The Open Biotechnology Journal




ISSN: 1874-0707 ― Volume 14, 2020

Microcalorimetric Investigation of the Effect of the Ionic Liquid 1-Butyl-3-Methylimidazolium Chloride on the Fermentation of Saccharomyces cerevisiae AY93161 for Lignocellulosic Ethanol Production



Wangxiang Huang1, Jiancheng Jin2, Liang Feng3, Wenjing Huang1, Ke Wang1, Yi Liu2, Yuanxin Wu1, Shengdong Zhu1, *
1 Key Laboratory for Green Chemical Process of Ministry of Education, Hubei Key Laboratory of Novel Chemical Reactor and Green Chemical Technology, School of Chemical Engineering and Pharmacy, Wuhan Institute of Technology, Wuhan 430073, P.R.China
2 State Key Laboratory of Virology & Key Laboratory of Analytical Chemistry for Biology and Medicine (MOE), College of Chemistry and Molecular Sciences, Wuhan University, Wuhan 430072, P.R. China
3 School of Environmental Studies, China University of Geosciences, Wuhan 430074, P. R. China

Abstract

The effects of ionic liquid 1-butyl-3-methylimidazolium chloride (BMIMCl) on the ethanol fermentation process of Saccharomyces cerevisiae AY93161 were investigated by using microcalorimetry. On the basis of microcalorimetric and process data, the thermokinetic parameters of the ethanol fermentation process at different BMIMCl concentrations from 0.001 to 5 gL-1 were calculated. Compared to the control, the BMIMCl caused a decreased value of the maximum specific growth rate µm (from 0.226 to 0.105 h-1), and an increased value of the maximum specific produced heat rate pm (from 2.08 to 7.06 mWlg-1) and the total heat output H for producing 1 g ethanol (from 990 to 1871 Jg-1). The decreased µm and increased pm and H led to lower final yeast concentration (from 3.85 to 2.39 gL-1) and ethanol concentration (from 40.3 to 25.1 gL-1). This gives useful information for improving the lignocellulosic ethanol production process using the ionic liquid technology.

Keywords: BMIMCl, Lignocellulosic Ethanol, Microcalorimetry, Thermokinetics.


Article Information


Identifiers and Pagination:

Year: 2016
Volume: 10
First Page: 391
Last Page: 397
Publisher Id: TOBIOTJ-10-391
DOI: 10.2174/1874070701610010391

Article History:

Received Date: 13/09/2016
Revision Received Date: 28/10/2016
Acceptance Date: 08/11/2016
Electronic publication date: 29/11/2016
Collection year: 2016

© Huang et al.; Licensee Bentham Open

open-access license: This is an open access article licensed under the terms of the Creative Commons Attribution-Non-Commercial 4.0 International Public License (CC BY-NC 4.0) (https://creativecommons.org/licenses/by-nc/4.0/legalcode), which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited.


* Address correspondence to this author at the Key Laboratory for Green Chemical Process of Ministry of Education, Hubei Key Laboratory of Novel Chemical Reactor and Green Chemical Technology, School of Chemical Engineering and Pharmacy, Wuhan Institute of Technology, Wuhan 430073, P.R.China; Tel/Fax: 0086-27-87194980; E-mails: whictzhusd@sina.com, zhusd2003@21cr.com





