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Effects of Ultrasound on Fermentation of Glucose to Ethanol by Saccharomyces Cerevisiae

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Effects of Ultrasound on Fermentation of Glucose to Ethanol by Saccharomyces Cerevisiae fermentation Article Effects of Ultrasound on Fermentation of Glucose to Ethanol by Saccharomyces cerevisiae Luis Huezo, Ajay Shah and Frederick C. Michel Jr. * Department of Food, Agricultural, and Biological Engineering, The Ohio State University; 1680 Madison Ave., Wooster, OH 44691, USA; [email protected] (L.H.); [email protected] (A.S.) * Correspondence: [email protected]; Tel.: +330-263-3859 Received: 31 December 2018; Accepted: 27 January 2019; Published: 29 January 2019 Abstract: Previous studies have shown that pretreatment of corn slurries using ultrasound improves starch release and ethanol yield during biofuel production. However, studies on its effects on the mass transfer of substrates and products during fermentation have shown that it can have both beneficial and inhibitory effects. In this study, the effects of ultrasound on mass transfer limitations during fermentation were examined. Calculation of the external and intraparticle observable moduli under a range of conditions indicate that no external or intraparticle mass transfer limitations should exist for the mass transfer of glucose, ethanol, or carbon dioxide. Fermentations of glucose to ethanol using Saccharomyces cerevisiae were conducted at different ultrasound intensities to examine its effects on glucose uptake, ethanol production, and yeast population and viability. Four treatments were compared: direct ultrasound at intensities of 23 and 32 W/L, indirect ultrasound (1.4 W/L), and no-ultrasound. Direct and indirect ultrasound had negative effects on yeast performance and viability, and reduced the rates of glucose uptake and ethanol production. These results indicate that ultrasound during fermentation, at the levels applied, is inhibitory and not expected to improve mass transfer limitations. Keywords: ultrasound; fermentation; glucose; ethanol; yeast; Saccharomyces cerevisiae; mass transfer 1. Introduction Ethanol is the principal biofuel used in the United States, with 15,800 million gallons produced in 2017. This represents 58% of the total biofuel ethanol produced globally [1]. Ethanol fermentation is accomplished using industrial strains of the yeast Saccharomyces cerevisiae, which are used due to their fast growth rate, high conversion efficiency, low byproduct production, and tolerance to high ethanol concentrations [2,3]. Various methods to improve biofuel ethanol production have been studied. These include genetic enhancements to increase the range of utilizable substrates [4]; as well as pretreatments, such as hydrodynamic cavitation to improve starch release [5,6] and enzyme additions to hydrolyze cellulose [6]. Another potential method to enhance ethanol production is ultrasound treatment, which could improve the mass transfer of substrates to, and products away from, yeast cells during fermentation. Ultrasound is defined as sound waves with frequencies above 20 kHz. Human hearing range is between 20 to 20,000 Hertz (20 kHz). Ultrasound can be applied directly or indirectly. Direct application of ultrasound (probe ultrasound) refers to direct application to the sample medium. Indirect application (bath ultrasound) refers to the application of ultrasound into a secondary medium (e.g., water bath). Direct ultrasound is usually applied with an ultrasonic probe and has a high localized intensity compared to bath ultrasound. Indirect ultrasound can be used to process larger volumes of solution at a more consistent intensity [7]. Fermentation 2019, 5, 16; doi:10.3390/fermentation5010016 www.mdpi.com/journal/fermentation Fermentation 2019, 5, 16 2 of 14 Ultrasound generates alternating high- and low-pressures, causing compression and rarefaction cycles in the medium. Rarefaction leads to the formation of cavities, which implode during compression [8,9]. This is a function of the frequency and the amplitude of the oscillations. The sudden drop in pressure creates vacuum bubbles or cavities. This is followed by a rapid return to the original pressure, which causes the cavities to collapse, releasing energy, which is then transferred to the medium [9]. The intensity of cavitation creates high local temperatures and powerful pressures for brief periods of time [8]. This could potentially have beneficial effects on mass transfer. Ultrasound has been used in bioprocessing for different purposes and with different types of equipment and methods of application. It has been used in feedstock pretreatment for de-agglomeration, particle size reduction, dispersion [6,10–15], particle separation [16], and corn ethanol and wastewater treatment processes [17,18]. It has also been used to disrupt cells [19–24] and cell membranes, allowing the recovery of intracellular components [25,26] and for the inactivation of microbes [27,28]. A few studies have focused on the benefits of ultrasound during fermentation. Improvements were found due to enhanced mixing, cell deagglomeration, and facilitating the