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Agrociencia

versão On-line ISSN 2521-9766versão impressa ISSN 1405-3195

Agrociencia vol.52 no.8 México Nov./Dez. 2018

 

Food Science

Production of xylitol from non-detoxified acid hydrolizates from sorghum straw by Debaryomyces hansenii

Edgar Ledezma-Orozco1 

Régulo Ruíz-Salazar1 

Guadalupe Bustos-Vázquez1 

Noé Montes-García2 

Viviana Roa-Cordero3 

Guadalupe Rodríguez-Castillejos1  * 

1Departamento de Tecnología de Alimentos, Universidad Autónoma de Tamaulipas U.A.M. Reynosa-Aztlán. Calle 16 y Lago de Chapala SN. Colonia Aztlán, C.P 88740. Reynosa, Tamaulipas, México.

2Centro de Investigación Regional Noreste, INIFAP Campo Río Bravo, Km. 61 Carretera Matamoros- Reynosa C.P. 88900, Ciudad Río Bravo, Tamaulipas, México.

3Universidad de Santander, Campus Universitario Lagos del Cacique, calle 70 No 55-210 Bucaramanga, Santander, Colombia.

Abstract

The industrial production of xylitol is carried out with the chemical hydrogenation of D-xylose and it is a costly process. An alternative procedure is the fermentation of lignocellulosic residues with yeasts such as Debaryomyces hansenii (Zopf) Lodder and Kreger-van Rij. Therefore, the objective of this study was to evaluate the extraction of xylitol from sorghum straw, in detoxified and non-detoxified media. White sorghum straw [Sorghum bicolor (L.) Moench.], variety RB-Paloma, was hydrolyzed with H2SO4 at 2, 4 and 6 %; solid liquid ratio 1:6, 1:8 and 1:10; all treatments at 120 °C for 80 min. Those hydrolyzed were neutralized and used to evaluate the production of xylitol; culture media contained 30, 40 or 50 g L-1 xylose were inoculated with D. hansenii and incubated at 30 and 35 °C, 150 and 200 RPM for 96 h. In addition, the data were analyzed with ANDEVA and means tests (p ≤ 0.05). The maximum concentration of xylitol in the detoxified media was 28.8 g L-1 (40 g xylose, 35 °C, 200 rpm), and in non-detoxified, the maximum found was 29.23 g L-1 (30 g xylose, 35 °C, 150 rpm). The straw evaluated could be used to obtain xylose with a potential use in media for fermentation, and results also suggest that D. hansenii can metabolize xylose in the presence of acetic acid and furfural.

Keywords: xylitol; Debaryomyces hansenii; Sorghum bicolor; detoxification

Introduction

Xylitol (C5H12O5) is a pentahydroxilated sugar-alcohol present in amounts below 405 mg in some fruits and vegetables (Mäkinen and Söderling, 1980), it is used as a sweetener in processed foods and is a substitute for sacarose for diabetics, since its metabolism is independent of insulin. The pharmaceutical industry uses it as an anticariogenic agent and to reduce the risk of otitis media (de Albuquerque et al., 2014; Vernacchio et al., 2014). The chemical way to extract xylitol includes the reduction of xylose in a hydrogenation process between 80 and 140 °C and a pressure higher than 50 atm. This process is costly and it produces secondary compounds; therefore, the synthesis with microorganisms that produce xylose reductase and xylitol dehydrogenase are an alternative for the production of xylitol (Prakasham et al., 2009; de Albuquerque et al., 2014; Pappu and Gummadi, 2017; Sena et al., 2017). Renewable sources of carbon can be used as a raw material for the extraction of xylose, for example, wood and agricultural residues with high amounts of lignocellulose, the most important structural component of plants, composed of hemicellulose, lignin and cellulose (Koutinas et al., 2014; Pal et al., 2013), and, when they are hydrolyzed, xylose stands out as the main monosaccharide. Lignocellulosic biomass has great potential in biotechnology to help obtain metabolites of industrial interest; here lies the importance of converting xylose to xylitol, since it adds value to the production chain (from Arruda et al., 2011; Prakash et al., 2011).