INTRODUCTION

Production of sustainable bio-energy has focused on the research towards renewable resources as an alternative to depletion of fossil resources as well as growing environmental issues such as emission of green house gases and air pollution by incomplete combustion of fossil fuels [1Gupta A, Verma JP. Sustainable bio-ethanol production from agroresidues: A review. Renew Sustain Energy Rev 2015; 41: 550-67.
[http://dx.doi.org/10.1016/j.rser.2014.08.032]
]. Lignocellulosic biomass is the most abundant and renewable natural resource in the world. It has the potential to serve as a renewable feed-stock to chemical commodity and production of fuel, particularly bio-ethanol [2Zhu S, Wang K, Huang W, et al. Acid catalyzed hydrolysis of lignocellulosic biomass in ionic liquids for ethanol production: opportunities & challenges. BioResources 2016; 11: 3-5.]. Production of ethanol generally consists of two sub-processes: conversion of carbohydrates in lignocellulosic biomass to fermentable sugars and fermentation of the obtained sugars to ethanol. Because of the complex structure of lignin and hemicellulose and cellulose in lignocellulosic biomass, preparation of fermentable sugars is often a challenging work during lignocellulosic ethanol production [2Zhu S, Wang K, Huang W, et al. Acid catalyzed hydrolysis of lignocellulosic biomass in ionic liquids for ethanol production: opportunities & challenges. BioResources 2016; 11: 3-5.]. Use of ionic liquids has provided a new technical tool to convert the carbohydrates in lignocellulosic biomass to fermentable sugars for ethanol production [3Wang Q, Wu Y, Zhu S. Use of ionic liquids for improvement of cellulosic ethanol production. BioResources 2011; 6: 1-2.]. A number of studies indicate that the carbohydrates in lignocellulosic biomass can be efficiently converted to fermentable sugars by using the ionic liquid technology [4Zhang S, Sun J, Zhang X, Xin J, Miao Q, Wang J. Ionic liquid-based green processes for energy production. Chem Soc Rev 2014; 43(22): 7838-69.
[http://dx.doi.org/10.1039/C3CS60409H] [PMID: 24553494]
-6Lee SH, Doherty TV, Linhardt RJ, Dordick JS. Ionic liquid-mediated selective extraction of lignin from wood leading to enhanced enzymatic cellulose hydrolysis. Biotechnol Bioeng 2009; 102(5): 1368-76.
[http://dx.doi.org/10.1002/bit.22179] [PMID: 19090482]
]. However, it is inevitable that some ionic liquids are remained in the obtained sugars. Some previous researches have shown that the residual ionic liquids in sugars have a negative effect on the subsequent ethanol fermentation process, especially for yeast growth [7Zhu S, Yu P, Lei M, et al. Investigation of the toxicity of the ionic liquid 1-butyl-3-methylimidazolium chloride to Saccharomyces cerevisiae AY93161 for lignocellulosic ethanol production. Polish J Chem Technol 2013; 15: 94-8.
[http://dx.doi.org/10.2478/pjct-2013-0029]
-9Ouellet M, Datta S, Dibble DC, et al. Impact of ionic liquid pretreated plant biomass on Saccharomyces cerevisiae growth and biofuel production. Green Chem 2011; 13: 2743-9.
[http://dx.doi.org/10.1039/c1gc15327g]
]. The toxicity studies on ionic liquids to yeast cells demonstrate that the interactions between ionic liquids and yeast mitochondrial membrane protein can lead to the morphology change of yeast and its mitochondria, alter the polarization of its mitochondrial membrane potential, and shift its metabolism from respiration to fermentation [10Mehmood N, Husson E, Jacquard C, et al. Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae: metabolic, physiologic, and morphological investigations. Biotechnol Biofuels 2015; 8: 17.
[http://dx.doi.org/10.1186/s13068-015-0206-2] [PMID: 25688291]
, 11Dickinson Q, Bottoms S, Hinchman L, et al. Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain. Microb Cell Fact 2016; 15: 17.
[http://dx.doi.org/10.1186/s12934-016-0417-7] [PMID: 26790958]
]. Therefore, alleviating the toxicity of residual ionic liquids to yeast growth and their negative effects on the subsequent fermentation process is a key issue for lignocellulosic ethanol production using the ionic liquid technology. To do so, it is essential to understand the metabolic regulation mechanism of the residual ionic liquids affecting ethanol fermentation process and its thermokinetics.

