Bermuda grass as feedstock for biofuel production: A review

Bioresource Technology 102 (2011) 7613–7620

Contents lists available at ScienceDirect

Bioresource Technology journal homepage: www.elsevier.com/locate/biortech

Review

Bermuda grass as feedstock for biofuel production: A review Jiele Xu, Ziyu Wang, Jay J. Cheng ⇑ Department of Biological and Agricultural Engineering, Campus Box 7625, North Carolina State University, Raleigh, NC 27695, USA

a r t i c l e

i n f o

Article history: Received 29 March 2011 Received in revised form 24 May 2011 Accepted 25 May 2011 Available online 30 May 2011 Keywords: Bermuda grass Enzymatic hydrolysis Ethanol Fermentation Pretreatment

a b s t r a c t Bermuda grass is a promising feedstock for the production of fuel ethanol in the Southern United States. This paper presents a review of the significant amount of research on the conversion of Bermuda grass to ethanol and a brief discussion on the factors affecting the biomass production in the field. The biggest challenge of biomass conversion comes from the recalcitrance of lignocellulose. A variety of chemical, physico-chemical, and biological pretreatment methods have been investigated to improve the digestibility of Bermuda grass with encouraging results reported. The subsequent enzymatic hydrolysis and fermentation steps have also been extensively studied and effectively optimized. It is expected that the development of genetic engineering technologies for the grass and fermenting organisms has the potential to greatly improve the economic viability of Bermuda grass-based fuel ethanol production systems. Other energy applications of Bermuda grass include anaerobic digestion for biogas generation and pyrolysis for syngas production. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction The world’s ever-increasing demand for energy, inevitable depletion of fossil fuels, and growing concerns over global warming have stimulated the exploration for alternative energy sources. In the US, ethanol is a promising alternative fuel and has been widely used in the transportation sector as a partial gasoline replacement to reduce petroleum usage and tailpipe emissions. Corn is currently the predominant feedstock for ethanol production in the US. However, corn-based ethanol production is not economically or environmentally sustainable because it not only competes with food and feed production for limited agricultural land, but has also been associated with some substantial environmental problems such as nutrient pollution and soil erosion resulted from corn cultivation (Sun and Cheng, 2002; Pimentel et al., 2003). Lignocellulose-to-ethanol conversion is regarded as a sustainable technology to supplement corn-based ethanol production due to the abundance of lignocellulosic biomass and diverse raw materials available. To improve the projected economic performance of ethanol production, the development of a local ethanol industry should be based on the specific types of biomass that are cheap and widely available in the region. In the Southern United States, Bermuda grass, a popular forage crop, is a competitive feedstock due to the existing cropping systems and established market. Growers have vast experience in the production and transport of millions of tons of Bermuda grass every

⇑ Corresponding author. Tel.: +1 919 515 6733; fax: +1 919 515 7760. E-mail address: [email protected] (J.J. Cheng). 0960-8524/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2011.05.070

year (Anderson et al., 2010). Bermuda grass is also grown in the region to remove the nutrients from animal wastes to prevent potential nutrient pollution to surface and ground waters. The harvested Bermuda grass is normally sold at a very low price as animal feed or given away in some cases (Sun and Cheng, 2005), making it an ideal feedstock for ethanol production. Compared with corn, Bermuda grass has a greater ethanol yield potential due to its excellent biomass production and the conversion of the whole carbohydrate-rich plant to ethanol. In addition, Bermuda grass has the benefit of having preexisting cultivars specifically bred for increased rumen digestibility, which also favors its conversion for energy purposes (Anderson et al., 2008). Bermuda grass (Cynodon dactylon) is a warm-season C4 perennial grass grown and used extensively as a ruminant feed in tropical and subtropical regions (Ball et al., 1991). It has short greygreen blades with rough edges, erect stems of 1–30 cm in length, and a deep root system that can penetrate 2 m into the ground, though most of the root mass is less than 60 cm under the ground surface (Ravindra, 2003). Although some Bermuda grass species grow to a height of 15–20 cm, others can grow as tall as 1 m or more (Taliaferro et al., 2004). Bermuda grass occurs naturally in North Africa, Asia, Australia and southern Europe (Mohamed Shabi et al., 2010), and was first introduced to the United States from Africa in 1751 (Hanson, 1972). Because of its excellent yield, increased rumen digestibility, persistence, and moderate nitrogen requirement for optimum production, Bermuda grass of various cultivars is currently covering over 4 million hectares (10 million acres) of land in the Southern United States for hay and forage (Boateng et al., 2007). Historically, it was after the development and release of the coastal Bermuda grass genotype in 1943 that

7614

J. Xu et al. / Bioresource Technology 102 (2011) 7613–7620

the planting of Bermuda grass as a forage began. Since then, other improved hybrids have been released. ‘Tifton 85’, the most recent genotype, was reported to yield 20% higher biomass and 10% more digestible than coastal Bermuda grass (Boateng et al., 2007). Since Bermuda grass has greater nutrient removal ability, many hog farmers in the southern US, where confined and contract swine production is rapidly growing, integrate Bermuda grass cultivation into wastewater management systems to prevent nutrient pollution to the environment (Sun and Cheng, 2005). Solid wastes such as broiler litter and dairy manure are also disposed on Bermuda grass fields for both nutrient management and biomass production (Muir et al., 2010a; Brink et al., 2002). Although Bermuda grass is a promising feedstock for ethanol production, especially in the Southern US, a review of the significant amount of studies that have been conducted regarding the conversion of Bermuda grass to fuel ethanol has not been presented to date. It is necessary that the results from previous studies be summarized, compared, and analyzed to identify the challenges in research and development and to reveal potential directions for future research. The objective of this paper, therefore, is to critically review the research on Bermuda grass-to-ethanol conversion and some other energy applications. In addition, a brief discussion on the agricultural management practice that significantly affects the yield of Bermuda grass biomass is also included in this paper.

2. Biomass production Bermuda grass dry matter yields of 6 to 27 t ha 1 yr 1 have been reported, depending on Bermuda grass cultivars and growing conditions (Muir et al., 2010b; Holtzapple et al., 1994; Hill et al., 1993). Since biomass yield, which is directly proportional to the ethanol yield from Bermuda grass, is strongly influenced by cultivar (Brink et al., 2003), comparative studies have been conducted among various Bermuda grass cultivars to investigate their responses to different cultivation practices. Hill et al. (1993) studied the dry matter yields of ‘Tifton 85’, ‘Tifton 68’, ‘Tifton 44’, and ‘Coastal’ Bermuda grass in two small-plot experiments using fertilizer, and found that ‘Tifton 85’ produced 18.5–41.3% more biomass than the other three hybrids in addition to the improved digestibility. Brink et al. (2003) compared the yields of ‘Alicia’, ‘Brazos’, ‘Coastal’, ‘Russell’, ‘Tifton 44’, and ‘Tifton 85’ hybrid Bermuda grass and common Bermuda grass cultivated using swine effluent at two sites under contrasting growing conditions. The results show that, at both sites, annual dry matter yields of ‘Brazos’, ‘Coastal’, ‘Russell’, and ‘Tifton 85’ were similarly high, respectively reaching 23.3–24.2 t ha 1 and 12.3–14.1 t ha 1. In another study, Sistani et al. (2004) reported that, using broiler litter as nutrient source, annual dry matter yields of ‘Coastal’ and ‘Tifton 85’, respectively, reached 16.9 t ha 1 and 18.8 t ha 1, which were 51% and 67% higher than that of common Bermuda grass, respectively. Muir et al. (2010b) reported that coastal Bermuda grass accumulated biomass earlier but ended growing seasons with dry matter yield comparable to ‘Tifton 85’. Growing conditions such as temperature, precipitation, and soil type, and agricultural management practices such as fertilization and harvest also have substantial impacts on Bermuda grass yield. Bermuda grass growth begins at temperatures above 15 °C, with optimum growth between 24 to 37 °C (Mohamed Shabi et al., 2010). In a controlled environment, dry matter yields of coastal Bermuda grass were substantially higher at the 40 °C/30 °C (day/night) temperature regime for both well-watered and water-stressed treatments than at the 30 °C/20 °C temperature regime (Bade et al., 1985). Although Bermuda grass is well known for its drought tolerance, adequate rainfall leads to higher biomass yields. Muir et al. (2010b) reported that the peak yield of coastal Bermuda grass was