Yeasts are candidate microorganisms for the fermentation of xylose, and the main genuses are Pichia sp., Candida sp. and Debaryomyces sp. (Pérez-Bibbins et al., 2014; Pappu and Gummadi, 2017). The yield of xylitol depends on the concentration of xylose, temperature, pH, and ventilation, which are important for the correct transportation of xylose inside the cells and the functioning of the enzymes involved in the conversion; in addition, most xylitolproducing yeasts have a low tolerance to toxic compounds such as furans and acetic acid (Pappu and Gummadi, 2016; López-Linares et al., 2018). Due to this, if the source of carbon is obtained from the lignocellulosic biomass, it is important to evaluate the presence of these inhibiting compounds, which are produced by hydrolyzing lignocellulose with acids or bases or high reaction temperatures. These compounds lead to the formation of free radicals, which damages DNA, proteins and cell membranes of yeasts, and also reduce the resistance to salts and sugars. However, certain yeasts are resistant to these compounds and can metabolize the carbon sources under conditions of stress (Allen et al., 2010; Field et al., 2015). These compounds can be eliminated using resin exchange methods, treatments with bases, active carbon, as well as filtering or centrifuging after any of these processes (Chandel et al., 2013).

The main goal of this study was to obtain xylose from sorghum straw and to evaluate the production of xylitol by Debaryomyces hansenii using the hydrolysates obtained, with or without detoxification treatments, in order to evaluate the resistance of yeast to inhibiting compounds. Our hypothesis was that xylose present in the hydrolysates is an adequate source of carbon for the production of xylitol and yeast increases the yield in the presence of inhibiting compounds.

Materials and methods

Raw material

Straw obtained from sorghum [Sorghum bicolor (L.) Moench.] of the RB-Paloma variety was donated by the National Farming Research Institute, Campo Experimental Río Bravo, Tamaulipas, Mexico. The straw was cut into pieces, 5 cm in length, dried in a stone with ventilation at 60 °C for 24 h, grounded and sieved to obtain particles with an approximate diameter of 500 mm.

Preliminary studies

Given that the most widely used pretreatment for acid hydrolysis is grinding, in order to obtain a larger surface area, we determined the feasibility of using fine flour (particle size ≤0.05 µm) and another, thicker one (≥500 mm, product of sieving), or using a mixture of both types of flour in a 1:1 proportion to use all the residue. Hydrolysis was carried out under the following conditions: sulfuric acid at 4 % for 80 min at 120 °C, with a solid-liquid ratio of 1:6 with all three treatments; these conditions were selected according to studies by Aguilar et al. (2002), Téllez-Luis et al. (2002) and Sepúlveda-Huerta et al. (2006).

Hydrolysis and detoxification

Hydrolysis was carried out with sulfuric acid under the following conditions: acid 2, 4 and 6 %; solid-liquid ratio of 1:6, 1:8 and 1:10. Reaction time and temperature were constant (80 min and 120 °C, respectively) and nine hydrolysis treatments with sorghum straw flour (Table 1).

Table 1 Conditions of acid hydrolysis with RB Paloma sorghum straw flour. 

Clave de tratamiento Ácido sulfúrico (%) Relación sólido:líquido
TH1 2 1:6
TH2 4 1:6
TH3 6 1:6
TH4 2 1:8
TH5 4 1:8
TH6 6 1:8
TH7 2 1:10
TH8 4 1:10
TH9 6 1:10

Afterwards, the best conditions for hydrolysis were chosen, the syrups obtained were divided into two equal parts, and one was treated with active carbon to eliminate inhibiting compounds, furfural and acetic acid. The detoxification conditions were as follows: pH 5 with a time of 45 min and a charge of active carbon at 1.5. The other part of the syrups was not detoxified, in order to evaluate the growth of yeast in the presence of furfural and acetic acid. Next, the pH of the hydrolysates and of the untreated ones was adjusted with active carbon; calcium carbonate (CaCO3) was added, followed by a vacuum filtering and measured using a potentiometer (Ultra Basic UB-10 Denver Instrument). A 50 g sample of the syrupactive carbon was placed in 250 mL beakers, stirred at 150 rpm and 45 °C in an incubator. The samples were then centrifuged at 10 000 rpm for 10 min, and the concentrations of xylose, acetic acid, and furfural were analyzed before and after adding active carbon. The concentration of xylose and acetic acid were determined using High Performance Liquid Chromatography (HPLC HP-1100) and a Transgenomic ION-300 column, with a stone temperature of 45 °C, and an isocratic elution of 0.4 mL min-1 of flow of mobile phase (H2SO4 0,0025 M). The concentration of furural was measured using UV-vis (UV-1800 Shimadzu) spectrophotometry at a wavelength of 270 nm.

