Nano-tubular cellulose for bioprocess technology development.

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Nano-Tubular Cellulose for Bioprocess Technology Development Athanasios A. Koutinas1*, Vasilios Sypsas1, Panagiotis Kandylis1, Andreas Michelis1, Argyro Bekatorou1, Yiannis Kourkoutas2, Christos Kordulis3,4, Alexis Lycourghiotis3, Ibrahim M. Banat5, Poonam Nigam5, Roger Marchant5, Myrsini Giannouli6, Panagiotis Yianoulis6 1 Food Biotechnology Group, Department of Chemistry, University of Patras, Patras, Greece, 2 Department of Molecular Biology, Democritus University of Thrace, Alexandroupolis, Greece, 3 Group of Catalysis and Interfacial Chemistry for Environmental Applications, University of Patras, Patras, Greece, 4 Institute of Chemical Engineering and High Temperature Chemical Processes (FORTH/ICE-HT), Patras, Greece, 5 School of Biomedical Sciences, University of Ulster, Coleraine, United Kingdom, 6 Department of Physics, University of Patras, Patras, Greece Abstract Delignified cellulosic material has shown a significant promotional effect on the alcoholic fermentation as yeast immobilization support. However, its potential for further biotechnological development is unexploited. This study reports the characterization of this tubular/porous cellulosic material, which was done by SEM, porosimetry and X-ray powder diffractometry. The results showed that the structure of nano-tubular cellulose (NC) justifies its suitability for use in ‘‘cold pasteurization’’ processes and its promoting activity in bioprocessing (fermentation). The last was explained by a glucose pump theory. Also, it was demonstrated that crystallization of viscous invert sugar solutions during freeze drying could not be otherwise achieved unless NC was present. This effect as well as the feasibility of extremely low temperature fermentation are due to reduction of the activation energy, and have facilitated the development of technologies such as wine fermentations at home scale (in a domestic refrigerator). Moreover, NC may lead to new perspectives in research such as the development of new composites, templates for cylindrical nano-particles, etc. Citation: Koutinas AA, Sypsas V, Kandylis P, Michelis A, Bekatorou A, et al. (2012) Nano-Tubular Cellulose for Bioprocess Technology Development. PLoS ONE 7(4): e34350. doi:10.1371/journal.pone.0034350 Editor: Vipul Bansal, RMIT University, Australia Received October 21, 2011; Accepted February 27, 2012; Published April 9, 2012 Copyright: ß 2012 Koutinas et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The authors have no support or funding to report. Competing Interests: The authors have declared that no competing interests exist. * E-mail: Introduction Research on bioprocess technology development has been extensive during the last decades; however most of these technologies have not been used at industrial level. The main problems associated with these technologies are related to productivity, ease of industrial application and production cost. However there are still opportunities to use abundant, low cost materials with specific chemical or nano-mechanical properties to create multiple new, effective bioprocessing systems. One of the major problems of food and drug production is the use of the relatively costly pasteurization processes. In addition to high operational cost, pasteurization reduces the nutritional quality of food products. However due to its importance, pasteurization is extensively used despite these disadvantages. Only in some food bioprocesses like wine production, membranes [1] are used to remove e.g. Leuconostoc oenos cells but they have a high cost and are not easy to handle at industrial level. Alternatively, if a nano-tubular solid of food grade purity, could be used to remove microbial cells through cell entrapment and immobilization at ambient and low temperatures, it could have wide applications in the food and pharmaceutical industries, such as the cold pasteurization of liquid foods and the cold sterilization of liquids that are used in drug production plants, respectively. Porous materials like c-alumina pellets [2] and mineral kissiris [3] have been used for cell entrapment and immobilization; however their composition (that liberates aluminium in the processed media) limits their applications. Especially their use in food and drug production is not recommended. On the other hand delignified cellulosic material is of food grade purity, abundant in nature and therefore of low cost. This material has been successfully used as support for cell immobilization [4]. The produced biocatalyst was used for extremely low temperature fermentations in order to improve the quality of the products [5], and it was found able to promote the alcoholic fermentation of molasses [6]. Nanotechnology is one of the most growing areas of research the last decades. Especially the subarea of nano-cellulosic materials has attracted considerably high-level attention from researchers. The applications of this technology are numerous and in many fields. For example cellulosic nano-fibrils coated with SnO2 have been