about 6.1 t ha 1 yr 1 during a growing season with 459 mm rainfall but ranged from 10.3 to 11.2 t ha 1 yr 1 during a growing season with 845 mm rainfall. Brink et al. (2003) compared the yields of Bermuda grass at two sites of different climatic conditions and suggested that the reduced precipitation was one of the reasons that contributed to the lower yield in one location. Soil property can be another important factor that causes the variation in biomass yield of Bermuda grass at different geographic locations (Adeli et al., 2006). A greenhouse study was conducted by Adeli et al. (2006) to determine the effects of three soil types (Leeper clay loam, Ruston sandy loam, and Marietta silt loam) on the response of ‘Russell’ Bermuda grass to broiler litter applications. The results show that the dry matter yields of Bermuda grass (2.6–6.8 t ha 1 yr 1) decreased in the order of Ruston > Leeper > Marietta, and the dry matter yields in all soils were much lower than that reported for Bermuda grass fertilized with similar loadings of broiler litter on a Savannah sandy loam (12.5–16.5 Mg ha 1 yr 1) (Brink et al., 2002). The different responses to soils could probably be related to soil properties such as soil pH and ammonium fixation capability. Bermuda grass responses readily to increasing nitrogen rates from either inorganic or organic sources (Overman et al., 1993). The yield of Bermuda grass increased from 1.2 to 16.6 t ha 1 yr 1 as the amount of nitrogen applied was increased from 0 to 448 kg ha 1 (0 to 400 lb acre 1) (Mueller et al., 1993). Wilkinson and Langdale (1974) reported that Bermuda grass yield response to nitrogen was linear up to 560 kg N ha 1. Liu et al. (1997) found that, with the nitrogen supply increased from 560 to 2240 kg ha 1 yr 1, a similar trend in Bermuda grass yield was observed, but the efficiencies of nitrogen and phosphorus utilization declined. Applying high nutrient loading, however, might result in the accumulation of nitrogen and phosphorus in the soil and, consequently, contribute to the ground and surface water pollution (Brink et al., 2003). Burns et al. (1985) reported that when 670 kg N ha 1 and 153 kg P ha 1 from swine effluent were received by coastal Bermuda grass, only a total of 382 kg N ha 1 and 43 kg P ha 1 was removed through plant utilization. Lee et al. (2002) recommended applying 84–112 kg N ha 1 (75 to 100 lb N acre 1) before the rapid growth of Bermuda grass begins in the spring and apply a similar quantity after each harvest except for the last harvest in the fall. Funderburg and Twidwell (2000) recommended 224–336 kg N ha 1 (200 to 300 lb N acre 1) for common Bermuda grass and 336– 448 kg N ha 1 (300 to 400 lb N acre 1) for hybrid Bermuda grass in split applications with no more than 112 kg N ha 1 (100 lb N acre 1) applied at any one time. When using animal waste as nutrient source for Bermuda grass cultivation, the buildup of soil phosphorus is normally observed due to the difference in N/P ratio between animal waste and plant requirement. It was reported that adding extra nitrogen would help the removal of phosphorus from the soil (Evers, 2002). Bermuda grass harvest has also been studied for improved biomass production. Prine and Burton (1956) reported that a clipping interval of six to eight weeks maximized the dry matter yield of coastal Bermuda grass in Tifton, GA. Overman et al. (1990) reported that coastal Bermuda grass had reduced dry matter accumulation beyond 6-week interval of growth because of death or drop off of lower plant leaves. However, Bermuda grass yields that reported for forage trials may not be appropriate for biomass-harvest regimens because biomass harvest for energy purposes targets yield without regard to nutritive value (Muir et al., 2010b). Further investigations are required, therefore, to optimize the harvest interval to maximize total Bermuda grass yield for ethanol production.

3. Conversion of Bermuda grass to ethanol Bermuda grass not only has the advantages of excellent biomass yield and wide availability, but also contains high carbohydrate which is favorable for the cost-effective production of cellulosic

7615

J. Xu et al. / Bioresource Technology 102 (2011) 7613–7620 Table 1 Composition of Bermuda grass and other herbaceous biomass feedstocks. Component

Bermuda grass

Switchgrass

Corn stover

Wheat straw

Cotton stalk

Rye straw

Holocellulose Glucan Xylan Arabinan Galactan Mannan Total lignin Acid-insoluble lignin Acid-soluble lignin Extractives Ash Reference

59.7 30.4 22.6 4.9 1.8 0 23.2 18.8 4.4 5.5 4.8 Lee et al. (2009)

53.5 32.0 17.9 1.7 1.9 0 21.4 17.2 4.2 N/A 3.8 Xu et al. (2010a)

56.8 34.6 18.3 2.5 1.0 0.4 17.7 N/A N/A 7.7 10.2 NREL (2006)

55.3 32.6 19.2 2.4 0.8 0.3 16.9 N/A N/A 13.0 10.2 NREL (2006)

46.4 37.0 7.0 1.3 1.1 0 30.8 28.9 1.9 9 6.0 Shi (2007)

55.4 33.1 19.5 2.5 0.3 0 N/A 19.8 N/A N/A 6.2 Sun and Cheng (2005)

duce cellulose crystallinity, and increase the surface area of the material through physical, chemical, or biological methods. Effective pretreatments should not only substantially improve the accessibility of biomass by enzymes in the subsequent hydrolysis, but also avoid intensive carbohydrate loss or degradation during the process. Besides, cost is also an important criterion to evaluate the promise of any pretreatment techniques (Sun and Cheng, 2002). Pretreatment is believed to have great potential for efficiency improvement and cost lowering through research and development (Mosier et al., 2005), and a number of technologies have been investigated for the effective pretreatment of Bermuda grass.

Fig. 1. Conversion of lignocellulosic biomass to ethanol.

ethanol. Table 1 shows the composition of Bermuda grass and other commonly studied herbaceous biomass feedstocks. Although Bermuda grass is a very promising feedstock for ethanol production, like other lignocellulosic biomass, its conversion to ethanol is quite challenging. As Fig. 1 shows, three basic steps are involved in the conversion: (1) pretreatment of raw biomass, (2) enzymatic hydrolysis for fermentable sugar production, and (3) ethanol fermentation. The biggest challenge of conversion comes from the recalcitrance of lignocellulosic biomass. This recalcitrance is due to both the composition of lignocellulose and the way specific components interact with each other. Lignocellulosic materials consist of three major components: cellulose, hemicellulose, and lignin. Cellulose and hemicellulose are polysaccharides that can be used for ethanol production, while lignin is a complex aromatic polymer that stiffens and surrounds the fibers of polysaccharides. The extensive interactions between these three components render a recalcitrant structure of lignocellulose, which necessitates a pretreatment step to break it up, thus making cellulose and hemicellulose more accessible to hydrolytic enzymes for fermentable sugar production. Challenges in the subsequent hydrolysis and fermentation include high cost of hydrolytic enzymes (cellulases), substrate and product inhibition to enzymes, enzyme inactivity, pentose fermentation, and compounds inhibitory to fermentation in lignocellulosic hydrolysate. All these challenges need to be addressed before the potential of ethanol production from lignocellulosic biomass is fully realized.