Microorganism and culture medium

The liophilized strain of D. hansenii NRRL Y-7426 was reactivated in Erlenmeyer beakers with100 mL of medium with xylose (30 g L-1), peptone (5 g L-1) and yeast extract (3 g L-1), the pH was adjusted to 5.5, incubated at 28 °C, stirring at 150 rpm for 48 h. Afterwards, the production of xylitol in the media based on xylose, product of the hydrolyzed acid from the sorghum straw.

Production of xylitol

The production of xylitol by D. hansenii was evaluated in media with detoxified and non-detoxified hydrolysates with 30, 40 and 50 g L-1 of xylose, at 30 and 35 °C and a stirring speed of 120 and 200 rpm; the concentration of xylitol was measured every 12 h up to 96 h of fermentation. The variables determined were yield or conversion factor (YP/S, g xylitol produced times g xylose consumed) and volumetric productivity (Qp, g xylitol produced per L of medium in 1 h). The concentration of xylitol was measured by HPLC using the same conditions as those mentioned for xylose.

With the data, a multi-factorial ANDEVA was carried out to determine the effect of the independent variables on the composition of the hydrolysate and production of xylitol. The differences between treatments were evaluated using a Fisher analysis for means comparison (p≤0.05).

Results and discussion

The analyses performed on fine and coarse flour obtained from the total sorghum residues showed no significant differences with the concentration of xylose obtained, as compared to the hydrolysis of flour with smaller particles (Table 2).

Table 2 Concentration of xylose obtained from the hydrolysis of the different types of sorghum straw flour. 

Tipo de harina Xilosa (g L-1)
Harina fina (HF) 45.7 ± 2.42a
Harina gruesa (HG) 50.91 ± 1.96a
Proporción 1:1 (HF:HG) 45.38 ± 2.93a

There were no significant differences between treatments (Fisher; p>0.05).

Acid hydrolysis of RB-Paloma sorghum straw and detoxification

Treatment TH3 (H2SO4 at 6 %, 120 °C for 80 min and solid-liquid ratio 1:6) produced the greatest concentration of xylose (63.82 ±0.78 g L-1), while the lowest concentration was obtained in treatment TH7 with 23.09 ±4.56 g L-1, with 2 % of H2SO4 at 120 °C for 80 min in a proportion of 1:10 (Table 3). This amount of xylose is similar to that reported by Téllez-Luis et al. (2001) with a concentration of 16 g L-1 of xylose with the acid hydrolysis of red sorghum hay with H2SO4 at 6 %, for 60 min and 120 °C. Herazo et al. (2009) hydrolyzed rice straw with H2SO4 at 2 % for 30 min and obtained 32.5 g L-1 of reducing sugars and 9.9 g L-1 of xylose.

Table 3 Concentration of xylose, acetic acid and furfural in the acid syrups of RB Paloma sorghum. 

Tratamiento Xilosa g L-1 Ácido acético g L-1 Furfural g L-1
TX1 44.60c ± 0.48 9.47b ± 0.53 5.81c ± 0.20
TX2 51.22c ± 0.31 11.07a,b ± 0.53 8.06b ± 0.24
TX3 63.82a ± 0.78 11.62a ± 0.51 9.77a ± 0.39
TX4 25.43d ± 0.46 4.22d ± 0.54 4.25d ± 0.30
TX5 44.40c ± 0.78 7.99c ± 0.66 6.39c ± 0.38
TX6 51.36c ± 7.42 9.04b,c ± 0.55 7.98b ± 0.49
TX7 23.09d ± 4.56 4.30d ± 0.56 4.15d ± 0.27
TX8 39.56c ± 4.64 10.03b ± 0.49 6.03c ± 0.02
TX9 61.46b ± 0.82 10.24b ± 0.27 7.97a,b,c ± 1.48

a,b,c,d: Different letters in a column indicate significant differences between treatments (Fisher; ≤0.05).