Microcalorimetry is a laboratory method for real-time, continuous measurement of the heat flow rate and cumulative amount of heat consumed or produced during a biological process [12Braissant O, Bonkat G, Wirz D, Bachmann A. Microbial growth and isothermal microcalorimetry: growth models and their application to microcalorimetric data. Thermochim Acta 2013; 555: 64-71.
[http://dx.doi.org/10.1016/j.tca.2012.12.005]
]. As a universal, integral, non-destructive, and highly sensitive method, microcalorimetry is often used to online monitor the bacterial growth and metabolism for a microbial fermentation process [13Kabanova N, Kazarjan A, Stulova I, Vilu R. Microcalorimetric study of growth of lactococcus lactis IL 1403 at different glucose concentrations in broth. Thermochim Acta 2009; 496: 87-92.
[http://dx.doi.org/10.1016/j.tca.2009.07.003]
]. At present, microcalorimetry has been widely used to study thermokinetics for a biological process [12Braissant O, Bonkat G, Wirz D, Bachmann A. Microbial growth and isothermal microcalorimetry: growth models and their application to microcalorimetric data. Thermochim Acta 2013; 555: 64-71.
[http://dx.doi.org/10.1016/j.tca.2012.12.005]
-14Yao J, Liu Y, Tuo Y, et al. Studies on the growth metabolism of Bacillus thuringiensis and its vegetative insecticidal protein engineered strains by microcalorimetry. Prikl Biokhim Mikrobiol 2006; 42(3): 310-4.
[PMID: 16878547]
]. In this work, the effects of ionic liquid 1-butyl-3-methylimidazolium chloride (BMIMCl) on the ethanol fermentation process of Saccharomyces cerevisiae AY93161 were investigated by using microcalorimetry in combination with the conventional microbial measurements. Based on the microcalorimetric and process data, the metabolic regulation mechanism of the BMIMCl affecting ethanol fermentation process and its thermokinetics were analyzed. This will give useful information for improving the lignocellulosic ethanol production process using the ionic liquid technology by alleviating the negative effect of residual ionic liquids on the subsequent fermentation process.

MATERIALS AND METHODS

All experiments were done in triplicate, and all experimental procedures were performed under aseptic conditions.

Chemicals

The BMIMCl used in this study was obtained from Lanzhou Greenchem ILs, LICP, CAS, China and its purity was 99% up based on HPLC analysis. All other chemicals employed in this study were of reagent grade and purchased from Wuhan Zhenchun Biological Technology Co. Ltd., China.

Inoculum Preparation

The yeast Saccharomyces cerevisiae AY93161 was used throughout this study. The stock cultures were maintained on YPD agar plates at 4 °C and transferred to fresh plates every 4 weeks to avoid micro-organism degradation. The inoculum preparation was by means of micro-organism transfer from stock cultures to a fresh plate and grew for 48 h at 30°C. Following this period, single colonies were transferred to a 250 ml flask with 100 ml YPD medium. The flask was placed on an orbital shaker with a shaking diameter 5 cm and a shaking frequency 200 rpm and incubated at 30°C for 24 h. This was used as the inoculum for microcalorimetric measurements and parallel ethanol fermentation experiments, and its yeast concentration is about 1.5× 1011 cells l-1.

Media Compositions

The composition of the YPD agar medium was as follows: D-glucose 20 gL-1, peptone 20 gL-1, yeast extract 10 gL-1, and agar 15 gL-1.

The composition of the YPD medium was as follows: D-glucose 20 gL-1, peptone 20 gL-1, and yeast extract 10 gL-1.

The composition of the ethanol fermentation medium was as follows: D-glucose monohydrate 100 gL-1, peptone 20 gL-1, and yeast extract 10 gL-1.

Each medium was autoclaved at 121°C for 20 minutes after the suitable amount of BMIMCl was added to a given concentration.

Ethanol Fermentation

In a 250 ml glass bottle, 96 ml ethanol fermentation medium with a given BMIMCl concentration and 4 ml inoculum were added. Then the suspension in the bottle was intensively stirred. After that, 5 ml fermentation broth from the bottle was put into a 20 ml calorimetric ampule, the ampule was sealed and used for later microcalorimetric measurement. The bottle with the remaining 95 ml suspension was also sealed and used for the parallel ethanol fermentation. As the parallel experiment of microcalorimetric measurement, the bottle was placed into a thermostat at 30°C and kept ethanol fermentation under the same conditions as microcalorimetric measurements. During the fermentation process, small samples were taken at regular intervals for later analytical usage.