3.1. Pretreatment processes The purpose of pretreatment is to improve the enzymatic digestibility of lignocellulose by removing lignin/hemicellulose, re-

3.1.1. Chemical pretreatment Acid and alkaline prehydrolysis are the two most intensively studied chemical methods in the pretreatment of lignocellulosic biomass. Acid pretreatment results in disruptions of covalent bonds, hydrogen bonds, and van der Waals forces that hold together the biomass components, which, consequently, causes solubilization of hemicellulose and reduction of cellulose crystallinity (Li et al., 2010). Rather than treating lignocellulose using concentrated acid, dilute acid pretreatments are normally practiced at high temperatures to improve cellulose hydrolysis. Dilute acid is also less toxic, hazardous, and corrosive to reactors (Sun and Cheng, 2002). To assess the potential of Bermuda grass for ethanol conversion, Anderson et al. (2008) used 1.75% (w/v) sulfuric acid to treat ‘Coastal’ Bermuda grass and ‘Tifton 85’ Bermuda grass at 121 °C for 1 h, and found the acid pretreatment resulted in great ethanol yields of 121.7–139.6 mg/g raw biomass. Sun and Cheng (2005) studied pretreatment of Bermuda grass at 121 °C under different sulfuric acid concentrations (0.6%, 0.9%, 1.2% and 1.5%, w/w) and residence times (30, 60, and 90 min), and reported that glucose and xylose in the prehydrolyzate increased with the increase of pretreatment severity, indicating improved solubilizations of cellulose and hemicellulose. The digestibility of the pretreated Bermuda grass also improved with the increase of pretreatment severity, reaching 83% when 1.5% sulfuric acid and 90 min of pretreatment time were applied. Based on the work of Sun and Cheng (2005), Redding et al. (2011) explored sulfuric acid pretreatment at higher temperatures to reduce the requirements for acid and residence time. After examining sulfuric acid concentrations of 0.3%, 0.6%, 0.9%, and 1.2% (w/w) at temperatures of 120, 140, 160, and 180 °C and residence times of 5, 15, 30, and 60 min, it was found that, with the increase of pretreatment severity, not only more hemicellulose and cellulose were solubilized, but furfural from hemicellulose degradation also increased in the prehydrolysate. Taking furfural inhibition into account, 1.2% acid at 140 °C for 30 min were recommended as the best pretreatment conditions, at which 97% of theoretical sugars were recovered from prehydrolysate and hydrolysate.

7616

J. Xu et al. / Bioresource Technology 102 (2011) 7613–7620

In contrast, alkaline pretreatment causes delignification of biomass and make the lignocellulose swollen through saponification reactions (Xu et al., 2010a). Unlike acid pretreatment, alkaline pretreatment has been proven effective within a wide temperature range at various chemical concentrations (Xu et al., 2010a,b). Sodium hydroxide (NaOH) and lime (Ca(OH)2) are the two alkaline reagents that have attracted most attention. Wang et al. (2010) studied pretreatment of coastal Bermuda grass using NaOH at concentrations from 0.5% to 3% (w/v) for a residence time from 15 to 90 min at 121 °C. It was observed that up to 86% lignin was removed during the pretreatment, and the removal rate generally increased with the increase of pretreatment severity. Hemicellulose solubilization was much more significant than that of cellulose because of the higher susceptibility of hemicellulose to alkaline attack. Based on total sugar production in the enzymatic hydrolysis, 0.75% NaOH and 15 min were recommended as the best pretreatment conditions, at which 71% of the theoretical recovery of reducing sugars was achieved in enzymatic hydrolysis. Lime pretreatment of Bermuda grass was examined within a wider temperature range of 50 to 121 °C, with the effects of residence time (15–60 min) and Ca(OH)2 loading (0.02–0.20 g/g raw biomass) determined (Wang, 2009). The results show that, compared with NaOH pretreatment, the delignification capability of lime was much lower, with only 10–20% of lignin removed. This can be the result of the fact that divalent calcium ions from Ca(OH)2 dissociation have high affinity for lignin and can effectively crosslink lignin molecules (Xu et al., 2010b), thus preventing them from solubilization under alkaline attack. Similar results were reported by Xu et al. (2010b) in the study of lime pretreatment of switchgrass. However, the digestibility improvement of Bermuda grass was not significantly effected. At the optimal conditions of 100 °C for 15 min with a lime loading of 0.1 g/g dry biomass, the production of total reducing sugars was 78% of the theoretical maximum, with 87.4% and 67.5% of glucan and xylan recovered in enzymatic hydrolysis, respectively. A plausible explanation is that, as long as the lignocellulosic structure of Bermuda grass is effectively broken up and biomass porosity substantially improved, enzymes can get good access to carbohydrates even in the presence of high lignin contents (Xu et al., 2010b). Other chemical techniques investigated include ozonolysis, phosphoric acid–acetone pretreatment, and enzyme pretreatment. Ozone pretreatment effectively removes lignin, slightly attacks hemicellulose, while hardly degrades cellulose (Sun and Cheng, 2002). It does not produce toxic byproducts that will be inhibitory to the downstream processes. Lee et al. (2010a) treated coastal Bermuda grass with ozone at room temperature and reported that, ozone removed significant amounts of lignin (31.3%) and hemicellulose (17.0%) from the raw biomass. With the increase of ozone consumption from 4.5% to 26.4%, the cellulose conversion increased from 30% to 53%. Another innovative pretreatment technology involves the application of the combination of a nonvolatile cellulose solvent (phosphoric acid) and a volatile organic solvent (acetone), which effectively separates the lignocellulose components at a moderate temperature, with both solvents easily recycled after pretreatment (Zhang et al., 2007). Li et al. (2009) investigated pretreatment of Bermuda grass with phosphoric acid of different concentrations at 50 °C for 60 min, followed by acetone wash of solid residue. The results show that, with the increase of acid concentration from 50% to 83%, the enzymatic digestibility of pretreated biomass increased by 126%. Ferulic acid esterase, an enzyme that breaks the ester bonds between arabinose and ferulic acid, was studied by Anderson et al. (2005) in treating different Bermuda grass cultivars at 37 °C for 24 h for improved digestibility. The results show that, enzyme pretreatment released a large amount of free sugars (generally higher than 100 mg/g dry biomass) that can be directly fermented to ethanol. However, the