±Standard deviation (95 %).

For the growth of D. hansennii and production of xylitol, we used the hydrolysis conditions of treatment TH9 because it produced less furfural and acetic acid. These compounds derive from the degradation of lignin and act as inhibitors of microbial growth by reducing the metabolism (Mussatto and Roberto, 2004; Oliva et al., 2006; Pereira et al., 2011); consequently, it is important to have low values of these toxic compounds. Fermentations were carried out in detoxified and non-detoxified media in order to evaluate the growth of yeast in the presence of inhibiting compounds, and therefore reduce production costs and time.

Detoxification

With the process of detoxification with active carbon, acetic acid and furfural decreased by 72 and 65.5 %, respectively (Table 4). Kamal et al. (2011) performed acid hydrolysis on palm trunk, then detoxified the syrups obtained with 1 and 2.5 % of active carbon, and the maximum reduction found was 58 % for furfural with 2.5% of active carbon. Villarreal et al. (2006) performed an acid hydrolysis on eucalyptus residues, and reported a reduction of 100 and 10.6 % of furfural and acetic acid, respectively, using 5 % active carbon at a pH of 5.5.

Table 4 Concentration of inhibiting compounds in hydrolysis before and after detoxification. 

Condición Furfural g L-1 Ácido acético g L-1
Antes de detoxificar 7.97± 1.48a 10.24 ± 0.27a
Después de detoxificar 2.27±0.27b 3.53 ± 1.64b

a,b:Different letters in a column indicate statistically significant differences between treatments (Fisher; p≤0.05).

±Standard deviation (95 %).

In order to evaluate which of the two factors (concentration of acid, solid-liquid ratio, or both) has a greater effect on the concentration of xylose obtained, a two-way ANOVA was carried out with a confidence level of 95 %. The result showed that the percentage of acid was the main factor in the hydrolyses performed (p≤0.05), and in this study, the solid-liquid ratio shows no significant difference (p>0.05) between treatments (Table 5).

Table 5 Analysis of variance of the factors involved in the extraction of xylose. 

Fuentes de variación Suma de Cuadrados G.L Cuadrados Medios F p ≤
Ácido sulfúrico, % 1162.62 2 581.309 17.98 0.0100
Relación s/l 305.479 2 152.739 4.72 0.0885
Residuos 129.311 4 32.3277
Total 1597.41 8

Solid-liquid ratio.

Production of xylitol in detoxified and nondetoxified media

The highest concentration of xylitol in the media detoxified with active carbon was obtained in TH8 (40 g xylose, 35 °C, 200 rpm) with 28.8 g L-1 after 48 h of fermentation; whereas in non-detoxified media, TH11 (30 g xylose, 35 °C, 150 rpm) produced a maximum concentration of 29.23 g L-1 after 48 h. The concentration of xylitol was similar in the media with detoxified and non-detoxified hydrolysate. Although Carvalheiro et al. (2005) mentioned that xylitol production is favored by high concentrations of xylose, in our study, the lowest concentration of xylitol was in the medium with 50 g L-1 of the carbon source. Carvalheiro et al. (2005) carried out detoxification treatments in hydrolyzed acids from rice straw, and found that the use of ionic exchange resin eliminated the highest concentration of furfural, although the media designed with these detoxified hydrolysates had a low xylitol yield (0.51 g g-1). This may be due to the fact that these processes eliminate inhibiting compounds as well as other compounds, such as minerals that can serve as growth factors for yeast.

