was diluted with 50 mL ultrapure water and the
concentration of each permeate fraction analysed by complexometric
titration as described above The final concentration of Cu2+ions was
then calculated using Eq 8, based on the titration (VEDTA) and aliquot
one EDTA molecule The mass of adsorbed Cu2+ ions was in turn
calculated based on the atomic weight (M) of copper (63.546 g mol− 1,
Eq 9) and the adsorption as a function of mass per unit area (qA, mg
m− 2) for the effective filtration area of 1460 mm2 (Eq 10) The
adsorption capacity (q, mg g− 1) of Cu2+was finally calculated from qA
and G (Eq 11)
c(Cu2+) (mmol L-1) =cEDTA(mmol L-1)∙VEDTA(L)
qA(mg m-2) =m (mg)
q (mg g-1) =qA(mg m-2)
3 Results and discussion
3.1 Chemical and elemental analysis of FChNF
Elemental analysis (Table 1) of FChNF extracted from whole
A bisporus mushrooms (yield 12 g kg− 1) resulted in a nitrogen content of
3.8 wt.%, which is significantly lower than that of commercial chitin
derived from crustaceans (6.5 wt.%) but slightly higher than previously
published data for A bisporus mushrooms (3.0–3.4 wt.% (Janesch et al.,
2020; Nawawi, Lee et al., 2019)) The lower N content of FChNF
compared to crustacean chitin indicates the presence of a second phase
within the nanofibres, glucan Slightly higher N contents of about
4.5 wt.% were determined for FChNF extracted from cap and stalk
constituent alone, prepared from different batches of mushrooms These
minor variations in elemental composition were likely due to the
influence of inherent biological variation during growth as commonly found in natural products (Nawawi, Jones et al., 2019)
The N content in fungal biomass corresponds with the secondary amide group of chitin, located in the fungal cell wall, with a lower N content indicating a smaller chitin fraction in the sample (Jones et al.,
2019; Nawawi, Lee et al., 2019) The lower N content of FChNF compared to crustacean chitin was primarily the result of the significant glucan fraction present, which is covalently bonded to the chitin and was not removed during the mild alkaline extraction treatment (Nawawi, Jones et al., 2019) However, the A bisporus mushrooms did
have significantly higher N contents than is typical for mycelial biomass, making them a better source of fungal chitin than mycelium (0.3–1.9 wt
%) (Jones et al., 2019) From the N content the ratio between chitin and glucan could be calculated to be 59:41, which is in good agreement with previous studies (Liu et al., 2013; Nawawi, Lee et al., 2019) This was also confirmed by sugar analysis, which gave a glucosamine to glucose ratio of 57:43
The presence of chitin in FChNF extracted from A bisporus
mush-room was also evident in ATR-FT-IR spectra (Fig 1); the -NH stretching band was present at 3276 cm− 1 and an − OH band at 3434 cm− 1 in addition to − CH bands at 2911 cm− 1 and 2841 cm− 1 as well as a C–O–C band at 1029 cm− 1 provided evidence of a carbohydrate backbone attributable to both the glucan and chitin polymer structure The chitin structure itself was verified by an amide I band associated with C––O stretching at 1628 cm− 1 in addition to amide II and III bands resulting from -NH deformation at 1560 cm− 1 and 1315 cm− 1, respec-tively (Janesch et al., 2020; Nawawi, Lee et al., 2019, 2020) The amide III band confirmed the presence of a secondary amide, indicating that the extracted FChNF primarily contained chitin as opposed to chitosan, which has a primary amine group resulting from the deacetylation of chitin in harsh alkaline conditions (Sikorski, Hori, & Wada, 2009) Compared to shrimp shell chitin, FChNF exhibited higher relative absorbance of the carbohydrate backbone in relation to the amide peaks supporting the presence of glucan No significant differences were visible in the spectra of the FChNF extracts based on the mushroom constituents analysed (cap, stalk, or whole mushroom) Subsequently, mushroom components were not separated and the FChNF gels pro-duced from whole mushrooms
3.2 Physical properties of the FChNF and FChNF-cellulose hybrid papers
Nanopapers prepared from FChNF had similar envelope densities (940− 1140 kg m− 3) irrespective of grammage and were similar in density (1090− 1210 kg m− 3) to commercial crustacean chitin (Mushi,
Table 1
C, H, N, O, and S elemental composition (wt.% of total mass) of alkaline treated
FChNF derived from whole A bisporus mushrooms compared to commercial
chitin
Sample Elemental composition (wt.% of total mass)
Commercial chitin * 44.64 7.29 6.49 39.61 <0.02
*Data from (Nawawi, Lee et al., 2019)
Fig 1 ATR-FTIR spectra for FChNF extracted from whole A bisporus
mush-rooms using mild alkaline treatment and a commercial chitin reference Peaks associated with -NH stretching and amides I-III are marked with red bounding boxes (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article)