study suggested the presence of inhibitors in the treated samples, which significantly reduced the ethanol production. More research is required to identify the inhibitors and improve the efficiency of enzyme pretreatment. 3.1.2. Physico-chemical pretreatment Ammonia fiber explosion (AFEX) is the most investigated physico-chemical technique for Bermuda grass pretreatment. In the AFEX process, lignocellulosic biomass is treated with liquid ammonia at moderate temperature and under high pressure for 10– 15 min, followed by an explosive pressure release (Reshamwala et al., 1995). Instantly releasing the pressure disrupts the fibrous structure of biomass and increases the accessible surface area, thus improving the digestibility of biomass (Teymouri et al., 2004). AFEX pretreatment also reduces lignin content, decrystallize cellulose, and prehydrolyze hemicellulose (Teymouri et al., 2005). Reshamwala et al. (1995) reported using AFEX to treat coastal Bermuda grass at conditions of 2 kg ammonia/kg dry biomass, 30 min treatment time at 90 °C, and 30% moisture (dry basis). After the treatment, a total reducing sugar yield of 684 mg/g dry biomass was obtained within 24 h of enzymatic hydrolysis, of which 48.4% was glucose. De la Rosa et al. (1994) investigated AFEX pretreatment of coastal Bermuda grass at similar treatment conditions and found that 90% conversion of cellulose and hemicellulose was achieved in the hydrolysis. Holtzapple et al. (1994) studied AFEX pretreatment at reduced temperatures (32–43 °C). After a single pretreatment at conditions of 32 °C, 11.2 atm absolute, 0.3 kg water/kg dry biomass, 1.3 kg ammonia/kg dry biomass, and 15 min, the 3-day reducing sugar and glucose yields were, respectively, 313 and 215 mg/g dry grass, only 40% and 59% of the theoretical yields, respectively. Even after two more rounds of treatments at 43 °C and 13.6 atm absolute, the 3-day reducing sugar yield was 381 mg/g dry grass, just increased by 22%. The study concluded that the low-temperature AFEX may not be the best pretreatment option for high sugar yield. A more recent study on AFEX pretreatment examined the temperatures of 80, 90, and 100 °C at a lower fixed ammonia loading (1.0 kg of ammonia/1.0 kg of dry biomass) for a reaction time of 5 and 30 min (Lee et al., 2010b). It was found that, after AFEX pretreatment, although no noticeable solid loss or compositional change of biomass was observed, the enzymatic digestibility was substantially improved. At the best conditions (100 °C for 30 min), 94.8% of the theoretical sugar yield was achieved in the enzymatic hydrolysis. Since no inhibitory byproducts are generated during pretreatment, the AFEX-treated biomass does not have to be washed, thus resulting in a negligible loss of biomass components (Holtzapple et al., 1994). Moreover, after pretreatment, ammonia is normally recovered and recycled, making AFEX a sustainable and cost-effective pretreatment technique. Eggeman and Elander (2005) embedded five corn stover pretreatment process models (dilute acid, hot water, AFEX, ammonia recycle percolation, and lime) in a full ethanol facility model to evaluate their economics and found that the minimum ethanol selling price (MESP) for AFEX was less than $1.40/gallon, making AFEX the second least costly pretreatment technique only next to dilute acid pretreatment. Autohydrolysis is another effective pretreatment method for Bermuda grass. It is regarded as an environmentally friendly technique, as water is the only media involved in biomass treatment. At high temperature and pressure, autohydrolysis predominantly depolymerizes hemicellulose with moderate impact on lignin and cellulose (Carvalheiro et al., 2009). Lee et al. (2009) studied autohydrolysis of coastal Bermuda grass using three temperatures (150, 160 and 170 °C) and two treatment times (30 and 60 min). At high temperatures, in addition to the depolymerization of hemicelluloses to soluble oligomers and mono-sugars, a variety of side-processes including extractive removal, partial dissolution of acid-

J. Xu et al. / Bioresource Technology 102 (2011) 7613–7620

soluble lignin and ashes, proteins solubilization, and generation of byproducts such as furfural and Hydroxymethylfurfural (HMF) also took place. Hemicellulose solubilization was more intensive at increased temperature and residence time. After pretreatment at 170 °C and 60 min, 83.3% of the hemicellulose in the raw biomass was solubilized. At the best pretreatment conditions of 150 °C and 60 min, 70% of the theoretical sugar could be recovered from pretreatment filtrate and enzymatic hydrolyzate. Further studies also show that autohydrolysis did not have a significant effect on the ultrastructure of the pretreated solids except for a color change. However, X-ray measurements found that autohydrolysis pretreatment caused a significant increase in crystallinity index, which was probably due to the changes of cellulose in crystallinity upon heating, as well as the solubilization of amorphous components including lignin and hemicellulose (Lee et al., 2010b). Brandon et al. (2008) investigated autohydrolysis pretreatment of Tifton 85 Bermuda grass at higher temperatures (200, 215, and 230 °C), shorter treatment times (2, 5, and 8 min), and different pressures (315– 700 psi). The results show that pressure negatively affect pretreatment effectiveness. During pretreatment, the release of glucose was not correlated with treatment severity, while those of xylose and total reducing sugars are both positively and linearly correlated with time and temperature. Moreover, the maximum sugar yield in the hydrolysis was obtained at the highest temperature (230 °C) and shortest time (2 min), at which the glucose yield was comparable with that from the biomass treated at 200 °C, while xylose yield increased by 110% due to the substantially increased dissolution of hemicellulose at 230 °C. Microwave heating is more rapid then convention heating and leads to a reduction of energy requirements by generating heat internally via direct interaction between the electromagnetic field and components of the biomass (De la Hoz et al., 2005). Keshwani et al. (2009) studied coastal Bermuda grass pretreatment by using the combination of alkali reagents including sodium carbonate (Na2CO3), NaOH, and Ca(OH)2 and microwave irradiation in a batch system at 250 W for 5 to 20 min. The study identified NaOH as the most effective alkali reagent and, at the optimal pretreatment conditions of 1% NaOH for 10 min, the glucose and xylose yields from pretreated biomass reached 87% and 59%, respectively, in the enzymatic hydrolysis. However, since most industrial processes applying microwave heating use continuous systems, verifying the feasibility of continuous microwave-based biomass pretreatment systems is required. 3.1.3. Biological pretreatment Biological pretreatment employs microorganisms and their enzyme systems to break down lignin structure of the lignocellulosic materials. White-rot fungi, which belong to Basidiomycetes, are the most effective and intensively studied organisms for lignocellulose pretreatment. Free radicals in the aromatic moieties generated by oxidative enzymes from the fungi, along with catalysts, result in degradation of aromatic compounds (Anderson and Akin, 2008). In the pretreatment of Bermuda grass, Akin et al. (1993) reported that, among three wild-type white-rot fungi and two cellulase-less mutants developed from Phanerochaete chrysosporium K-3, Ceriporiopsis subvermispora caused the most lignin removal and 80% biodegradation improvement by extensively removing ester-linked pcoumaric and ferulic acids, as well as the greatest amount of nonester-linked aromatics from plant cell walls. A further study comparing P. chrysosporium K-3 and Ceriporiopsis subvermispora show that, P. chrysosporium K-3 caused a higher loss in polysaccharide components than in phenolic components, while C. subvermispora removed a proportionate amount of phenolic components compared with polysaccharide components (Gamble et al., 1994). Another study by Akin et al. (1995) shows that, after 6-week treatment of Bermuda grass with C. subvermispora and Cyathus