Microcalorimetric Measurement

A TAM Air isothermal microcalorimeter (Thermometric AB, Sweden), which was a multichannel microcalorimetric system, was used to record the heat flow rate of the ethanol fermentation process, which was calibrated by the release of electrical energy in a resistor and the heat effect of the sample ampoule. The heat power detection limit is stated to be ±2μW. The detailed structure and operation of the instrument have been described previously [14Yao J, Liu Y, Tuo Y, et al. Studies on the growth metabolism of Bacillus thuringiensis and its vegetative insecticidal protein engineered strains by microcalorimetry. Prikl Biokhim Mikrobiol 2006; 42(3): 310-4.
[PMID: 16878547]
]. All microcalorimetric experiments were performed at 30°C using the ampule method. The 20 ml sealed ampules with 5 ml ethanol fermentation broth, which were prepared as described above, were used for these microcalorimetric measurements. The power time curves of the ethanol fermentation process were recorded by a computer.

Analytical Methods

The samples taken from the ethanol fermentation process were used to determine the concentration of yeast, ethanol and the fermentable sugars. Yeast concentration was determined by the dry weight method [7Zhu S, Yu P, Lei M, et al. Investigation of the toxicity of the ionic liquid 1-butyl-3-methylimidazolium chloride to Saccharomyces cerevisiae AY93161 for lignocellulosic ethanol production. Polish J Chem Technol 2013; 15: 94-8.
[http://dx.doi.org/10.2478/pjct-2013-0029]
]. Ethanol content was determined by gas chromatography [15Zhu S, Wu Y, Yu Z, et al. Fed-batch simultaneous saccharification and fermentation of microwave/acid/alkali/H2O2 pretreated rice straw for production of ethanol. Chem Eng Commun 2006; 193: 639-48.
[http://dx.doi.org/10.1080/00986440500351966]
] and the fermentable sugars concentration was estimated using the 3,5-dinitrosalicylic acid method [16Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 1959; 31: 420-8.
[http://dx.doi.org/10.1021/ac60147a030]
].