Trang 5Carbohydrate Polymers 253 (2021) 117273
Butchosa, Salajkova, Zhou, & Berglund, 2014) (Table 2) However, a
trend suggesting higher densities at higher grammages was observed,
which has already been reported for cellulose nanopapers (Bloch, Engin,
& Sampson, 2019; Gülsoy, Hürfikir, & Turgut, 2016) Accordingly,
po-rosities remained at a fairly constant ~25 % at grammages > 40 g m− 2
and ~35 % at grammages ≤ 40 g m− 2, respectively As such, FChNF
nanopapers exhibited similar porosity to cellulose nanopapers, which
typically have porosities of ~20 % (Henriksson, Berglund, Isaksson,
Lindstrom, & Nishino, 2008) to above ~30 % in the case of filtration
applications (Mautner et al., 2014, 2015) The decrease in porosity with
increasing grammage was a direct result of all nanopapers being pressed
at the same pressure and the fibrils of higher grammage papers
subse-quently being more densely packed than in lower grammage
nanopapers
FChNF are nanoscale fibrils with diameters as low as 11 nm and 90 %
of fibrils smaller than 20.5 nm in diameter The average fibril diameter
was 17 nm with a recorded maximum value of 26 nm (Fig 2a (right))
These results confirmed that no further mechanical or chemical
treat-ment was necessary to obtain nano-sized fibrils directly from common
mushrooms, as opposed to crustacean chitin or plant-derived
nano-cellulose for which energy intensive defibrillation steps are necessary to
prepare nanofibrils (Nawawi, Jones et al., 2019) The nanoscale
struc-ture of the nanopapers was clearly visible in SEM images (Fig 2a (left))
Hybridisation (Mautner, Mayer, Hervy, Lee, & Bismarck, 2018), i.e
combination of fibres at various size scales, was used to increase the
porosity of FChNF nanopapers as reported before for nanocellulose
(Mautner et al., 2019) However, while the combination of chitin-glucan
nanofibrils with cellulose microfibrils facilitates porosity control in
hybrid papers it also results in synergies based on the interaction
be-tween cellulose and chitin-glucan complex in the composite material, as
previously demonstrated for chitin derived from animal sources (Duan,
Freyburger, Kunz, & Zollfrank, 2018; Robles, Salaberria, Herrera,
Fer-nandes, & Labidi, 2016; Shamshina et al., 2018; Shen, Shamshina,
Berton, Gurau, & Rogers, 2016; Takegawa, Murakami, Kaneko, &
Kadokawa, 2010; Tang, Chang, & Zhang, 2011) Porosity could be
significantly increased through the addition of 20− 80 wt.% cellulose
microfibrils to form hybrid papers and even cellulose quantities as low
as 20 wt.% doubled the porosity of the 50 g m− 2 nanopapers (48 % for
hybrid papers containing 20 wt.% cellulose compared to 25 % for
FChNF nanopapers), with porosities as high as 74 % achieved with a
cellulose fraction of 80 wt.% in the hybrid papers (Table 2) These
greatly increased porosities were clearly visible in SEM images, with the
nanoscale FChNF network partially covering the micro-sized cellulose
fibres and the surface roughness and porosity visibly increasing as the
cellulose fraction in the hybrid papers was increased from 0 to 50 and
finally 80 wt.% (Fig 2b and c) Increases in porosity were accompanied
by a reduction in envelope densities (Table 2) in the hybrid papers as the void volume increased and packing efficiency was reduced
The ζ-potential of FChNF nanopapers as a function of pH showed no significant difference in isoelectric points (IEP) across various gram-mages (IEP = 3.1) This behaviour was due to the N-acetyl groups that are protonated at low pH and in good agreement with other studies utilising fungi-derived FChNF nanopapers (IEP = 2.8) (Nawawi et al.,
2020) It was also similar to the IEP of pure chitin, which is typically
~3.5 (Wysokowski et al., 2014) Hybrid papers consisting of FChNF and cellulose microfibres had higher IEPs (~3.5− 3.8) than pure FChNF nanopapers, exhibiting similar values to cellulose filter papers (IEP = 3.7) (Fig 3) This was again likely the result of carboxyl groups from uronic acids forming during the pulping process, which affect the pKa value on which the IEP is based (Chai, Zhu, & Li, 2001) Increasing quantities of cellulose fibres also affected the ζ-potential, resulting in increasingly negative ζ-potential plateau values with increasing cellu-lose content Papers containing 20 and 50 wt.% cellucellu-lose had plateau values of − 16 and − 20 mV, respectively, while a cellulose content of
80 wt.% resulted in a ζ-potential plateau of − 28 mV Interestingly, pure FChNF nanopapers plateaued at − 21 mV, a more negative value than papers incorporating 20 and 50 wt.% cellulose This was likely the result