7617

stercoreus, about 23% and 41% of total aromatics were removed, respectively, resulting in the improvement of digestibility of Bermuda grass stem by 29–32% and 63–77%, respectively. Both fungi removed proportionately more aromatics than carbohydrates. Although biological pretreatments of Bermuda grass avoid high energy requirements for heating and other chemical expenses, they have not been studied as extensively as other chemical or physico-chemical methods due to the low reaction rates. 3.2. Enzymatic hydrolysis To release fermentable sugars from the pretreated Bermuda grass, a subsequent hydrolysis step is required, which usually involves chemicals or enzymes. Compared with conventional acid or alkaline hydrolysis, enzymatic hydrolysis requires less utility cost as it is normally carried out at mild conditions (about 50 °C and pH 4.8) (Duff and Murray, 1996). Cellulose is hydrolyzed by cellulases which can be generated by various microorganisms including bacteria and fungi. Fugal cellulases are the most promising cellulolytic enzymes to release reducing sugars for ethanol production on a commercial scale, especially those from soft-rot fungus Trichoderma reesei (Duff and Murray, 1996; Kadam, 1996). Cellulases are a mixture of three different enzymes, endoglucanase (1,4-b-D-glucan glucanohydrolase), exoglucanase (1,4-b-D-glucan cellobiohydrolase), and cellobiase (b-glucosidase), that act synergistically to hydrolyze cellulose. Endoglucanase randomly attacks b-(1–4) glycosidic bonds of cellulose to create free chain-ends, exoglucanase releases cellobiose from the free chain-ends, and b-glucosidase degrades cellobiose into glucose (Sun and Cheng, 2002). Cellulases generally act on amorphous regions of cellulose and very few isolated cellulases have shown the ability to hydrolyze crystalline cellulose (Shewale, 1982). Due to its insufficient amount in cellulases from T. reesei, b-glucosidase is normally supplemented during hydrolysis to prevent cellulases inhibition caused by cellobiose accumulation (Ryu and Mandels, 1980). The inhibition of endoglucanase and exoglucanase by cellobiose as well as the inhibition of b-glucosidase by glucose can negatively affect the performance of enzymes in the hydrolysis process. Cellulases dosage has been investigated in many studies and the best dosage varies based on the properties of substrate and the pretreatment method used. Unlike cellulose which forms a crystalline structure, hemicellulose molecules are amorphous, low molecular weight, heterogeneous and branched polysaccharides, thus more accessible to enzymes during hydrolysis. Hemicellulases also come from a variety of microbial sources including bacteria, fungi, and yeasts (McAuliffe et al., 2007). In the hydrolysis of xylan, which is the dominant hemicellulose in many lignocellulosic feedstocks, three major enzymes including endo-b-1–4-xylanase which catalyzes the hydrolysis of the b-1–4 bonds between D-xylose residues of heteroxylans and xylo-oligosaccharides, exoxylanase which releases xylobioses, and b-xylosidase which hydrolyzes xylo-oligosaccharides to xylose are involved (Saha and Bothast, 1999). Other accessory enzymes including a-L-arabinofuranosidase, aglucuronidase, acetylxylan esterase, ferulic acid esterase, and pcoumaric acid esterase are necessary for the hydrolysis of different substituted xylans (Saha, 2003). Enzymatic hydrolysis of Bermuda grass pretreated using different methods has been extensively studied. Table 2 summarized the results of these studies. Based on the properties of pretreated biomass, hydrolysis conditions, and economic concerns, cellulase loadings of 10 to 40 FPU g 1 dry biomass were usually applied to enable high glucose yield. To prevent accumulation of cellobiose, cellobiase was supplemented in almost all the studies and proven necessary for the achievement of high sugar yields. It was reported that hemicellulase did not significantly (P < 0.05) enhance sugar yields from pretreated Bermuda grass when cellulases from

7618

J. Xu et al. / Bioresource Technology 102 (2011) 7613–7620

Table 2 Enzyme requirements from various studies on Bermuda grass. Pretreatment

Enzyme loading Cellulase

Dilute sulfuric acid Dilute sulfuric acid Sodium hydroxide Lime

a

Cellobiase

25 FPU g

1

40 FPU g

1

40 FPU g

75 IU g

None

70 CBU g

None

1

70 CBU g

1

None

40 FPU g

1

70 CBU g

1

None

Phosphoric acid– acetone AFEX

25 FPU g

1

None

AFEX

30 FPU g

Autohydrolysis

4.5 FPU g

5 IU g

28.4 U g 1

1

Autohydrolysis

10 FPU g

1

Autohydrolysis

30 FPU g

1

Ozone

10 FPU g

1

40 FPU g

1

Microwave

Result

References

50 °C, 100 rpm, 48 h, pH 4.8 55 °C, 155 rpm, 72 h, pH 4.8 55 °C, 155 rpm, 72 h, pH 4.8 55 °C, 155 rpm, 72 h, pH 4.8 50 °C, 150 rpm, 24 h, pH 4.8 48 °C, agitated, 24 h, pH 4.8 50 °C, 180 rpm, 48 h, pH 4.8 40 °C, 48 h, pH 4.5

229.3 mg g

Hemicellulase

1

1

1

Condition

None 1

None

30% of cellulase by volume 44.3 CBU g 1

30% of cellulase by volume None

30% of cellulase by volume 30% of cellulase by volume 30% of cellulase by volume 70 CBU g 1

30% of cellulase by volume 30% of cellulase by volume 30% of cellulase by volume None

50 °C, 180 rpm, 48 h, pH 4.8 50 °C, 180 rpm, 48 h, pH 4.8 50 °C, 180 rpm, 48 h, pH 4.8 55 °C, 155 rpm, 72 h, pH 4.8

1

sugar yield

95% theoretical sugar yield 90.4% glucan conversion and 65.1% xylan conversion 87.4% glucan conversion and 67.5% xylan conversion 97.3% enzymatic digestibility 684 mg g

1

sugar yield

101% cellulose conversion and 83% hemicellulose conversion 635 mg g 1 glucose yield and 282 mg g xylose yield 85% cellulose conversion and 60% hemicellulose conversion 57% cellulose conversion and 51% hemicellulose conversion 53% cellulose conversion and 23% hemicellulose conversion 87% glucan conversion and 57% xylan conversion

Sun and Cheng (2005) Redding et al. (2011) Wang et al. (2010) Wang (2009) Li et al. (2009) Reshamwala et al. (1995) Lee et al. (2010b)

1

Brandon et al. (2008) Lee et al. (2009) Lee et al. (2010b) Lee et al. (2010a) Keshwani and Cheng (2010)

a FPU (filter paper unit) is defined as the amount of enzyme that produces 1 lmol of glucose from filter paper per minute; CBU (cellobiase unit) is defined as the amount of enzyme that produces 2 lmol of glucose from cellobiose per minute; IU (international enzyme activity unit) is defined as the amount of enzyme that converts 1 lmol of substrate per minute.

T. reesei was used (Wang, 2009). This is probably due to the existence of xylanases in the T. reesei cellulases system, which was proven by Vinzant et al. (2001) using 2D electrophoresis. Other studies, however, indicate that the addition of hemicellulase may help to further improve the efficiency of hemicellulose conversion (Lee et al., 2009, 2010a,b). 3.3. Fermentation Yeasts, bacteria, and fungi can ferment ethanol based on lignocellulosic hydrolysate. The most commonly used microbe for ethanol production is Saccharomyces cerevisiae. It could produce ethanol to a concentration as high as 18% of the fermentation broth and is proven to be quite robust and less sensitive to inhibitors (Varga et al. 2004; Lin and Tanaka, 2006). To improve the economic viability of lignocellulose-to-ethanol conversion, hemicellulose hydrolysates containing high proportion of pentoses should also be utilized for ethanol production. Unlike hexoses, pentoses cannot be fermented by ordinary S. cerevisiae and other commonly used microorganisms. Based on principles of breeding and natural selection, Attfield and Bell (2006) developed strains of S. cerevisiae that can double in less than 6 h using xylose as a sole source. This represented an important step in developing pentose-utilizing S. cerevisiae strains for ethanol production. Development of genetically engineered microorganisms capable of metabolizing both hexoses and pentoses is another way to make the most of biomass-derived sugars. Some industrial pentose-fermenting S. cerevisiae strains have been developed to address this challenge. Recombinant strains including TMB 3400, TMB 3006, and 424A (LNF-ST) have been reported to achieve ethanol yields above 0.4 g ethanol/g sugar in lignocellulosic hydrolysate (Hahn-Hägerdal and Pamment, 2004; Sedlak and Ho, 2004). Quite a few other microorganisms (natural as well as recombinant) have been studied to convert xylose to ethanol. For example, Zymomonas mobilis is an exceptional bacterium with high ethanol yield and productivity. When two operons encoding xylose assimilation and pentose phosphate path-