RESULTS AND DISCUSSION

Effect of BMIMCl on the Ethanol Fermentation Process

The BMIMCl inhibits yeast growth and has a negative effect on ethanol production [7Zhu S, Yu P, Lei M, et al. Investigation of the toxicity of the ionic liquid 1-butyl-3-methylimidazolium chloride to Saccharomyces cerevisiae AY93161 for lignocellulosic ethanol production. Polish J Chem Technol 2013; 15: 94-8.
[http://dx.doi.org/10.2478/pjct-2013-0029]
, 8Zhu S, Yu P, Tong Y, et al. Effects of the ionic liquid 1-butyl-3-methylimidazolium chloride on the growth and ethanol fermentation of Saccharomyces cerevisiae AY92022. Chem Biochem Eng Q 2012; 26: 105-9.]. Under different fermentation conditions, the BMIMCl has a different influencing degree on the ethanol fermentation process [7Zhu S, Yu P, Lei M, et al. Investigation of the toxicity of the ionic liquid 1-butyl-3-methylimidazolium chloride to Saccharomyces cerevisiae AY93161 for lignocellulosic ethanol production. Polish J Chem Technol 2013; 15: 94-8.
[http://dx.doi.org/10.2478/pjct-2013-0029]
, 8Zhu S, Yu P, Tong Y, et al. Effects of the ionic liquid 1-butyl-3-methylimidazolium chloride on the growth and ethanol fermentation of Saccharomyces cerevisiae AY92022. Chem Biochem Eng Q 2012; 26: 105-9.]. In order to have a correct understanding on microcalorimetric data, the ethanol fermentation was carried out under the same conditions as the microcalorimetric measurement in this work. The time courses of yeast growth, ethanol production and the fermentable sugars consumption at different BMIMCl concentrations for ethanol fermentation process are shown in Fig. (1). As shown in Fig. (1), the ethanol fermentation had the characteristics of the typical batch fermentation process at all BMIMCl concentrations. The yeast growth during ethanol fermentation process consisted of four different periods: the lag phase, the log growth phase, the late log growth phase, and the stationary phase. Compared with the control, the lag and log growth phase cost almost the same time at all BMIMCl concentrations, but the time of the late log growth phase and the integral fermentation time were extended with increase of BMIMCl concentration. When the BMIMCl concentration was 0, 0.001, 0.01 and 1 gL-1, the yeast reached its highest concentration at 21, 27, 30, 33 and 36 h, and the produced ethanol arrived at its highest concentration at 27, 30, 33, 36 and 39 h respectively. When the BMIMCl concentration was 5 gL-1, the yeast and ethanol concentration was slowly increased at 42 h. Table 1 lists some important ethanol fermentation process data at different BMIMCl concentrations. As indicated in Table 1, when the BMIMCl concentration increased from 0 to 1 gL-1, the final yeast and ethanol concentration, the ethanol yield from the fermentable sugars (Yp/s) and the maximum yeast specific growth rate (µm) all decreased, but the final fermentable sugars concentration and the average specific ethanol productivity of yeast (E) was slightly increased. All these results suggest that the negative effect of BMIMCl on ethanol production came from its inhibition on yeast growth. This is consistent with our previous studies [7Zhu S, Yu P, Lei M, et al. Investigation of the toxicity of the ionic liquid 1-butyl-3-methylimidazolium chloride to Saccharomyces cerevisiae AY93161 for lignocellulosic ethanol production. Polish J Chem Technol 2013; 15: 94-8.
[http://dx.doi.org/10.2478/pjct-2013-0029]
, 8Zhu S, Yu P, Tong Y, et al. Effects of the ionic liquid 1-butyl-3-methylimidazolium chloride on the growth and ethanol fermentation of Saccharomyces cerevisiae AY92022. Chem Biochem Eng Q 2012; 26: 105-9.]. From Fig. (1) and Table 1, it is also found that the BMIMCl severely inhibited yeast growth and ethanol formation when its concentration reached 5 gL-1. Its final yeast and ethanol concentration was much lower than that when the BMIMCl concentration was 1 gL-1. It implies that high BMIMC1 concentrations may cause a change in the yeast metabolism. This is consistent with the previous studies that ionic liquids could shift yeast metabolism from respiration to fermentation and damage mitochondrial function by inducing hyperpolarization of the mitochondrial membrane [10Mehmood N, Husson E, Jacquard C, et al. Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae: metabolic, physiologic, and morphological investigations. Biotechnol Biofuels 2015; 8: 17.
[http://dx.doi.org/10.1186/s13068-015-0206-2] [PMID: 25688291]
, 11Dickinson Q, Bottoms S, Hinchman L, et al. Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain. Microb Cell Fact 2016; 15: 17.
[http://dx.doi.org/10.1186/s12934-016-0417-7] [PMID: 26790958]
].

Thermokinetic Analysis on the Ethanol Fermentation Process at Different BMIMCl Concentrations

Ethanol fermentation is a biological process which converts the fermentable sugars to ethanol and, at the same time, produces large amounts of heat. Microcalorimetry can easily record the thermogenic power-time curves of the ethanol

Fig. (1)
Time courses of ethanol fermentation process at different BMIMCl concentrations.


Table 1
Effect of BMIMCl concentration on ethanol fermentation process data and thermokinetic parameters.