of charge compensation of negatively charged surface groups of cellu-lose microfibrils with the amino groups (degree of deacetylation ≈ 13 % (Janesch et al., 2020)) in the FChNF component The ζ-potential of hybrids containing 80 wt.% cellulose fibres on the other hand was lower than that of pure FChNF papers, which was attributed to the very low FChNF content and hence N-acetyl concentration of this nanopaper compared to the pure FChNF nanopaper, resulting in a lower ζ-potential Negative ζ-potential is anticipated to facilitate adsorption of positively charged heavy metal ions
3.3 Membrane properties of the FChNF nanopapers and hybrid papers
Characterisation of both organic solvent and water filtration mem-branes is commonly based on the pure liquid permeance and the rejec-tion of pollutants, i.e the average pore size of membranes Higher porosity at lower grammages, in addition to lower grammage itself, affected the water permeance of the FChNF nanopapers, which was exponentially higher at lower grammages (Fig 4) The maximum water permeance of 53 L h− 1m− 2MPa− 1 at a grammage of 10 g m− 2 was more than halved at 20 g m− 2 and stabilised at values of 1.5 to 3.7 L
h− 1m− 2MPa− 1 for grammages of 30 g m− 2 and higher The permeances
of FChNF nanopapers were thus higher than those of chitosan films (~1 L h− 1m− 2MPa− 1) (Marques, Pereira, Sotto, & Arsuaga, 2019) or papers produced from cellulose nanocrystals (~1 L h− 1m− 2MPa− 1 at
80 g m− 2), but lower than papers made from cellulose nanofibres (Mautner et al., 2014) or bacterial cellulose (5 L h− 1m− 2MPa− 1 at 80 g
m− 2) (Mautner et al., 2015) The higher permeance of bacterial cellulose and cellulose nanofibre nanopapers in this instance stems from their larger diameter fibrils, which average 30− 50 nm in diameter compared
to 13.5 nm for cellulose nanocrystals and 17 nm for FChNF nanopapers This confirms that, in general, the pore size and hence the permeance of nanopapers is determined by the fibril diameter in the network that it constitutes (Mautner et al., 2014)
Higher permeances compared to pure water permeance for FChNF nanopapers were observed during filtration of organic solvents Ethanol had a permeance of 7.7 L h− 1m− 2MPa− 1 at 60 g m− 2, over 3 times that
of water, and THF exceeded the water permeance of the nanopapers by over 9 times with a permeance of 19.2 L h− 1m− 2MPa− 1 at 60 g m− 2 The significantly higher permeance of THF was attributable to THF being the least hydrophobic liquid of the three, with the permeance of organic solvents through hydrophilic nanopapers being dependent on the hydrophilicity of the liquid The network pore size determining fibril diameters also affected the permeance for organic solvents as shown through comparison with TEMPO-oxidised nanocellulose papers
con-sisting of nanofibrils < 10 nm that had a THF permeance of < 2 L
Table 2
Composition, grammage G, thickness d, envelope density ρe, and porosity Φ of
(a) FChNF nanopapers of various grammages and (b) hybrid papers comprising
varying ratios of FChNF and cellulose fibres
Membrane composition
(wt.%) G (g m− 2 ) d (μm) ρe (g cm − 3 ) Φ (%)
FChNF Cellulose
100 0
30 29.6 ± 1.6 0.96 ± 0.05 35 ± 2
40 42.4 ± 2.4 0.94 ± 0.06 36 ± 2
50 48.8 ± 1.7 1.11 ± 0.03 25 ± 1
60 51.8 ± 2.6 1.14 ± 0.05 22 ± 1
70 57.8 ± 2.7 1.14 ± 0.05 23 ± 1
80 75.1 ± 3.8 1.13 ± 0.05 23 ± 1
90 92.4 ± 4.4 1.09 ± 0.05 26 ± 1
100 98.0 ± 4.4 1.12 ± 0.04 24 ± 1
80 20 50 79.6 ± 7.3 0.77 ± 0.09 48 ± 6
60 40 50 83.4 ± 2.5 0.68 ± 0.03 54 ± 2
50 50 50 103.2 ± 3.7 0.59 ± 0.04 60 ± 4
40 60 50 111.5 ± 5.6 0.53 ± 0.05 65 ± 6
20 80 50 147.1 ± 8.8 0.39 ± 0.06 74 ± 11
N Yousefi et al
Trang 6h− 1m− 2MPa− 1 at 60 g m− 2 (Mautner et al., 2014)
Nanopaper permeance could generally be increased through the
introduction of cellulose microfibres to produce hybrid papers,
comprising a hierarchical architecture of micro-sized cellulose fibrils
and nanoscale FChNF, which resulted in larger pores and increased
porosity Water permeance was significantly increased with the
intro-duction of 50 wt.% cellulose fibres (5.1 L h− 1m− 2MPa− 1 compared to
3.2 L h− 1m− 2MPa− 1 for FChNF nanopapers at 50 g m− 2) and increased
exponentially to a water permeance of 394 L h− 1m− 2MPa− 1 for a
cel-lulose loading of 80 wt.%, an increase by a factor of > 100
The average pore size of FChNF nanopapers was determined using
PEG of various molecular weights dissolved in water (Fig 5) (See Toh
et al., 2007) The nanopapers retained 40 % of 2 kDa PEG but completely rejected 20 and 50 kDa PEG, with an interpolated molecular weight cut-off (MWCO) of ~18 kDa, which corresponds to an average pore size of ~10 nm based on the hydrodynamic diameter of PEG in solution (Armstrong, Wenby, Meiselman, & Fisher, 2004) Similar re-sults were achieved using PS in THF with a 30 % retention of PS having a molecular weight of 2.5 kDa, a 75 % retention of 20 kDa PS, and com-plete rejection of 50 kDa PS This indicated a MWCO of ~45 kDa for PS