used for the production of membranes [7], while nanoporous cellulose combined with carbon nano-tubes have been used in batteries and supercapacitors [8]. Following that trend the main goal of the present work was to use nano-tubular cellulose (NC) for the development of bioprocesses related to food industries. More specifically the work addresses the characterization of the tubular structure of NC and its suitability, due to that structure, for (i) ‘‘cold pasteurization’’ processes, (ii) promotion of alcoholic fermentation, (iii) extremely low temperature fermentations, and (iv) home-scale (domestic refrigerator) bioprocesses. Finally the perspectives for NC PLoS ONE | 1 April 2012 | Volume 7 | Issue 4 | e34350 Nano-Tubular Cellulose Figure 1. Characterization of nano-tubular cellulose (NC). (a) SEM micrographs of NC produced by delignification of sawdust with NaOH (scale bar in 1, 2, 5, 6 corresponds to 20 mm, while in 3 to 50 mm and in 4 to 100 mm). (b) NC average pore diameter and cumulative surface area of the pores. (c) Spectra from X-ray diffractometry of blank sample and NC sample. (d) Crystallinity and crystallite size of NC calculated using spectra from Figure 2C. doi:10.1371/journal.pone.0034350.g001 applications in nanobiotechnology are discussed, taking into account the results of the present study. Results and Discussion Nanostructure and microstructure of tubular cellulose In the context of limited availability of complex materials for advanced bioprocessing, this investigation initially examines (i) the characterization of the structure of the NC material, (ii) the crystallinity of NC, and (iii) the degree of its crystallinity. Figure 1A shows the tubular structure in the remaining mass of cellulose after removal of lignin, while Figure 1B illustrates that the tubes have nano-scale dimensions. The cumulative surface area of the tubes is in the range of 0.8–0.89 m2 g21 as indicated by porosimetry analysis. This surface is relatively small compared with other PLoS ONE | 2 April 2012 | Volume 7 | Issue 4 | e34350 Nano-Tubular Cellulose porous materials such as c-alumina [9]. However, using a natural organic tubular biopolymer is attractive from the point of view that it is safer for bioprocess applications. The relatively small surface can be attributed to the fact that the lignin content in sawdust is about 16% and therefore its removal leads to limited tubing in the remaining mass of cellulose. However, this tubing is enough to encourage application for bioprocess development. Furthermore, single tubes (Fig. 1A, panel 3) and small groups of 3–4 tubes (Fig. 1A, panel 4) are observed. The tubes are horizontal (Fig. 1A, panel 2) and vertical (Fig. 1A, panel 1) and contain holes of varying diameters covering a relatively small area of the tubes (Fig. 1A, panel 6). Tubes with big differences of diameter are shown in the SEM photo of Figure 1A, panel 1. Likewise, tubes forming normal patterns such as a normal square are shown in Figure 1A, panel 5. However, Figure 1A, panel 1, 1A, panel 2 and 1A, panel 6 show tubes of small and bigger diameters. In the SEM micrographs it is shown that the bigger tubes are in micro-scale dimension and the small ones in nano-scale. Therefore, there is a mixture of micro and nano-tubing. The cumulative surface area and average pore diameter of the nano-tubes was measured by porosimetry. Figure 1D illustrates that NC has 65% degree of crystallinity indicating that the treatment with sodium hydroxide applied for delignification did not destroy its crystal structure. The size of the crystallites is 3 nm, which is big enough to contain a part of the tubes. Therefore, NC provides the possibility of cell entrapment and immobilization. These three different potential properties of NC make this nano-material suitable for different bioprocesses development as described above. Furthermore, this natural structure facilitates various new perspectives in research, which are discussed in this paper and which point to new nano-structured materials development. NC was produced by delignification of softwood sawdust and the observed microstructures reflect the architecture of the tracheids in the wood. The use of other starting materials would produce slightly different end products. In any case it is necessary to increase the nano-tubing and microtubing of cellulose. Pure microbial cellulose containing higher percentages of lignin could be examined, that would lead to more extended tubing after lignin removal. Cold pasteurization of liquid foods NC can be used to remove microorganisms from liquid foods or liquids used in the pharmaceutical industries at ambient and low temperatures. The aim is to develop a novel technology for cold pasteurization of drinking water, fruit juices, milk, wine, beer and other beverages, which could also be applied in pharmaceutical processing liquids. To test this possibility, NC was selected as a suitable new material due to its nano-tubular structure, ideal for the entrapment and immobilization of cells [4]. Water contaminated with bacteria and yeasts was passed continuously through the nano-tubular NC