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Sugarcane bagasse and leaves: Foreseeable biomass of biofuel and bio-products. J Chem Technol Biotechnol ARTICLE in JOURNAL OF CHEMICAL TECHNOLOGY & BIOTECHNOLOGY · JANUARY 2012 Impact Factor: 2.35 · DOI: 10.1002/jctb.2742
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(wileyonlinelibrary.com) DOI 10.1002/jctb.2742
Sugarcane bagasse and leaves: foreseeable biomass of biofuel and bio-products Anuj K. Chandel,a∗ Silvio S. da Silva,a Walter Carvalhoa and Om. V. Singhb∗ Abstract Sugarcane is among the principal agricultural crops cultivated in tropical countries. The annual world production of sugarcane is ∼1.6 billion tons, and it generates ∼279 million metric tons (MMT) of biomass residues (bagasse and leaves). Sugarcane residues, particularly sugarcane bagasse (SB) and leaves (SL) have been explored for both biotechnological and non-biotechnological applications. For the last three decades, SB and SL have been explored for use in lignocellulosic bioconversion, which offers opportunities for the economic utilization of residual substrates in the production of bioethanol and value-added commercial products such as xylitol, specialty enzymes, organic acids, single-cell protein, etc. However, there are still major technological and economic challenges to be addressed in the development of bio-based commercial processes utilizing SB and SL as raw substrates. This article aims to explore SB and SL as cheaper sources of carbohydrates in the developing world for their industrial implications, their use in commercial products including commercial evaluation, and their potential to advance sustainable bio-based fuel systems. c 2011 Society of Chemical Industry Keywords: sugarcane residues; ethanol; xylitol; organic acids; industrial enzymes
INTRODUCTION The constant demand for non-food and feed based substrates has influenced the need to exploit sustainable and cheaper resources for their bioconversion into value-added products of commercial interest through basic routes of microbial bio-conversion.1 With this objective, there have been many products obtained from renewable resources such as biomass. Due to advancement in the agricultural industries, millions of tons of wastes and byproducts are generated every year that have potential as low-cost sources of energy and material.1 – 4 One of these byproducts is sugarcane bagasse, which can be used in the production of industrial enzymes, ethanol, xylitol, organic acids, etc.4,5 Bagasse is a residue obtained from sugarcane after it is crushed to obtain the juice used for sugar and ethanol production. Another important sugarcane residue is the leaves, which are usually left in agricultural fields during sugarcane harvesting.6 – 8 The dried leaves, called sugarcane trash (ST), are produced in abundance (6–8 tons from one hectare of sugarcane crop).7 Generally, leaves are burnt in the fields, which produces fly ash, severely damages soil microbial diversity, and raises environmental concerns. Sugarcane bagasse (SB) and sugarcane leaves/trash (SL or ST) contain appreciable amount of cellulose and hemicellulose, which can be de-polymerized by chemical or enzyme cocktails into simple sugar monomers (glucose, xylose, arabinose, mannose, galactose, etc.).7,8 Such sugar streams obtained from SB and SL can be converted into bioethanol and value-added products of commercial significance, which has joint economic importance.4,7 – 10 Harnessing bagasse and leaves for industrial purposes could provide a sustainable and economic solution for the production of biobased, value-added products such as ethanol, xylitol, organic acids, industrial enzymes, and other products.4,5 The proposed model in Fig. 1 shows the efficient utilization of SB or SL/ST into products of economic importance via both biological and non-biological
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routes. The efficient utilization of sustainable resources will assist in improving the socioeconomic status of developing countries, creating employment opportunities and improving the environment. Among sugarcane-producing countries, Brazil is the top producer, with 625 million tons of sugarcane in 2011, followed by India and China (http://www.unica.com.br). Generally, 280 kg of humid bagasse is generated from 1 ton of sugarcane.10 A significant quantity of post-harvest SL is also generated (250 kg dry weight per ton of sugarcane).7 Pandey et al.4 reported that 50% of SB is used for energy generation within the plant and the rest remains unused in the environment. Therefore, the bioconversion of leftover bagasse into value-added products may have sustainable economic and strategic benefits.4,11 . Figure 2 summarizes the procedural steps involved in the application of SB for the production of various industrially important products of commercial significance (bio-products and biorefineries) along with its application for entrapment of microbial cells as an immobilized or growth support. SB has long been considered in bioethanol industries for ethanol production, referred to as ‘second-generation ethanol’.10,11 De-
∗
Correspondence to: Anuj K. Chandel, Department of Biotechnology, School of Engineering of Lorena, University of S˜ao Paulo, Lorena- 12.602.810, Brazil. E-mail:
[email protected];
[email protected] Om. V. Singh, Division of Biological and Health Sciences 300 Campus Drive, University of Pittsburgh, Bradford, PA-16701, USA. E-mail:
[email protected];
[email protected]
a Department of Biotechnology, School of Engineering of Lorena, University of S˜ao Paulo, Lorena 12.602.810, Brazil b Division of Biological and Health Sciences, University of Pittsburgh, Bradford, PA 16701, USA
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Sugarcane bagasse
AK Chandel et al.