in THF corresponding to a hydrodynamic diameter of 12 nm and hence pore size (Uliyanchenko, Schoenmakers, & Van der Wal, 2011) Results for the MWCO were further verified by filtration of 10 nm gold nano-particles that were almost completely (99.7 %) rejected by FChNF nanopapers as confirmed by UV–vis spectroscopy For water-based ap-plications this pore size qualifies the FChNF nanopapers as tight ultra-filtration membranes, rather than nanoultra-filtration membranes, with defects in the paper likely affecting filtration performance This is typical in paper membranes prepared from nano-fibrous materials that form random networks (Mautner et al., 2015) In terms of organic sol-vent filtration this result is remarkable Solsol-vent stability tests resulted in
mass losses of < 0.02 wt.% for acetone, ethanol, and THF indicating
excellent solvent stability also in organic solvents, a characteristic not often achieved by conventional filtration membranes made from syn-thetic polymers (Darvishmanesh et al., 2011; Gao, Wu, Tao, Qu, & Li,
2018; Van der Bruggen, Geens, & Vandecasteele, 2002) A pore size of
12 nm is hence already valued, which when coupled with the high permeance characteristics of the FChNF membranes for organic solvents exhibiting low hydrophilicity makes FChNF nanopapers a potent alter-native to traditional membranes in organic solvent filtration
3.4 Adsorption of copper ions on FChNF and papers
Heavy metal ions, such as copper (Cu2+), readily adsorb on chitin (Gonz´alez-D´avila & Millero, 1990) making it a useful natural material
Fig 2 1k magnification SEM micrographs with 20k magnification insets detailing (a) the surface morphology (left) and fibril diameter size distribution (right) of
FChNF papers, and the surface morphology of hybrid papers comprising (b) 50 wt.% FChNF and 50 wt.% cellulose and (c) 20 wt.% FChNF and 80 wt.% cellulose
Fig 3 ζ-potential measured in 1 mM KCl as a function of pH for hybrid papers
comprising FChNF and increasing quantities of cellulose microfibres (FChNF
only and hybrid papers containing 20, 50, and 80 % cellulose), respectively,
compared to cellulose filter paper
Trang 7Carbohydrate Polymers 253 (2021) 117273
for water treatment Static adsorption tests were performed to determine
the effectiveness of FChNF in removing copper ions from water, with
Langmuir and Freundlich isotherms used to model adsorption behaviour
(Fig 6, Table 3) The Langmuir isotherm proved a more accurate
sorp-tion model than the Freundlich isotherm with R2 values of 0.983− 0.997
compared to 0.70− 0.84, respectively The suitability of this monolayer
sorption model for heavy metal adsorption on FChNF has also been
supported by several other studies (Cao, Pan, Shi, & Yu, 2018; Liu et al.,
2013; Tang et al., 2011), with the Langmuir constants calculated similar
in value to those of literature in which chitin was utilised as a natural
absorbent The maximum adsorption capacity (qm) of the FChNF ranged
from 20.1–43.4 mg g− 1, with a maximum value reached after 20 min
exposure
The dynamic adsorption capacities of hybrid papers, comprising
FChNF and cellulose microfibres, were assessed by filtration tests
Hybrid papers comprising 20 wt.% FChNF and 80 wt.% cellulose
exhibited considerable dynamic adsorption properties, with an
adsorption per unit area of 805 mg m− 2 and overall dynamic adsorption capacity of 81 mg g− 1 Adsorption levelled off at a filtration volume of
400 mL and the nanopaper reached saturation at a filtration volume of
700 mL (Fig 7), with these volumes resulting from the low membrane
papers comprising cellulose microfibres and FChNF at various ratios The error (< 2%) is too small to be visible in the graphs
Fig 5 Molecular weight cut-off (MWCO) of FChNF nanopapers for (a) PEG in
aqueous solution and (b) PS in THF MWCO relates to the molecular weight of a
solute which is 90 % retained by a membrane
FChNF after 3 min
Table 3
Langmuir and Freundlich isotherm parameters for copper ion (Cu2+) adsorption
on FChNF over a period of up to 60 min
Sample
K L (L
mg − 1 ) q(mg m
g − 1 )
Δ G 0 (kJ mol − 1 ) R
(mg
g − 1 )
n F R 2
Cu 1min 0.16 20.1 − 12.5 0.983 7.9 0.16 0.79
Cu 3min 0.11 24.1 − 11.7 0.997 8.9 0.17 0.82
Cu 20min 0.02 43.4 − 7.7 0.986 5.4 0.34 0.84
Cu 30min 0.05 35.1 − 9.6 0.989 7.1 0.27 0.70
Cu 60min 0.21 33.1 − 13.3 0.988 8.0 0.26 0.68
N Yousefi et al
Trang 8area (0.0014 m2) used in these tests and scaling with membrane area
The overall dynamic adsorption capacities of the FChNF-cellulose
hybrid papers outperformed other renewable heavy metal adsorption
membranes coated with an active layer of cellulose nanocrystals, which
had adsorption capacities of 33 mg g− 1 (Karim, Claudpierre, Grahn,
Oksman, & Mathew, 2016) but were lower than TEMPO-oxidised
cel-lulose membranes (300 mg g− 1) (Karim, Hakalahti, Tammelin, &
Mathew, 2017) It should, however, be noted that the TEMPO-oxidised
membranes only utilised a very shallow surface cellulose modification