way enzymes were constructed and transformed into it, the recombinant Z. mobilis could grow on xylose, the main pentose component in hemicellulose, and fermented it to ethanol (Zhang et al., 1995). Further efforts, however, are required to improve the efficiencies of pentose fermentation to make the ethanol production viable. Fermentation step has two common categories: separate hydrolysis and fermentation (SHF) in which enzymatic hydrolysis is performed separately from the fermentation, and simultaneous saccharification and fermentation (SSF) in which cellulose hydrolysis is carried out in the presence of the fermentative microbes (Mosier et al., 2005). During conventional SHF, the increased glucose content in hydrolyzate is inhibitory to both cellulase and cellobiase (Xiao et al., 2004). In order to avoid end-product inhibition, the approach of SSF has been developed, in which the fermentable sugars generated during enzymatic hydrolysis is consumed immediately by yeast for ethanol fermentation. The optimum temperature used in SSF is around 38 °C, which is a compromise between hydrolysis (45–50 °C) and fermentation (30 °C) (Philippidis, 1996). Since enzymatic hydrolysis is considered the rate-limiting step in SSF, which requires a higher reaction temperature, thermophilic strains of S. cerevisiae are preferred in SSF to prevent the negative effect of high temperature on the ethanol production and tolerance abilities of the yeast. Li et al. (2009) used SSF to produce ethanol from the Bermuda grass pretreated with phosphoric acid–acetone. At the reaction conditions of 38 °C, pH 5.0, 150 rpm, 96 h, cellulase loading of 25 FPU g 1 cellulose, and 10% (v/v) S. cerevisiae inoculum, 94.7% of theoretical ethanol yield was achieved. Anderson et al. (2008) reported that, at the reaction conditions of 35 °C, pH 4.5, 150 rpm, 72 h, cellulase loading of 5 FPU g 1 biomass, cellubiase loading of 12 U g 1 biomass, and optical S. cerevisiae density (600 nm, OD) of 0.5, the ethanol yields from the acid pretreated Bermuda grass leaves and stems reached 122 to 141 mg g 1 biomass, depending on the genotype. At the same SSF conditions, Anderson et al. (2010) examined the ethanol yield from 50 genetically diverse Bermuda grass accessions and reported ethanol

J. Xu et al. / Bioresource Technology 102 (2011) 7613–7620

yields ranging from 105.3 to 167.3 mg g 1 biomass, with the mean value of 139.9 mg g 1. Anderson and Akin (2008) also reported that Bruce Dien achieved ethanol yields of 159.7, 156.5, and 145.9 mg g 1 respectively from ‘Tifton 85’, ‘Coastcross II’, and ‘Coastal’ Bermuda grass using SSF, which were substantially higher than that from switchgrass. However, in all the above studies, pentose was not utilized as a sugar source for fermentation. Further studies, therefore, are required to develop novel approaches for pentose fermentation or make better use of pentose residues to improve the cost-effectiveness of SSF. 4. Other energy applications Besides fuel ethanol production, Bermuda grass can be used as a feedstock in other energy applications. Anaerobic digestion of Bermuda grass has been studied to evaluate the suitability of using Bermuda grass to produce biogas. Klass and Ghosh (1981) reported that, under conventional mesophilic conditions, a methane yield of about 118.6 L/kg volatile solids was observed. When supplemented with extra nitrogen (ammonium chloride), the methane yield continually increased up to 218.5 L/kg volatile solids until reaching the lowest C/N ratio (6.3). Thermophilic digestion with supplemental nitrogen additions resulted in methane yields of about 168.6 L/kg volatile solids. Ghosh et al. (1980) studied anaerobic digestion of Bermuda grass-organic waste blends and found that, without external nutrients addition, Bermuda grass-water hyacinth–MSW (municipal solid waste)–sludge blends can keep anaerobic digestion working under conventional mesophilic conditions for long periods without difficulty. The results also show that pretreatment of the feed biomass with 3% NaOH solution at room temperature could improve methane yield by 20%. Thermochemical conversion process is another promising method of converting Bermuda grass for energy purposes. The syngas produced can be converted to fuel alcohols via the Fischer–Tropsch process (Boateng et al., 2006). Boateng et al. (2007) studied pyrolysis of two genotypes of Bermuda grass, ‘Coastal’ and ‘Tifton 85’, at 500, 700, and 900 °C, and reported that the gas and char yields were, respectively, 10– 12.5 wt.% and 5.5–16 wt.% of raw biomass, with the maximum gas yield and minimum char yield occurring at 900 °C. The research also found that the effects of Bermuda grass genotype and plant part might not significantly affect thermochemical conversion when Bermuda grass feedstocks were harvested at the same maturity. 5. Conclusions Bermuda grass is a promising biomass feedstock for biofuel production in the Southern United States and many other parts of the world where it is cheap and readily available. It has the advantages of having preexisting cultivars developed for improved digestibility and providing remarkable environmental benefit when involved in nutrient management in animal industry. Intensive studies have been conducted to convert Bermuda grass to biofuels with promising results reported. Undoubtedly, genetic engineering technologies that help to reduce lignin and increase polysaccharides in plant, and produce cellulases within the plant would remarkably improve the economic viability of Bermuda grass-tobiofuel conversion. References Adeli, A., Rowe, D.E., Read, J.J., 2006. Effects of soil type on bermuda grass response to broiler litter application. Agron. J. 98 (1), 148–155. Akin, D.E., Rigsby, L.L., Sethuraman, A., Morrison III, W.H., Gamble, G.R., Eriksson, K.L., 1995. Alterations in structure, chemistry, and biodegradability of grass lignocellulose treated with the white rot fungi Ceriporiopsis subvermispora and Cyathus stercoreus. Appl. Environ. Microbiol. 61 (4), 1591–1598.