fermentation process. The power-time curves can provide considerable kinetic and thermodynamic information about the ethanol fermentation process that is unavailable in other methods. The power-time curves of the ethanol fermentation process at different BMIMCl concentrations are shown in Fig. (2). From these power-time curves, it is found that the heat output of ethanol fermentation process at all BMIMCl concentrations included four different periods: the slow heat producing phase, the log heat producing phase, the stationary heat producing phase, and the declining heat producing phase. The slow and log heat producing heat phase was in good agreement with the lag and log growth phase during the ethanol fermentation process in the parallel experiments, and the stationary and declining heat producing phase was corresponding to the late log growth and the stationary phase. As shown in Fig. (2), for all BMIMCl concentrations, the heat producing power reached the maximum almost at the same time, but the integral fermentation time was extended with the BMIMCl concentration increasing. Based on the microcalorimetric measurement, some important thermokinetic parameters of ethanol fermentation process at different BMIMCl concentrations could be obtained and were listed in Table 1. As indicated in Table 1, the time of the maximum producing heat power (Tm) at all BMIMCl concentrations was almost simultaneous, and at Tm, the yeast and ethanol concentration decreased, but the maximum specific producing heat power (pm) increased with the BMIMCl concentration increasing, which led to the maximum producing heat power (Pm) decreased at the BMIMCl concentration from 0 to 0.1 gL-1, but it increased at the BMIMCl concentration from 0.1 to 5 gL-1. The producing heat power constant (K) at a given BMIMCl concentration was calculated as described by Braissant et al. [12Braissant O, Bonkat G, Wirz D, Bachmann A. Microbial growth and isothermal microcalorimetry: growth models and their application to microcalorimetric data. Thermochim Acta 2013; 555: 64-71.
[http://dx.doi.org/10.1016/j.tca.2012.12.005]
], but it was not equal to the µm, which indicated the specific producing heat power changed during the ethanol fermentation process. The heat output for log phase (Qlog) and the total heat output for the integral ethanol fermentation process (Qtotal) could be obtained from the power-time curves as described by Yao et al. [14Yao J, Liu Y, Tuo Y, et al. Studies on the growth metabolism of Bacillus thuringiensis and its vegetative insecticidal protein engineered strains by microcalorimetry. Prikl Biokhim Mikrobiol 2006; 42(3): 310-4.
[PMID: 16878547]
]. Based on the Qlog and Qtotal, the heat output for yeast concentration increasing 1 gL-1 (Hy) and the heat output for ethanol concentration increasing 1 gL-1 (HE) could be easily calculated. The HE was the same for all BMIMCl concentrations, but the Hy increased with the BMIMCl concentration increasing, which caused the increase in the total heat output for producing 1 g ethanol (H) when the BMIMCl concentration increases. It is noteworthy that Hy and H were much higher at BMIMCl concentration 5 gL-1 than 1 gL-1. This gave another evidence that high BMIMCl concentration might cause a change in the yeast metabolism. Some previous studies have indicated the BMIMCl inhibited yeast growth because of its interaction with the yeast mitochondrial membrane protein [7Zhu S, Yu P, Lei M, et al. Investigation of the toxicity of the ionic liquid 1-butyl-3-methylimidazolium chloride to Saccharomyces cerevisiae AY93161 for lignocellulosic ethanol production. Polish J Chem Technol 2013; 15: 94-8.
[http://dx.doi.org/10.2478/pjct-2013-0029]
, 8Zhu S, Yu P, Tong Y, et al. Effects of the ionic liquid 1-butyl-3-methylimidazolium chloride on the growth and ethanol fermentation of Saccharomyces cerevisiae AY92022. Chem Biochem Eng Q 2012; 26: 105-9., 10Mehmood N, Husson E, Jacquard C, et al. Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae: metabolic, physiologic, and morphological investigations. Biotechnol Biofuels 2015; 8: 17.
[http://dx.doi.org/10.1186/s13068-015-0206-2] [PMID: 25688291]
, 11Dickinson Q, Bottoms S, Hinchman L, et al. Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain. Microb Cell Fact 2016; 15: 17.
[http://dx.doi.org/10.1186/s12934-016-0417-7] [PMID: 26790958]
]. This interaction could lead to more heat output for yeast growth and maintenance, which might be the reason why H increases with the BMIMCl concentration increasing. Base on the above analysis, the possible influencing mechanism of the BMIMCl on ethanol fermentation process was the interaction between the BMIMCl and the yeast mitochondrial membrane protein inhibited yeast growth [10Mehmood N, Husson E, Jacquard C, et al. Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae: metabolic, physiologic, and morphological investigations. Biotechnol Biofuels 2015; 8: 17.
[http://dx.doi.org/10.1186/s13068-015-0206-2] [PMID: 25688291]
, 11Dickinson Q, Bottoms S, Hinchman L, et al. Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain. Microb Cell Fact 2016; 15: 17.
[http://dx.doi.org/10.1186/s12934-016-0417-7] [PMID: 26790958]
, 17Zhu S, Wu Y, Chen Q, Chi R, Shen X, Yu Z. A mini-review on greenness of ionic liquids. Chem Biochem Eng Q 2009; 23: 207-11., 18Zhao D, Liao Y, Zhang Z. Toxicity of ionic liquids. Clean-Soil Air Water 2007; 35: 42-8.], more fermentable sugars were consumed for yeast growth and maintenance, which led to lower final yeast and ethanol concentration, lower ethanol yield from the fermentable sugars and longer fermentation time. It also caused that the H increases with the BMIMCl concentration increasing. These results indicate that residual concentrations of ionic liquids affect the fermenting yeast cell metabolism and its thermokinetics, hence strategies to reduce their effects on the biocatalyst are required for optimizing product yields using the ionic liquid technology.