filter and the filtrate was analyzed for viable cells. The experiments were carried out at ambient temperature. There was an obvious difference in turbidity among the contaminated influent and the effluent water. Figure 2A shows that the microbiological load removal was 100%. The operational stability at this level of microbiological load removal remained constant for two days and then dropped. It was restored to 100% after regeneration of the NC filter achieved by washing it with hot water. The regeneration was successfully repeated every two days for more than one month, keeping the microbial removal at 100%. After the success of this experiment, cold pasteurization of the contaminated flow was carried out at 3–5uC since food processing is preferred at low temperatures to maintain the nutritional value and quality of the food. However, the removal of cells was greatly reduced and the effluent water was turbid. This unsuccessful result Figure 2. Nano-tubular cellulose (NC) in food, environmental and health care applications. (a) Removal of bacteria and yeasts from water (22–26uC). (b) SEM micrograph of L. casei flocculation in NC that was sampled from the bioreactor, which was pumped at low temperature (5uC) with its liquid culture for cold pasteurization (scale bar corresponds to 10 mm). doi:10.1371/journal.pone.0034350.g002 was attributed to the crystallization of sodium chloride added to the water to maintain the osmotic balance of cells. The crystals seemed to block the NC tubes preventing cell entrapment. Additionally, cell flocculation caused by low temperature stress [10], could also block the tubes. Figure 2B illustrates the formation of microbial flocks and proves that the reduction in microbial removal can be attributed to cell flocculation. Although low temperature cold pasteurization of the model system (contaminated water) failed, the experimental work involving a real food, i.e. orange juice, was attempted. Cold pasteurization of orange juice should be performed at low temperatures to preserve the quality characteristics, and it could be presumed successful since components in the juice (like ascorbic acid) are essential for the synthesis of substances like carnitine that reduce the stress of cells [11]. Indeed, the low temperature cold pasteurization of orange juice resulted in 100% microbial load removal, as demonstrated by plate counting of influent and effluent samples (data not shown). Nano-tubular cellulose as promoted of the alcoholic fermentation Enhancement of the alcoholic fermentation of molasses by delignified cellulosic material has been exhibited [6]. This observation motivated further research to examine the physicochemical structure of delignified cellulosic material and correlate it with its promotional effect on the rate of alcoholic fermentation. The characterization showed that cellulose has nano-scale tubular PLoS ONE | 3 April 2012 | Volume 7 | Issue 4 | e34350 Nano-Tubular Cellulose pores. This nano-tubular material (NC) was used as yeast immobilisation support to examine the activation energy Ea of the alcoholic fermentation and the reaction speed constant k versus temperature, in comparison with free yeast cells, in order to prove if NC affects the catalytic activity and therefore acts as promoter of the alcoholic fermentation. Fermentations were performed at different temperatures in the presence of NC and with free cells, separately. Figure 3A shows that the NC biocatalyst increased the fermentation rate and was more effective as the temperature was reduced compared with free cells. Furthermore, Figure 3B and 3C shows that the activation energy Ea of the NC biocatalyst was 28% lower than that of free cells. Likewise, the reaction speed constant k was higher for the NC biocatalyst. These results indicate that NC is an excellent carrier to promote the catalytic action of cells for the fermentation of molasses, as it was observed for delignified cellulosic material by Iconomou et al. [6]. Figure 3. Nano-tubular cellulose (NC) and promotion of the alcoholic fermentation. (a) Fermentation kinetics observed at 25uC and 15uC by free cells and cells immobilised on NC (NC-yeast biocatalyst). (b) Arrhenius plot for evaluation of the activation energy and the pre-exponential factor of alcoholic fermentation performed with free and NC-yeast biocatalyst. (c) Activation energies and reaction rate constants of the fermentations made using free cells (FC) and cells immobilised on NC (IC). doi:10.1371/journal.pone.0034350.g003 PLoS ONE | 4 April 2012 | Volume 7 | Issue 4 | e34350 Nano-Tubular Cellulose It seems that this catalytic behaviour of NC is strongly related to its tubular structure, and can find application in fuel-grade ethanol production by increasing productivity and allowing a reduction in the size of the production plant [12]. NC is the first natural nano-tubular material characterized as a promoter of a bioconversion and the first biomolecule that promotes the alcoholic fermentation. The effect on the catalytic activity by NC that contains functional active hydroxyl groups is in agreement with a recent study, which proposed