resulting in their high adsorption capacity per unit mass of the thin top
layer adsorption agent The FChNF-cellulose hybrids also performed
remarkably better than chitosan (films), which are also used for water
treatment due to their high affinity for heavy metal ions, such as copper
(Cu2+) (Babel & Kurniawan, 2003; Crini & Badot, 2008; Guibal, 2004;
Kumar, 2000; Varma, Deshpande, & Kennedy, 2004) Examples of
comparable chitosan membranes include membranes produced by
so-lution casting of chitosan from acetic acid followed by crosslinking with
glutaraldehyde to enhance their stability (47 mg g− 1) (Ghaee et al.,
2010), formaldehyde crosslinked modified chitosan–thioglyceraldehyde
Schiff’s base (76 mg g− 1) (Monier, 2012), and crosslinked chitosan
beads (46− 81 mg g− 1) (Ngah, Endud, & Mayanar, 2002), although
chitosan membranes produced via thermally induced phase separation
did exhibit a higher dynamic adsorption capacity (163 mg g− 1) (Qin
et al., 2017) This demonstrated the suitability of FChNF hybrid papers
for water treatment applications without resorting to the use of chitosan
and thus constitutes a simpler, cheaper manufacturing process Both the
FChNF nanopapers and FChNF-cellulose hybrid papers produced in this
study also have several advantages over other natural and traditional
membranes, such as simple production, not requiring cross-linking
(Marques, Chagas, Fonseca, & Pereira, 2016), or modification (
Saheb-jamee, Soltanieh, Mousavi, & Heydarinasab, 2019), and being
inher-ently nanofibrillated, facilitating preparation of porous networks with
nm pores
4 Conclusion
Fungal chitin nanofibres (FChNF) were extracted from common
white button mushrooms (A bisporus) as an alternative to crustacean
chitin, using a mild alkaline treatment and low-energy mechanical
blending Pure FChNF nanopapers and FChNF-cellulose hybrid paper
filters were produced and their membrane and adsorption properties
assessed Nanopaper water permeance had an inverse correlation with
grammage but could be exponentially increased through incorporation
of cellulose to form hybrid filters Higher permeances in FChNF
nano-papers were achieved for organic solvents, such as ethanol and
tetra-hydrofuran, with the FChNF filters exhibiting excellent solvent stability
FChNF nanopapers had molecular weight cut-offs associated with a pore size of 10− 12 nm, as also confirmed by rejection of 10 nm diameter gold nanoparticles This characterises them as tight ultrafiltration mem-branes, which when coupled with their high organic solvent permeance and stability makes them a valuable alternative to traditional mem-branes, particularly for organic solvent filtration FChNF/cellulose hybrid papers exhibited significant dynamic Cu2+adsorption capacities, outperforming membranes produced by solution casting and crosslinked chitosan beads, while being simpler to produce, naturally porous, and not requiring crosslinking The remarkable filtration properties of these low-cost and sustainable filters across both organic solvent filtration and water treatment applications, coupled with their simple manufacturing process enables their use as renewable alternatives to synthetic filters, which could help to reduce the ecological impact associated with traditional membranes and their manufacturing processes
CRediT authorship contribution statement Neptun Yousefi: Conceptualization, Methodology, Investigation,
Validation, Writing - review & editing Mitchell Jones:
Conceptuali-zation, VisualiConceptuali-zation, Writing - original draft, Funding acquisition
Alexander Bismarck: Conceptualization, Methodology, Validation,
Writing - review & editing, Supervision, Project administration, Funding
acquisition Andreas Mautner: Conceptualization, Methodology,
Investigation, Visualization, Validation, Writing - review & editing, Supervision
Acknowledgements
The authors acknowledge Johannes Theiner (Mikroanalytisches Laboratorium, Faculty of Chemistry, University of Vienna) for elemental analysis as well as Beatrice Giaier for support with adsorption studies
We also thank Prof Eero Kontturi (Aalto University) for carbohydrate analysis University of Vienna is acknowledged for funding NY and AM
References
Armstrong, J K., Wenby, R B., Meiselman, H J., & Fisher, T C (2004) The hydrodynamic radii of macromolecules and their effect on red blood cell
aggregation Biophysical Journal, 87(6), 4259–4270
Babel, S., & Kurniawan, T A (2003) Low-cost adsorbents for heavy metals uptake from
contaminated water: A review Journal of Hazardous Materials, 97(1-3), 219–243
Baker, J S., & Dudley, L Y (1998) Biofouling in membrane systems — A review
Desalination, 118(1), 81–89
Bloch, J.-F., Engin, M., & Sampson, W W (2019) Grammage dependence of paper
thickness Appita Journal, 72(1), 30–40
Cao, Y.-L., Pan, Z.-H., Shi, Q.-X., & Yu, J.-Y (2018) Modification of chitin with high