The highest concentration of xylitol was 29.23 g L-1 (Table 6) and was obtained using a nondetoxified hydrolysate, although the detoxification process promotes the ability of fermentation of microorganisms in media based on lignocellulosic hydrolysates (Alriksson et al., 2011; Cavka and Jönsson, 2013). Treatments 1 to 8 are fermentations with detoxified hydrolysates, while treatments 9 to 19 are non-detoxified. After reaching the maximum production of xylitol, the concentration of xylose decreases, due to its conversion into xylitol, since the latter is a primary metabolite, meaning it is related to the growth of yeast; that is, D. hansenii uses xylose as a source of carbon to grow and therefore the relation xylose-growth is inversely proportional. Therefore, it is important to establish the optimum time of fermentation, because when the microorganism enters a stationary phase, the concentration of the metabolite decreases.

Table 6 Conditions of fermentation used for the production of xylitol and fermentative parameters. 

Tratamiento Xilosa g L-1 Temp (°C) RPM Detox T (h) Xilitol (g L-1) YP/S (g g-1) Qp (g L-1 h-1)
TX1 30 30 150 HD 36 23.58 ±° 5.50a,b 0.84 ± 0.16a 0.49 ± 0.11d
TX2 30 30 200 HD 36 28.41 ± 2.90ª,b 1.18 ± 0.40a 0.79 ± 0.01c
TX3 30 35 150 HD 48 23.8 ± 2.37b 0.89 ± 0.06a 0.5 ± 0.05d
TX4 30 35 200 HD 36 25.56 ± 5.47a,b 0.97 ± 0.01a 0.71 ± 0.02c
TX5 40 30 150 HD 48 27.97 ± 5.55a,b 0.78 ± 0.37a 0.58 ± 0.28b,c
TX6 40 30 200 HD 36 23.42 ± 4.64a,b 0.85 ± 0.20a 0.65 ± 0.16c
TX7 40 35 150 HD 36 26.79 ± 3.03a,b 0.73 ± 0.13a 0.74 ± 0.08c
TX8 40 35 200 HD 48 28.86 ± 8.98a,b 0.82 ± 0.25a 0.6 ± 0.19c
TX9 30 30 150 HND 24 25.99 ± 4.49a,b 1.03 ± 0.14a 1.08 ± 0.09a
TX10 30 30 200 HND 48 22.73 ± 5.20a,b 0.82 ± 0.21a 0.47 ± 0.16d
TX11 30 35 150 HND 48 29.23 ± 2.64a,b 1.16 ± 0.06a 0.61 ± 0.02d
TX12 30 35 200 HND 24 26.4 ± 4.48a,b 1.01 ± 0.13a 1.1 ± 0.09a
TX13 40 30 150 HND 36 23.4 ± 4.46a,b 0.68 ± 0.15a 0.97 ± 0.06a
TX14 40 30 200 HND 48 22.74 ± 4.42a,b 0.66 ± 0.13a 0.47 ± 0.09d
TX15 40 35 150 HND 24 27.07 ± 9.65a,b 0.78 ± 0.35a 1.13 ± 0.25a
TX16 40 35 200 HND 36 19.22 ± 1.09c 0.51 ± 0.01b 0.53 ± 0.01d
TX17 50 30 150 HND 24 15.93 ± 2.43c 0.35 ± 0.07d 0.66 ± 0.05c
TX18 50 30 200 HND 24 20.44 ± 4.60b 0.43 ± 0.01c,d 0.85 ± 0.01b
TX19 50 35 200 HND 24 21.78 ± 0.38a,b 0.45 ± 0.01c 0.91 ± 0.01a

a,b,c,d:Different letters in a column indicate significant differences between treatments (Fisher; p≤0.05); °Standard deviation (95 %); RPM: revolutions per minute; HD: detoxified hydrolysates; HND: non-detoxified hydrolysates; YP/S: Yield factor and Qp: volumetric productivity.

Indicates the time at which the highest concentration of xylitol was reached in each treatment.

Some of the most common detoxification methods include adjusting the pH with calcium carbonate, followed by adsorption with active carbon (Carvalheiro et al., 2005). Greetham et al. (2016) mention that a low concentration of acetic acid exerts an antagonistic effect on furfural, which helps yeast grow under these stress conditions.