that effective catalysts can be created by adding functional hydroxyl groups in materials with nano-tubes, for example carbon nano-tubes [13]. This creates a new opportunity in research to examine this material as a possible catalytic promoter of other biochemical reactions like the reaction of lactic acid fermentation, malolactic fermentation, or the oxidation of alcohol by acetic acid bacteria to acetic acid. Also, its chemical and physical structure that has been studied in the context of this investigation can provide the base for the synthesis of new promoters of bioprocesses, having similar polymeric structures. Glucose pump theory for the promotion of fermentation by nano-tubular cellulose The catalytic effect of NC on the fermentation rate can be attributed to a glucose pump operating among the system of cellulose tubes that increase the surface, cells and glucose. The operation and rationale of a glucose pump is presented in Figure 4. According to this theory cells are encapsulated and joined by hydrogen bonding with hydroxyl groups between the surface of NC and the cell wall. Likewise, glucose molecules are joined with cellulose at the surface of the tubes through their hydroxyl group hydrogen bonds. Therefore, high cell and glucose concentrations are created mainly on the surface of the cellulose nano-tubes, increasing the rate of the biochemical reaction. Another factor that may affect the rate of the reaction is that glucose molecules and cells that are attached on the surface of the nano-tubes come very close to each other, increasing the glucose uptake rate. The bioconversion of glucose by the cells liberates alcohol, leading to continuous glucose pumping from the solution, mainly to the surface of the nano-tubes. Nano-tubular cellulose for domestic refrigerator bioprocess development The catalytic effect and reduction of the activation energy Ea of the alcoholic fermentation by NC, explains the high increase of the fermentation rate at low temperatures that was observed when delignified cellulosic materials where used as yeast immobilisation supports [4]. The feasibility of low temperature fermentation led to the idea of developing technologies for producing foods at home scale. Domestic wine making was of the stability of the surface layer: a growing instability in the surface layer leads to stronger convection and mixing. The drag coefficient is calculated following CH = κ2 A·B (43) with   z  z  zsl sl 0m − 9M + 9M , z0m L L   z  z  zsl sl 0h − 9H + 9H , B = ln z0h L L A = ln (45) where rs,min is the minimum surface resistance, LAI the leaf area index of the vegetated fraction, f1 a correction function Geosci. Model Dev., 8, 453–471, 2015 (50) where f2 is calculated following Eq. (47). where RiB is the bulk Richardson number and θv,s and hθv i are the virtual potential temperatures of the surface and the mixed-layer atmosphere respectively. The calculations of both resistances rveg and rsoil follow the method of Jarvis (1976) and are employed similarly as in the ECMWF global forecasting model. The vegetation resistance is based on the following multiplicative equation. rs,min f1 (Sin ) f2 (w2 ) f3 (VPD)f4 (T ), LAI where wwilt is the volumetric soil moisture at wilting point, wfc is the volumetric soil moisture at field capacity and gD is a correction factor for vapour pressure deficit that only plays a role in high vegetation. The soil resistance depends on the amount of soil moisture in the layer that has direct contact with the atmosphere. rsoil = rs,min f2 (w1 ), where κ is the von Kármán constant, z0m and z0h are the roughness lengths for momentum and heat, respectively, zsl is the depth of the atmospheric surface layer of 0.1h, L is the Monin–Obukhov length and 9M and 9H are the integrated stability functions for momentum and heat taken from Beljaars (1991). To find the values of L that are required in this function, the following implicit function is solved using a Newton–Raphson iteration method:  g zsl hθv i − θv,s RiB = (44) hθv i hU i2 h   i zsl zsl  z0h  zsl ln z0h − 9H L + 9H L = h    i2 , L sl 0m ln zz0m − 9M zLsl + 9M zL rveg = depending on incoming short wave radiation Sin , f2 a function depending on soil moisture w, f3 a function depending on vapour pressure deficit (VPD) and f4 a function depending on temperature T . Of these correction functions, the first three originate from the ECMWF model documentation and the fourth from Noilhan and Planton (1989) and are defined as   0.004Sin + 0.05 1 = min 1, (46) f1 (Sin ) 0.81 (0.004Sin + 1) 1 w − wwilt = (47) f2 (w) wfc − wwilt 1 = exp (gD VPD) (48) f3 (VPD) 1 = 1.0 − 0.0016(298.0 − T )2 , (49) f4 (T ) 2.7.3 Evapotranspiration calculation The total evapotranspiration consists of three parts: soil evaporation, leaf transpiration and evaporation of liquid water from the leaf surface. The total evapotranspiration is therefore proportional to the vegetated fraction of the land surface: LE = cveg (1 − cliq )LEveg + cveg cliq LEliq + (1 − cveg )LEsoil , (51) where LEveg is the transpiration from vegetation, LEsoil the evaporation from the soil and LEliq the evaporation of liquid