7619

Akin, D.E., Sethuraman, A., Morrison III, W.H., Martin, S.A., Eriksson, K.E.L., 1993. Microbial delignification using white rot fungi improves forage digestibility. Appl. Environ. Microbiol. 59 (12), 4274–4282. Anderson, W.F., Akin, D.E., 2008. Structural and chemical properties of grass lignocelluloses related to conversion for biofuels. J. Ind. Microbiol. Biotechnol. 35 (5), 355–366. Anderson, W.F., Dien, B.S., Brandon, S.K., Peterson, J.D., 2008. Assessment of Bermuda grass and bunch grasses as feedstock for conversion to ethanol. Appl. Biochem. Biotechnol. 145 (1), 13–21. Anderson, W.F., Dien, B.S., Jung, H.G., Vogel, K.P., Weimer, P.J., 2010. Effects of forage quality and cell wall constituents of Bermuda grass on biochemical conversion to ethanol. Bioenerg. Res. 3 (3), 225–237. Anderson, W.F., Peterson, J., Akin, D.E., Herbert Morrison III, W., 2005. Enzyme pretreatment of grass lignocellulose for potential high-value co-products and an improved fermentable substrate. Appl. Biochem. Biotechnol. 121 (1), 303– 310. Attfield, P.V., Bell, P.J.L., 2006. Use of population genetics to derive nonrecombinant Saccharomyces cerevisiae strains that grow using xylose as a sole carbon source. FEMS Yeast Res. 6 (6), 862–868. Bade, D.H., Conrad, B.E., Holt, E.C., 1985. Temperature and water stress effects on growth of tropical grasses. J. Range Manage. 38 (4), 321–324. Ball, D.M., Hoveland, C.S., Lacefield, G.D., 1991. Southern forages. Potash and Phosphate Institute: Foundation for Agronomic Research. Atlanta, Georgia. Boateng, A.A., Anderson, W.F., Phillips, J.G., 2007. Bermuda grass for biofuels: effect of two genotypes on pyrolysis. Energy Fuels 21 (2), 1183–1187. Boateng, A.A., Hicks, K.B., Vogel, K.P., 2006. Pyrolysis of switchgrass (Panicum virgatum) harvested at several stages of maturity. J. Anal. Appl. Pyrolysis 75 (2), 55–64. Brandon, S.K., Eiteman, M.A., Patel, K., Richbourg, M.M., Miller, D.J., Anderson, W.F., Peterson, J.D., 2008. Hydrolysis of Tifton 85 Bermuda grass in a pressurized batch hot water reactor. J. Chem. Technol. Biotechnol. 83 (4), 505–512. Brink, G.E., Rowe, D.E., Sistani, K.R., 2002. Broiler litter application effects on yield and nutrient uptake of ‘Alicia’ Bermuda grass. Agron. J. 94 (4), 911–916. Brink, G.E., Rowe, D.E., Sistani, K.R., Adeli, A., 2003. Bermuda grass cultivar response to swine effluent application. Agron. J. 95 (3), 597–601. Burns, J.C., Westerman, P.W., King, L.D., Cummings, G.A., Overcash, M.R., Goode, L., 1985. Swine lagoon effluent applied to ‘Coastal’ Bermuda grass: I. Forage yield, quality, and element removal. J. Environ. Qual. 14 (1), 9–14. Carvalheiro, F., Silva-Fernandes, T., Duarte, L.C., Girio, F.M., 2009. Wheat straw autohydrolysis: process optimization and products characterization. Appl. Biochem. Biotechnol. 153 (1), 84–93. De la Hoz, A., Diaz-Ortiz, A., Moreno, A., 2005. Microwaves in organic synthesis. Thermal and non-thermal effects. Chem. Soc. Rev. 34, 164–178. De la Rosa, L.B., Reshamwala, S., Latimer, V.M., Shawky, B.T., Dale, B., Stuart, E.D., 1994. Integrated production of ethanol fuel and protein from coastal Bermuda grass. Appl. Biochem. Biotechnol. 45–46 (1), 483–497. Duff, S.J.B., Murray, W.D., 1996. Bioconversion of forest products industry waste cellulosics to fuel ethanol: a review. Bioresour. Technol. 55 (1), 1–33. Eggeman, T., Elander, R.T., 2005. Process and economic analysis of pretreatment technologies. Bioresour. Technol. 96 (18), 2019–2025. Evers, G.W., 2002. Ryegrass–Bermuda grass production and nutrient uptake when combining nitrogen fertilizer with broiler litter. Agron. J. 94 (4), 905–910. Funderburg, E.R., Twidwell, E.K., 2000. Fertilizing Summer Hay Fields. Pub. 2612. Louisiana State Univ. Agric. Ctr., LSU, Baton Rouge, LA. Gamble, G.R., Sethuraman, A., Akin, D.E., Eriksson, K.L., 1994. Biodegradation of lignocellulose in Bermuda grass by white rot fungi analyzed by solid-state 13C nuclear magnetic resonance. Appl. Environ. Microbiol. 60 (9), 3138–3144. Ghosh, S., Henry, M.P., Klass, D.L., 1980. Bioconversion of water hyacinth-coastal bermuda grass–MSW–sludge blends to methane. In: Biotech. Bioeng. Symp. No. 10. John Wiley and Sons Inc, New York, pp. 165–237. Hahn-Hägerdal, B., Pamment, N., 2004. Microbial pentose metabolism. Appl. Biochem. Biotechnol. 113–116, 1207–1209. Hanson, A.A., 1972. Breeding of grasses. In: Youngner, V.B., McKell, C.M. (Eds.), The Biology and Utilization of Grasses. Academic Press, New York, pp. 36–52. Hill, G.M., Gates, R.N., Burton, G.W., 1993. Forage quality and grazing steer performance from Tifton 85 and Tifton 78 Bermuda grass pastures. J. Anim. Sci. 71 (12), 3219–3225. Holtzapple, M.T., Ripley, E.P., Nikolaou, M., 1994. Saccharification, fermentation, and protein recovery from low-temperature AFEX-treated coastal Bermuda grass. Biotechnol. Bioeng. 44 (9), 1122–1131. Kadam, K.L., 1996. Cellulases production. In: Wyman, C.E. (Ed.), Handbook on Bioethanol: Production and Utilization. Taylor and Francis, Washington, DC, pp. 213–252. Keshwani, D., Cheng, J.J., 2009. Microwave-based alkali pretreatment of switchgrass and coastal Bermuda grass for bioethanol production. Biotechnol. Prog. 26 (3), 644–652. Klass, D.L., Ghosh, S., 1981. Methane production by anaerobic digestion of Bermuda grass. In: Klass, D.L. (Ed.), Biomass as a Nonfossil Fuel Source (14th edition), ACS Symposium Series 144. American Chemical Society, Washington, DC. Lee, J.M., Jameel, H., Venditti, R.A., 2010a. Effect of ozone and autohydrolysis pretreatments on enzymatic digestibility of coastal Bermuda grass. Bioresource 5 (2), 1084–1101. Lee, J.M., Jameel, H., Venditti, R.A., 2010b. A comparison of the autohydrolysis and ammonia fiber explosion (AFEX) pretreatments on the subsequent enzymatic hydrolysis of coastal Bermuda grass. Bioresour. Technol. 101 (14), 5449–5458.