Villarreal et al. (2006) performed a hydrolysis with hemicellulosic eucaliptus (Eucalyptus grandis) and they used a strain of Candida guilliermondii responsible for the conversion of xylose; the highest concentration of xylitol reached was 32.7 g L-1 after 48 h of fermentation, with a yield of 0.57 g g-1 and a Qp of 0.68 g L-1 h-1. Mussatto and Roberto (2001) hydrolyzed rice hay with 0.1 M H2SO4 at 121 °C for 20 min and a solid-liquid ratio of 1:10, and for the conversion of xylose by C. guilliermondii FTI 20037, they used 20 g L-1 of xylose in the culture media and they obtained 0.72 g g-1 and a volumetric productivity of 0.61 g L-1 h-1.

Carvalheiro et al. (2006) evaluated the production of xylitol by D. hansenii in media based on acid hydrolysates from beer grains, they processed detoxified and non-detoxified hydrolysates with active carbon, and the values obtained for YP/S were 0.51 and 0.5 g g-1 , and for Qp, 0.29 and 0.33 g L-1 h-1 in detoxified and non-detoxified media, respectively. These amounts are lower than those obtained in our study: top values of 1.16 g g-1 and 1.13 g L-1 h-1 for YP/S and Qp respectively, after 24 h of fermentation in a non-detoxified medium; in a detoxified hydrolysate, values for YP/S and maximum Qp were 1.18 g g-1 and 0.79 g L-1 h-1. The tendency in both studies was similar regarding higher volumetric productivity of xylitol from non-detoxified media. Huang et al. (2011) isolated the strain of C. tropicalis JH030 from residual sludge from a bioethanol-producing plant, they evaluated its growth and production of xylitol in non-detoxified rice hay media and reported a YP/S= 0.71 g g-1. In our study, the media based on RB-Paloma white sorghum straw, still not detoxified, are a considerable amount of carbon for the D. hansenii growth process and its conversion from xylose to xylitol due to a good yield and volumetric productivity, which is higher to reports from other studies with lignocellulosic materials.

Wang et al. (2011) used hydrolysates from maize ears and carried out fermentations at 150 and 200 rpm with 140 g L-1 of xylose and a temperature of 30 °C; the highest amount of xylitol was obtained with 200 rpm, and a Qp of 2.12 g L-1 h-1 after 24 h of fermentation. Although the volumetric productivity is double than the one in our study, the concentration of xylose used is almost five times higher, which increases production costs.

Finally, with the highest concentrations of each fermentation treatment, a multifactorial ANOVA was carried out, with a 95 % confidence and no significant differences were found (Table 7). Therefore, these results help us deduce that there is no difference between using detoxified or nondetoxified hydrolysates, which means a potential increase in the production of xylitol with a reduction in time, cost, and materials, by eliminating the detoxification process in the hydrolysates.

Table 7 Analysis of variance for xylitol. 

Fuente de variación Suma de cuadrados G. L. Cuadrado medio del error Razón-F p≤
Efectos principales
A: xilosa 53.0942 2 26.5471 3.09 0.0797
B: temperatura 10.1644 1 10.1644 1.18 0.2963
C: rpm 1.113 1 1.113 0.13 0.7246
D: detox 8.42451 1 8.42451 0.98 0.3399
Residuos 111.579 13 8.58298
Total (corregido) 222.413 18

Conclusions

The straw of RB-Paloma white sorghum can be used to obtain xylose for fermentation media. This study shows that there is no difference between the extraction of xylose from fine flour, coarse flour, or a mixture of both. The concentration of sulfuric acid is the factor of the most impact in hydrolysis, because increasing it leads to a higher concentration of xylose. In RB-Paloma sorghum straw hydrolysates, the xylose present is a good source of carbon for the production of xylitol by D. hansenii.

Detoxification helps to reduce the amount of furfural and acetic acid, which, in high concentrations, inhibit the growth of microorganisms for fermentation; however, D. hansenii was able to metabolize xylose in the presence of these inhibiting compounds. This shows the potential of this agricultural residue in the production of fermentation media as an alternative in the production of xylitol.

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Received: June 2017; Accepted: January 2018

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