water. The fractions that are used are cveg , which is the fraction of the total area that is covered by vegetation and cliq , which is the fraction of the vegetated area that contains liquid water. Since cliq is not constant in time, it is modelled following cliq = Wl , LAI Wmax (52) where Wmax is the representative depth of a water layer that can lay on one leaf and Wl the actual water depth. The evolution of Wl is governed by the following equation: LEliq dWl = , dt ρw Lv (53) where ρw is the density of water. R. H. H. Janssen and A. Pozzer: Boundary layer dynamics with MXL/MESSy 2.7.4 Soil model 2.7.5 A soil model is available for the calculation of soil temperature and moisture changes that occur on diurnal time scales, and therefore affect the surface heat fluxes. It is a forcerestore soil model, based on the model formulation of Noilhan and Planton (1989) with the soil temperature formulation from Duynkerke (1991). The soil model consists of two layers, of which only the thin upper layer follows a diurnal cycle. The soil temperature in the upper layer (Tsoil1 ) is calculated using the following equation, where the first term is the force term and the second the restore term: 2π dTsoil1 = CT G − (Tsoil1 − Tsoil2 ), dt τ (54) where CT is the surface soil/vegetation heat capacity, G the soil heat flux already introduced in the SEB, τ the time constant of one day and Tsoil2 the temperature of the deeper soil layer. The soil heat flux is calculated using G = 3(Ts − Tsoil1 ), (55) where 3 is the thermal conductivity of the skin layer. The heat capacity CT is calculated following Clapp and Hornberger (1978) using   wsat b/2 log 10 CT = CT,sat , (56) w2 where CT,sat is the soil heat capacity at saturation, w2 the volumetric water content of the deeper soil layer and b an empirical constant that originates from data fitting. The evolution of the volumetric water content of the top soil layer w1 is calculated using  dw1 C1 LEsoil C2 w1 − w1,eq , =− − dt ρw d1 Lv τ (57) where w1,eq is the water content of the top soil layer in equilibrium, d1 is a normalization depth and where C1 and C2 are two coefficients related to the Clapp and Hornberger parametrization (Clapp and Hornberger, 1978), that are calculated using   wsat b/2+1 C1 = C1,sat , (58) w1 w2 C2 = C2,ref , (59) wsat − w2 where C1,sat and C2,ref are constants taken from Clapp and Hornberger (1978). The water content of the top soil layer in equilibrium is     ! w2 p w2 8p 1− (60) w1, eq = w2 − wsat a wsat wsat with a and p two more fitted constants from Clapp and Hornberger (1978). 461 Surface fluxes of momentum Finally, we introduce parametrizations for the momentum fluxes at the surface (Stull, 1988) and the friction velocity (u∗ ), which are required to calculate the horizontal wind budget in the mixed layer (Sect. 2.3). p u∗ = CM hU i, (61) u0 w 0 s = −CM hU ihui, (62) v 0 w 0 s = −CM hU ihvi, (63) where CM is the drag coefficient for momentum, defined as κ2 CM = h    sl − 9M zLsl + 9M ln zz0m 3 z0m  L i. (64) Implementation in the MESSy structure MESSy is an interface to couple submodels of earth system processes, which offers great flexibility to choose between different geophysical and -chemical processes. In the first version of MESSy, only the general circulation model ECHAM5 could be used (Jöckel et al., 2005). The second round of development also enabled the use of base models with different dimensions (Jöckel et al., 2010). For the current implementation, we used MESSy version 2.50. Here, we give a brief overview of the MESSy structure, more details can be found in Jöckel et al. (2005, 2010). In MESSy, each FORTRAN module belongs to one of the following layers: – The Base Model Layer (BML) defines the domain of the model, which can be a box, 1-D or 3-D. This can be a complex atmospheric model, for instance a general circulation model like ECHAM5 (Jöckel et al., 2005), but in our case it consists of two boxes stacked on top of each other (Fig. 3). – The Base Model Interface Layer (BMIL) manages the calls to specific submodels, data input and output, and data transfer between the submodels and the base model. Global variables are stored in structures called “channel objects”. – The SubModel Interface Layer (SMIL) collects relevant data from the BMIL, transfers it to the SMCL and sends the calculated results back to the BMIL. The SMIL contains the calls of the respective submodel routines for the initialization, time integration, and finalizing phase of the model. – The SubModel Core Layer (SMCL) contains the code for the base model-independent implementation of the physical and chemical processes or a diagnostic tool. Geosci. Model Dev., 8, 453–471, 2015 462 R. H. H. Janssen and A. Pozzer: Boundary layer dynamics with MXL/MESSy free troposphere entrainment gas/particle partitioning chemical conversion boundary height layer land surface sunrise deposition emission time sunset Figure 3. Processes relevant to evolution of species concentrations in the boundary layer. Open and closed circles depict gas-phase and aerosol-phase species, respectively. 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