Fig. (2)
Power-time curves of ethanol fermentation process at different BMIMCl concentrations.


CONCLUSION

The negative effects of BMIMCl on the ethanol fermentation process of Saccharomyces cerevisiae AY93161 were investigated via microcalorimetry, and its metabolic regulation mechanism was analyzed based on its thermokinetic data. The BMIMCl decreased µm and increased pm and H, which caused lower final yeast and ethanol concentration. This provides useful information for the improvement of the lignocellulosic ethanol production process by using the ionic liquid technology.

CONFLICT OF INTEREST

The authors confirm that this article content has no conflict of interest.

ACKNOWLEDGEMENTS

This work was supported by the National Natural science Foundation of China No.21176196, Graduate Innovative Fund of Wuhan Institute of Technology CX2015077, Key Laboratory for Green Chemical Process of Ministry of Education GCP201501 and Hubei Key Laboratory of Novel Chemical Reactor and Green Chemical Technology NRGCT201501.

REFERENCES

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[2] Zhu S, Wang K, Huang W, et al. Acid catalyzed hydrolysis of lignocellulosic biomass in ionic liquids for ethanol production: opportunities & challenges. BioResources 2016; 11: 3-5.
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[7] Zhu S, Yu P, Lei M, et al. Investigation of the toxicity of the ionic liquid 1-butyl-3-methylimidazolium chloride to Saccharomyces cerevisiae AY93161 for lignocellulosic ethanol production. Polish J Chem Technol 2013; 15: 94-8.
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[9] Ouellet M, Datta S, Dibble DC, et al. Impact of ionic liquid pretreated plant biomass on Saccharomyces cerevisiae growth and biofuel production. Green Chem 2011; 13: 2743-9.
[http://dx.doi.org/10.1039/c1gc15327g]
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[http://dx.doi.org/10.1186/s13068-015-0206-2] [PMID: 25688291]
[11] Dickinson Q, Bottoms S, Hinchman L, et al. Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain. Microb Cell Fact 2016; 15: 17.
[http://dx.doi.org/10.1186/s12934-016-0417-7] [PMID: 26790958]
[12] Braissant O, Bonkat G, Wirz D, Bachmann A. Microbial growth and isothermal microcalorimetry: growth models and their application to microcalorimetric data. Thermochim Acta 2013; 555: 64-71.
[http://dx.doi.org/10.1016/j.tca.2012.12.005]
[13] Kabanova N, Kazarjan A, Stulova I, Vilu R. Microcalorimetric study of growth of lactococcus lactis IL 1403 at different glucose concentrations in broth. Thermochim Acta 2009; 496: 87-92.
[http://dx.doi.org/10.1016/j.tca.2009.07.003]
[14] Yao J, Liu Y, Tuo Y, et al. Studies on the growth metabolism of Bacillus thuringiensis and its vegetative insecticidal protein engineered strains by microcalorimetry. Prikl Biokhim Mikrobiol 2006; 42(3): 310-4.
[PMID: 16878547]
[15] Zhu S, Wu Y, Yu Z, et al. Fed-batch simultaneous saccharification and fermentation of microwave/acid/alkali/H2O2 pretreated rice straw for production of ethanol. Chem Eng Commun 2006; 193: 639-48.
[http://dx.doi.org/10.1080/00986440500351966]
[16] Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 1959; 31: 420-8.
[http://dx.doi.org/10.1021/ac60147a030]
[17] Zhu S, Wu Y, Chen Q, Chi R, Shen X, Yu Z. A mini-review on greenness of ionic liquids. Chem Biochem Eng Q 2009; 23: 207-11.
[18] Zhao D, Liao Y, Zhang Z. Toxicity of ionic liquids. Clean-Soil Air Water 2007; 35: 42-8.
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Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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