release of CO2 from the medium, lowering its concentration [23,29–34]. Another mechanism by which ultrasound may impact ethanol fermentation is by reducing mass transfer limitations for glucose, ethanol, and carbon dioxide in the vicinity of yeast cells [35,36]. Mass transfer limitations may limit the rate of fermentation by reducing glucose concentration at the cell surface. High concentrations of ethanol and carbon dioxide close to the cell could also modify cell membranes and inhibit fermentation rates. Intraparticle and external mass transfer resistances related to porous catalysts, immobilized cell systems, and fungal pellets have all been shown to limit the rates of fermentation and bioconversion [37]. By applying ultrasound during fermentation, a greater rate of ethanol production may occur due to higher rates of glucose uptake, a decrease in the concentration of ethanol and CO2 at the cell surface, and a greater rate of release from the medium. The purpose of this study was to evaluate the effects of ultrasound in improving these mass transfer limitations during ethanol fermentation from glucose. The hypothesis of the study was that ultrasound enhances the performance of Saccharomyces cerevisiae by interfering with the boundary layer at the cell surface and reducing mass transfer limitations for glucose, ethanol, and carbon dioxide. The external and intraparticle mass transfer resistances were first calculated for a range of conditions to determine whether these limitations may be significant. Then the effects of ultrasound were determined during fermentation by measuring glucose uptake, ethanol production, and yeast cell population and viability over a range of direct and indirect ultrasound intensities. 2. Materials and Methods 2.1. Inoculum and Medium Preparation The inoculum used for fermentation was prepared based on methods described in Ramirez [6], Dowe and McMillan [38], and Montalbo-Lomboy [39]. Yeast extract and peptone (YP) 10× were prepared by mixing 100 g of yeast extract and 200 g of peptone into double-deionized water (DDIW), to a total volume of 1 L. This solution was autoclaved at 121 ◦C for 30 min and used as a stock solution for media preparation. Glucose solution (50%) was prepared by diluting 500 g of glucose in DDIW to a total volume of 1 L. YP-glucose (5%) was prepared by mixing 100 mL of YP 10× and 100 mL of 50% glucose solution in 800 mL of DDIW. Citrate buffer (pH 4.5, 1 M) was prepared by adding 192 g of anhydrous citric acid to DDIW to a total volume of 1 L; the solution was titrated to a pH of 4.3 with a solution of sodium hydroxide 10 M (NaOH). The yeast pre-culture media was prepared by mixing 1 L of YP-glucose 5%, 100 mL of citrate buffer, and adding 3.07 g of magnesium sulfate heptahydrate (MgSO4·7H2O), 1.80 g of potassium phosphate monobasic (KH2PO4), 4.87 g of sodium phosphate monohydrate (Na2HPO4·H2O), 0.32 g of zinc sulfate heptahydrate (ZnSO4·7H2O), and DDIW to a total volume of 1.5 L. To this, 1.0 g of dried Saccharomyces cerevisiae (Bio-Ferm XR, North Fermentation 2019, 5, x 3 of 14 Fermentation 2019, 5, 16 3 of 14 DDIW to a total volume of 1.5 L. To this, 1.0 g of dried Saccharomyces cerevisiae (Bio-Ferm XR, North American Bioproducts Corporation) was added. The yeast inoculum was incubated at 32 °C, 180 Americanrpm for 19 Bioproducts h in a shaker Corporation) (InnovaTM was 2300, added. Platform The yeast shaker, inoculum New was Brunswick) incubated to at 32a viable◦C, 180 yeast rpm concentrationfor 19 h in a shaker of ~1×10 (InnovaTM8 cells/mL. 2300, Platform shaker, New Brunswick) to a viable yeast concentration of ~1 × 108 cells/mL. 2.2. Fermentation 2.2. Fermentation Glucose was used as the sole carbon substrate to eliminate the effects of ultrasound on starch release.Glucose Fermentations was used for as theall treatments sole carbon were substrate conducted to eliminate in autoclaved the effects 125 of mL ultrasound Erlenmeyer on starchflasks (totalrelease. volume Fermentations 155 mL). forFermentation all treatments medium were consis conductedted of in 112.5 autoclaved mL of gluc 125ose mL solution Erlenmeyer (200 flasksg/L), 6.25(total mL volume YP 10×, 155 and mL). 6.25 Fermentation mL of yeast inoculum, medium consistedfor a total ofvolume 112.5 mLof 125 of mL. glucose Flasks solution were sealed (200 g/L), and a6.25 syringe mL YP needle 10×, andwas 6.25inserted mL ofthrough yeast inoculum,the stopper for to a totalvent volumeCO2. All of treatments 125 mL. Flasks were wereplaced sealed in a water-bath-shakerand a syringe needle (Model was insertedG76D, Gyrotory through® the, New stopper Brunswick to vent Scientific CO2. All Co. treatments Inc. NJ, wereUSA) placed in a 32 in °C a water-bath-shakerwarm room. (Model G76D, Gyrotory®, New Brunswick Scientific Co. Inc., Edison, NJ, USA) in a 32 ◦C warm room. 2.3. Ultrasound 2.3. Ultrasound The ultrasound equipment (Sonics® & Materials, Inc. CT, U.S.A) used included a vibracell ® controlThe panel ultrasound operating equipment at 750 W, (Sonicsa converter& Materials,(Model CV33), Inc., and Newtown, a probe (13 CT, mm USA) diameter, used included threaded a end)vibracell (Figure control 1 a,b).
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