7620

J. Xu et al. / Bioresource Technology 102 (2011) 7613–7620

Lee, J.M., Shi, J., Venditti, R.A., Jameel, H., 2009. Autohydrolysis pretreatment of coastal Bermuda grass for increased enzyme hydrolysis. Bioresour. Technol. 100 (24), 6434–6441. Lee, R.D., Harris, G., Murphey, T.R., 2002. Bermuda grasses in Georgia. Georgia Cooperative Extension Service. Bull. 911. University of Georgia, Athens, GA. Li, C., Knierim, B., Manisseri, C., Arora, R., Scheller, H.V., Auer, M., Vogel, K.P., Simmons, B.A., Singh, S., 2010. Comparison of dilute acid and ionic liquid pretreatment of switchgrass: biomass recalcitrance, delignification and enzymatic saccharification. Bioresour. Technol. 101 (13), 4900–4906. Li, H., Kim, N., Jiang, M., Kang, J.W., Chang, H.N., 2009. Simultaneous saccharification and fermentation of lignocellulosic residues pretreated with phosphoric acidacetone for bioethanol production. Bioresour. Technol. 100 (13), 3245–3251. Lin, Y., Tanaka, S., 2006. Ethanol fermentation from biomass resources: current state and prospects. Appl. Microbiol. Biotechnol. 69 (6), 627–642. Liu, F., Mitchell, C.C., Odom, J.W., Hill, D.T., Rochester, E.W., 1997. Swine lagoon effluent disposal by overland flow: effects on forage production and uptake of nitrogen and phosphorus. Agron. J. 89 (6), 900–904. McAuliffe, J.C., Aehle, W., Whited, G.M., Ward, D.E., 2007. In: Kent, J.A. (Ed.), Kent and Riegel’s Handbook of Industrial Chemistry and Biotechnology, vol. 1. Springer Science, Business Media, LLC, New York, p. 1384. Mohamed Shabi, M., Sasikala, S.S., Gayathri, K., Sreelakshmi, B.S., 2010. Cynodon dactylon: a review. Int. J. Biomed. Res. Anal. 1 (2), 65–67. Mosier, N., Wyman, C., Dale, B., Elander, R., Lee, Y.Y., Holtzapple, M., Ladisch, M., 2005. Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour. Technol. 96 (6), 673–686. Mueller, J.P., Green, J.T., Chamblee, D.S., Burns, J.C., Bailey, J.E., Brandenburg, R.L., 1993. Bermuda grass management in North Carolina. N.C. Cooperative Extension Service, Raleigh, NC. Muir, J.P., Butler, T., Helton, T.J., McFarland, M.L., 2010a. Dairy manure compost application rate and timing influence Bermuda grass yield and nutrient concentration. Crop Sci. 50 (5), 2133–2139. Muir, J.P., Lambert, B.D., Greenwood, A., Lee, A., Riojas, A., 2010b. Comparing repeated forage Bermuda grass harvest data to single, accumulated bioenergy feedstock harvests. Bioresour. Technol. 101 (1), 200–206. NREL, 2006. Biomass Feedstock Composition and Property Database. Available from: . Overman, A.R., 1993. Logistic response of Bermuda grass and bunchgrass cultivars to applied nitrogen. Agron. J. 85 (3), 541–545. Overman, A.R., Neff, C.R., Wilkinson, S.R., Martin, F.G., 1990. Water, harvest interval, and applied nitrogen effects on forage yield of Bermuda grass and bahiagrass. Agron. J. 82 (5), 1011–1016. Philippidis, G.P., 1996. Cellulose bioconversion technology. In: Wyman, C.E. (Ed.), Handbook on Bioethanol: Production and Utilization. Taylor and Francis, Washington, DC, pp. 253–285. Pimentel, D., 2003. Ethanol fuel: energy balance, economics, and environmental impacts are negative. Nat. Resour. Res. 12 (2), 127–134. Prine, G.M., Burton, G.W., 1956. The effect of nitrogen rate and clipping frequency upon the yield, protein content and certain morphological characteristics of coastal Bermuda grass (Cynodon dactylon (L) Pers.). Agron. J. 48, 296–301. Ravindra, S., 2003. Medicinal plants of India: an encyclopedia. Daya Publishing House, Delhi. Redding, A.P., Wang, Z., Keshwani, D.R., Cheng, J.J., 2011. High temperature dilute acid pretreatment of coastal Bermuda grass for enzymatic hydrolysis. Bioresour. Technol. 102 (2), 1415–1424. Reshamwala, S., Shawky, B.T., Dale, B.E., 1995. Ethanol production from enzymatic hydrolysates of AFEX-treated coastal Bermuda grass and switchgrass. Appl. Biochem. Biotechnol. 51–52, 43–55. Ryu, D.D.Y., Mandels, M., 1980. Cellulases – biosynthesis and applications. Enzyme Microb. Technol. 2, 91–102.

Saha, B.C., 2003. Hemicellulose bioconversion. J. Ind. Microbiol. Biotechnol. 30 (5), 279–291. Saha, B.C., Bothast, R.J., 1999. Enzymology of xylan degradation. In: Imam, S.H., Greene, R.V., Zaidi, B.R. (Eds.), Biopolymers: Utilizing Nature’s Advanced Materials. ACS, Washington DC, pp. 167–194. Sedlak, M., Ho, N.W., 2004. Production of ethanol from cellulosic biomass hydrolysates using genetically engineered Saccharomyces yeast capable of cofermenting glucose and xylose. Appl. Biochem. Biotechnol. 113–116, 403– 416. Shewale, J.G., 1982. b-glucosidase: its role in cellulases synthesis and hydrolysis of cellulose. Int. J. Biochem. 14 (6), 435–443. Shi, J., 2007. Microbial Pretreatment of Cotton Stalks by Phanerochaete chrysosporium for Bioethanol Production, Ph.D. dissertation, North Carolina State University, Raleigh. Sistani, K.R., Brink, G.E., Adeli, A., Tewolde, H., Rowe, D.E., 2004. Year-round soil nutrient dynamics from broiler litter application to three Bermuda grass cultivars. Agron. J. 96 (2), 525–530. Sun, Y., Cheng, J., 2002. Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresour. Technol. 83 (1), 1–11. Sun, Y., Cheng, J.J., 2005. Dilute acid pretreatment of rye straw and Bermuda grass for ethanol production. Bioresour. Technol. 96 (14), 1599–1606. Taliaferro, C.M., Bouquette Jr., F.M., Mislevy, P., 2004. In: Bermuda grass and star grass. In: Moser, L.E., Burson, B.L., Solenberger, L.E. (Eds.), . Warm-season (C4) grasses. American Society of Agronomy: Crop Science Society of America: Soil Science Society of America, Madison, WI, pp. 417–475. Teymouri, F., Laureano-Perez, L., Alizadeh, H., Bale, B.E., 2004. Ammonia fiber explosion treatment of corn stover. Appl. Biochem. Biotechnol. 115 (1), 951– 963. Teymouri, F., Laureano-Perez, L., Alizadeh, H., Dale, B.E., 2005. Optimization of the ammonia fiber explosion (AFEX) treatment parameters for enzymatic hydrolysis of corn stover. Bioresour. Technol. 96 (18), 2014–2018. Varga, E., Reczey, K., Zacchi, G., 2004. Optimization of steam pretreatment of corn stover to enhance enzymatic digestibility. Appl. Biochem. Biotechnol. 114 (1), 509–523. Vinzant, T.B., Adney, W.S., Decker, S.R., Baker, J.O., Kinter, M.T., Sherman, N.E., Fox, J.W., Himmel, M.E., 2001. Fingerprinting Trichoderma reesei hydrolases in a commercial cellulases preparation. Appl. Biochem. Biotechnol. 91 (1), 99–107. Wang Z., 2009. Alkaline Pretreatment of Coastal Bermuda Grass for Bioethanol Production. M.S. thesis, North Carolina State University, Raleigh, North Carolina. Wang, Z., Keshwani, D.R., Redding, A.P., Cheng, J.J., 2010. Sodium hydroxide pretreatment and enzymatic hydrolysis of coastal Bermuda grass. Bioresour. Technol. 101 (10), 3583–3585. Wilkinson, S.R., Langdale, G.W., 1974. Fertility needs of warm-season grasses. In: Mays, D.A. (Ed.), Forage fertilization. ASA, CSSA, and SSSA, Madison, WI. Xiao, Z., Zhang, X., Gregg, D.J., Saddler, J.N., 2004. Effects of sugar inhibition on cellulases and b-glucosidase during enzymatic hydrolysis of softwood substrates. Appl. Biochem. Biotechnol. 115 (1), 1115–1126. Xu, J., Cheng, J.J., Sharma-Shivappa, R.R., Burns, J.C., 2010a. Sodium hydroxide pretreatment of switchgrass for ethanol production. Energy Fuels 24 (3), 2113– 2119. Xu, J., Cheng, J.J., Sharma-Shivappa, R.R., Burns, J.C., 2010b. Lime pretreatment of switchgrass at mild temperatures for ethanol production. Bioresour. Technol. 101 (8), 2900–2903. Zhang, M., Eddy, C., Deanda, K., Finkelstein, M., Picataggio, S., 1995. Metabolic engineering of a pentose metabolism pathway in ethanologenic Zymomonas mobilis. Science 267, 240–243. Zhang, Y.H.P., Ding, S.Y., Mielenz, J.R., Cui, J.B., Elander, R.T., Laser, M., Himmel, M.E., McMillan, J.R., Lynd, L.R., 2007. Fractionating recalcitrant lignocellulose at modest reaction conditions. Biotechnol. Bioeng. 97 (2), 214–223.