adsorption capacity for methylene blue removal International Journal of Biological
Macromolecules, 114, 392–399
Chai, X., Zhu, J., & Li, J (2001) A simple and rapid method to determine hexeneuronic
acid groups in chemical pulps Journal of Pulp and Paper Science, 27(5), 165–170
Crini, G., & Badot, P.-M (2008) Application of chitosan, a natural aminopolysaccharide, for dye removal from aqueous solutions by adsorption processes using batch studies:
A review of recent literature Progress in Polymer Science, 33(4), 399–447
Darvishmanesh, S., Tasselli, F., Jansen, J C., Tocci, E., Bazzarelli, F., Bernardo, P., et al (2011) Preparation of solvent stable polyphenylsulfone hollow fiber nanofiltration
membranes Journal of Membrane Science, 384(1), 89–96
Di Mario, F., Rapana, P., Tomati, U., & Galli, E (2008) Chitin and chitosan from
Basidiomycetes International Journal of Biological Macromolecules, 43(1), 8–12
Dong, J., Zhang, M., Lu, L., Sun, L., & Xu, M (2012) Nitric oxide fumigation stimulates flavonoid and phenolic accumulation and enhances antioxidant activity of
mushroom Food Chemistry, 135(3), 1220–1225
Dragan, E S., & Dinu, M V (2020) Advances in porous chitosan-based composite
hydrogels: Synthesis and applications Reactive & Functional Polymers, 146, Article
104372
Duan, Y., Freyburger, A., Kunz, W., & Zollfrank, C (2018) Cellulose and chitin
composite materials from an ionic liquid and a green co-solvent Carbohydrate
Polymers, 192, 159–165
Freundlich, H M F (1906) Über die adsorption in L¨osungen The Journal of Physical
Chemistry, 57, 385–471
Gao, T., Wu, H., Tao, L., Qu, L., & Li, C (2018) Enhanced stability and separation
efficiency of graphene oxide membranes in organic solvent nanofiltration Journal of
Materials Chemistry A, 6(40), 19563–19569
filtration volume (V, mL) for FChNF and hybrid papers comprising 80 wt.%
cellulose and 20 wt.% FChNF
Trang 9Carbohydrate Polymers 253 (2021) 117273
Ghaee, A., Shariaty-Niassar, M., Barzin, J., & Matsuura, T (2010) Effects of chitosan
membrane morphology on copper ion adsorption Chemical Engineering Journal, 165
(1), 46–55
Gonz´alez-D´avila, M., & Millero, F J (1990) The adsorption of copper to chitin in
seawater Geochimica et Cosmochimica Acta, 54(3), 761–768
Guan, W., Fan, X., & Yan, R (2013) Effect of combination of ultraviolet light and
hydrogen peroxide on inactivation of Escherichia coli O157:H7, native microbial
loads, and quality of button mushrooms Food Control, 34(2), 554–559
Guibal, E (2004) Interactions of metal ions with chitosan-based sorbents: A review
Separation and Purification Technology, 38(1), 43–74
Gülsoy, S., Hürfikir, Z., & Turgut, B (2016) Effects of decreasing grammage on the
handsheet properties of unbeaten and beaten kraft pulps Türkiye Ormancılık Dergisi,
17(1), 56–60
Gustafsson, O., Manukyan, L., Gustafsson, S., Tummala, G K., Zaman, S., Begum, A.,
et al (2019) Scalable and sustainable total pathogen removal filter paper for point-
of-Use drinking water purification in Bangladesh ACS Sustainable Chemistry &
Engineering, 7(17), 14373–14383
Hammond, J B W (1979) Changes in composition of harvested mushrooms (Agaricus
bisporus) Phytochemistry, 18(3), 415–418
Hassainia, A., Satha, H., & Boufi, S (2018) Chitin from Agaricus bisporus: Extraction
and characterization International Journal of Biological Macromolecules, 117(1),
1334–1342
Henriksson, M., Berglund, L A., Isaksson, P., Lindstrom, T., & Nishino, T (2008)
Cellulose nanopaper structures of high toughness Biomacromolecules, 9(6),
1579–1585
Honda, S., Miyata, N., & Iwahori, K (2002) Recovery of biomass cellulose from waste
sewage sludge Journal of Material Cycles and Waste Management, 4(1), 46–50
Janesch, J., Jones, M., Bacher, M., Kontturi, E., Bismarck, A., & Mautner, A (2020)
Mushroom-derived chitosan-glucan nanopaper filters for the treatment of water
Reactive & Functional Polymers, 146, Article 104428
Jones, M., Weiland, K., Kujundzic, M., Theiner, J., Kahlig, H., Kontturi, E., et al (2019)
Waste-derived low-cost mycelium nanopapers with tunable mechanical and surface
properties Biomacromolecules, 20(9), 3513–3523
Karim, Z., Claudpierre, S., Grahn, M., Oksman, K., & Mathew, A P (2016) Nanocellulose
based functional membranes for water cleaning: Tailoring of mechanical properties,
porosity and metal ion capture Journal of Membrane Science, 514, 418–428
Karim, Z., Hakalahti, M., Tammelin, T., & Mathew, A P (2017) In situ TEMPO surface
functionalization of nanocellulose membranes for enhanced adsorption of metal ions
from aqueous medium RSC Advances, 7(9), 5232–5241
Khalil, T E., Elhusseiny, A F., El-dissouky, A., & Ibrahim, N M (2020) Functionalized
chitosan nanocomposites for removal of toxic Cr (VI) from aqueous solution Reactive
& Functional Polymers, 146, Article 104407
King, A., & Watling, R (1997) Paper made from bracket fungi Mycologist, 11(2), 52–54
Kumar, M N R (2000) A review of chitin and chitosan applications Reactive &
Functional Polymers, 46(1), 1–27
Langmuir, I (1918) The adsorption of gases on plane surfaces of glass, mica and
platinum Journal of the American Chemical Society, 40, 1361–1403
Lin, Q., Lu, Y., Zhang, J., Liu, W., Guan, W., & Wang, Z (2017) Effects of high CO2 in-
package treatment on flavor, quality and antioxidant activity of button mushroom
(Agaricus bisporus) during postharvest storage Postharvest Biology and Technology,
123, 112–118
Lindequist, U., Niedermeyer, T H J., & Jülich, W.-D (2005) The pharmacological
potential of mushrooms Evidence-based Complementary and Alternative Medicine, 2,
Article 906016
Liu, D., Zhu, Y., Li, Z., Tian, D., Chen, L., & Chen, P (2013) Chitin nanofibrils for rapid
and efficient removal of metal ions from water system Carbohydrate Polymers, 98(1),
483–489
Liu, P., Zhu, C., & Mathew, A P (2019) Mechanically robust high flux graphene oxide -
nanocellulose membranes for dye removal from water Journal of Hazardous
Materials, 371, 484–493
Mansouri, J., Harrisson, S., & Chen, V (2010) Strategies for controlling biofouling in
membrane filtration systems: Challenges and opportunities Journal of Materials
Chemistry, 20(22), 4567–4586
Manukyan, L., Padova, J., & Mihranyan, A (2019) Virus removal filtration of chemically
defined Chinese Hamster ovary cells medium with nanocellulose-based size
exclusion filter Biologicals, 59, 62–67
Marchetti, P., Jimenez Solomon, M F., Szekely, G., & Livingston, A G (2014) Molecular
separation with organic solvent nanofiltration: A critical review Chemical Reviews,
114(21), 10735–10806
Marques, J., Chagas, J., Fonseca, J., & Pereira, M (2016) Comparing homogeneous and
heterogeneous routes for ionic crosslinking of chitosan membranes Reactive &
Functional Polymers, 103, 156–161
Marques, J S., Pereira, M R., Sotto, A., & Arsuaga, J M (2019) Removal of aqueous
copper(II) by using crosslinked chitosan films Reactive & Functional Polymers, 134,
31–39
Mautner, A (2020) Nanocellulose water treatment membranes and filters: A review
Polymer International, 69(9), 741–751
Mautner, A., Kwaw, Y., Weiland, K., Mvubu, M., Botha, A., John, M J., et al (2019)
Natural fibre-nanocellulose composite filters for the removal of heavy metal ions
from water Industrial Crops and Products, 133, 325–332
Mautner, A., Lee, K.-Y., Lahtinen, P., Hakalahti, M., Tammelin, T., Li, K., et al (2014)
Nanopapers for organic solvent nanofiltration Chemical Communications, 50(43),
5778–5781
Mautner, A., Lee, K.-Y., Tammelin, T., Mathew, A P., Nedoma, A J., Li, K., et al (2015)
Cellulose nanopapers as tight aqueous ultra-filtration membranes Reactive &
Functional Polymers, 86, 209–214
Mautner, A., Mayer, F., Hervy, M., Lee, K.-Y., & Bismarck, A (2018) Better together:
Synergy in nanocellulose blends Philosophical Transactions Mathematical Physical and
Engineering Sciences, 376(2112), Article 20170043
Metreveli, G., Wågberg, L., Emmoth, E., Bel´ak, S., Strømme, M., & Mihranyan, A (2014)
A size-exclusion nanocellulose filter paper for virus removal Advanced Healthcare
Materials, 3(10), 1546–1550
Mohammad, A W., Teow, Y H., Ang, W L., Chung, Y T., Oatley-Radcliffe, D L., & Hilal, N (2015) Nanofiltration membranes review: Recent advances and future
prospects Desalination, 356, 226–254
Monier, M (2012) Adsorption of Hg2+, Cu2+ and Zn2+ ions from aqueous solution using formaldehyde cross-linked modified chitosan–thioglyceraldehyde Schiff’s
base International Journal of Biological Macromolecules, 50(3), 773–781
Mushi, N E., Butchosa, N., Salajkova, M., Zhou, Q., & Berglund, L A (2014) Nanostructured membranes based on native chitin nanofibers prepared by mild
process Carbohydrate Polymers, 112, 255–263
Nawawi, W M F W., Lee, K.-Y., Kontturi, E., Bismarck, A., & Mautner, A (2020)
Surface properties of chitin-glucan nanopapers from Agaricus bisporus International
Journal of Biological Macromolecules, 148, 677–687
Nawawi, W., Jones, M., Murphy, R J., Lee, K.-Y., Kontturi, E., & Bismarck, A (2019)
Nanomaterials derived from fungal sources - is it the new hype? Biomacromolecules,
21(1), 30–55
Nawawi, W M F W., Lee, K.-Y., Kontturi, E., Murphy, R J., & Bismarck, A (2019) Chitin nanopaper from mushroom extract: Natural composite of nanofibers and
glucan from a single biobased source ACS Sustainable Chemistry & Engineering, 7(7),
6492–6496
Ng, L Y., Mohammad, A W., Leo, C P., & Hilal, N (2013) Polymeric membranes incorporated with metal/metal oxide nanoparticles: A comprehensive review
Desalination, 308, 15–33
Ngah, W W., Endud, C., & Mayanar, R (2002) Removal of copper (II) ions from aqueous
solution onto chitosan and cross-linked chitosan beads Reactive & Functional
Polymers, 50(2), 181–190
Noble, R., Dobrovin-Pennington, A., Hobbs, P J., Pederby, J., & Rodger, A (2009) Volatile C8 compounds and pseudomonads influence primordium formation of
Agaricus bisporus Mycologia, 101(5), 583–591
Paulino, A T., Santos, L B., & Nozaki, J (2008) Removal of Pb2+, Cu2+, and Fe3+ from battery manufacture wastewater by chitosan produced from silkworm
chrysalides as a low-cost adsorbent Reactive & Functional Polymers, 68(2), 634–642
Pillai, C K S., Paul, W., & Sharma, C P (2009) Chitin and chitosan polymers:
Chemistry, solubility and fiber formation Progress in Polymer Science, 34(7),
641–678
Preethi, J., Prabhu, S M., & Meenakshi, S (2017) Effective adsorption of hexavalent chromium using biopolymer assisted oxyhydroxide materials from aqueous solution
Reactive & Functional Polymers, 117, 16–24
Qin, W., Li, J., Tu, J., Yang, H., Chen, Q., & Liu, H (2017) Fabrication of porous chitosan membranes composed of nanofibers by low temperature thermally induced phase
separation, and their adsorption behavior for Cu2+ Carbohydrate Polymers, 178,
338–346
Robles, E., Salaberria, A M., Herrera, R., Fernandes, S C M., & Labidi, J (2016) Self- bonded composite films based on cellulose nanofibers and chitin nanocrystals as
antifungal materials Carbohydrate Polymers, 144, 41–49
Rostamian, R., Firouzzare, M., & Irandoust, M (2019) Preparation and neutralization of forcespun chitosan nanofibers from shrimp shell waste and study on its uranium
adsorption in aqueous media Reactive & Functional Polymers, 143, Article 104335
Sahebjamee, N., Soltanieh, M., Mousavi, S M., & Heydarinasab, A (2019) Removal of Cu2+, Cd2+ and Ni2+ ions from aqueous solution using a novel chitosan/polyvinyl
alcohol adsorptive membrane Carbohydrate Polymers, 210, 264–273
See Toh, Y H., Loh, X X., Li, K., Bismarck, A., & Livingston, A G (2007) In search of a standard method for the characterisation of organic solvent nanofiltration
membranes Journal of Membrane Science, 291(1), 120–125
Shaheen, S M., Eissa, F I., Ghanem, K M., El-Din, H M G., & Al Anany, F S (2013) Heavy metals removal from aqueous solutions and wastewaters by using various
byproducts Journal of Environmental Management, 128, 514–521
Shamshina, J L., Zavgorodnya, O., Choudhary, H., Frye, B., Newbury, N., & Rogers, R D (2018) In search of stronger/cheaper chitin nanofibers through electrospinning of
chitin–cellulose composites using an ionic liquid platform ACS Sustainable Chemistry
& Engineering, 6(11), 14713–14722
Shen, X., Shamshina, J L., Berton, P., Gurau, G., & Rogers, R D (2016) Hydrogels based
on cellulose and chitin: Fabrication, properties, and applications Green Chemistry, 18
(1), 53–75
Shi, Y.-l., James, A E., Benzie, I F F., & Buswell, J A (2004) Genoprotective activity of
edible and medicinal mushroom components International Journal of Medicinal
Mushrooms, 6(1), 1–14
Sikorski, P., Hori, R., & Wada, M (2009) Revisit of α-Chitin crystal structure using high
resolution X-ray diffraction data Biomacromolecules, 10(5), 1100–1105
Takegawa, A., Murakami, M.-a., Kaneko, Y., & Kadokawa, J.-i (2010) Preparation of
chitin/cellulose composite gels and films with ionic liquids Carbohydrate Polymers,
79(1), 85–90
Tang, H., Chang, C., & Zhang, L (2011) Efficient adsorption of Hg2+ ions on chitin/ cellulose composite membranes prepared via environmentally friendly pathway
Chemical Engineering Journal, 173(3), 689–697
Uliyanchenko, E., Schoenmakers, P J., & Van der Wal, S (2011) Fast and efficient size- based separations of polymers using ultra-high-pressure liquid chromatography
Journal of Chromatography A, 1218(11), 1509–1518
Van der Bruggen, B., Geens, J., & Vandecasteele, C (2002) Influence of organic solvents
on the performance of polymeric nanofiltration membranes Separation Science and
Technology, 37(4), 783–797
N Yousefi et al
Trang 10Vandezande, P., Gevers, L E M., & Vankelecom, I F J (2008) Solvent resistant
nanofiltration: Separating on a molecular level Chemical Society Reviews, 37(2),
365–405
Varma, A., Deshpande, S., & Kennedy, J (2004) Metal complexation by chitosan and its
derivatives: A review Carbohydrate Polymers, 55(1), 77–93
Vold, I M., Vårum, K M., Guibal, E., & Smidsrød, O (2003) Binding of ions to
chitosan—Selectivity studies Carbohydrate Polymers, 54(4), 471–477
Wysokowski, M., Klapiszewski, Ł., Moszy´nski, D., Bartczak, P., Szatkowski, T.,
Majchrzak, I., et al (2014) Modification of chitin with kraft lignin and development
of new biosorbents for removal of cadmium (II) and nickel (II) ions Marine Drugs, 12
(4), 2245–2268
Yu, L., Fernig, D G., Smith, J A., Milton, J D., & Rhodes, J M (1993) Reversible inhibition of proliferation of epithelial cell lines by agaricus bisporus (Edible
mushroom) lectin Cancer Research, 53, 4627–4632
Zhang, L., Zeng, Y., & Cheng, Z (2016) Removal of heavy metal ions using chitosan and
modified chitosan: A review Journal of Molecular Liquids, 214, 175–191