Sugarcane tops and leaves (ST)
Nonbiotechnological Applications
Biotechnological Applications
Pretreatment Fermentation (SSF) Enzymatic hydrolysis Microbial fermentation (SmF)
Ethanol as fuel Xylitol Industrial enzymes Organic acids Other value-added products (antibiotics, Single cell protein, bio-hydrogen, aroma, pigments etc)
Pyrolysis Chemical catalysis Chem-remediation Biochar Coumaric acid Methyl cellulose Furfural and 5-hydroxy methyl furfural Pyrolysis and steam gasification etc.
Figure 1. Strategic applications of sugarcane plant. The pocessing of sugarcane in fields yield green tops and dried leaves, so-called sugarcane trash (ST). The bagasse is products from the stem after juice extraction. Both have profound importance in biotechnological and non-biotechnological applications.
spite major research efforts to promote SB as a bioenergy material, commercial use of SB on an industrial scale has yet to be explored.12,13 However, recent advancements in genetic engineering to improve microbial strains, media formulations, and product recovery have enabled more efficient conversion of SB and SL into value-added products of commercial interest.1,3,14 This article discusses the possibilities of exploiting SB and SL/ST as potential substrates for biofuel and value-added products of commercial interest. Special emphasis is placed on recent developments such as genetically modified microbial strains, statistical software for designing the process parameters and media formula-
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tion, including downstream recovery in the process and products developed including commercial evaluation of bio-products from SB and SL/ST.
CHEMISTRY OF SUGARCANE BAGASSE AND SUGARCANE LEAVES The complex chemical composition of the cell walls in SB limits its use as fodder for cattle and ruminants, in contrast to wheat straw, rice straw, sorghum straw, etc., which makes SB a more attractive substrate for commercialization. Generally, SB is composed (% w/w
c 2011 Society of Chemical Industry
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Bio-industrial benefits of sugarcane bagasse and leaves
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Mild alkali pretreatment
Sugarcane bagasse
Industrial enzymes Organic acids, pigments, vitamins Antibiotics, single cell protein Immobilizationcarrier
Direct carbon source for microbes in SSF or SmF systems
Pentose sugar rich hydrolysate + inhibitory compounds
Auto hydrolysis or dilute acid
Detoxification (Chemical or biological)
Cellulignin or Holocellulose
Delignification (alkali or biodelignification)
Enzymatic hydrolysis by cellulolytic enzymes cocktail
Fermentation of sugars (C5 + C6) metabolizing strains)
Xylitol Ethanol Organic acids Industrial enzymes Solvents, pigments, single cell protein and others.
Figure 2. Procedural steps involved in the application of SB for the formation of various industrially important products.
dry basis) of hemicellulose (26.2–35.8), cellulose (35–45), lignin (11.4–25.2), and others (2.9–14.4).15,16 The unequal chemical composition of bagasse depends upon multiple factors, including crop variety, climate conditions, location and mode of growth, use of fertilizers, and physical and chemical composition of soil.16 The method of chemical composition analysis may also play a crucial role in establishing the chemical makeup of bagasse.17 A detailed chemical analysis (% dry matter) from the cell wall of SB and SL showed glucan (41.4, 33.3); xylan (22.5, 18.1); arabinan (1.3, 3.1); galactan (1.3, 1.5); mannan (3.4, 1.5); and lignin (23.6, 36.1), respectively.18 The higher content of lignin limits the SL or lignocellulosic biomass (LB) usage for industrial applications. In order to utilize the LB into value-added products, harnessing of cellulosics fraction into ready-to-fermentable sugars is inevitable.15 It is evident that the high content of lignin in the plant cell wall is a major barrier to access the carbohydrate fraction of the cell wall, which essentially requires pretreatment (higher chemical loadings in conjunction with increased reaction time and temperature) and higher cellulase loadings result in an uneconomic process.14,30 The costs of cellulolytic enzymes are high, and the required amount of cellulases is also high, which increases processing costs. The removal of lignin increases accessibility to cellulose and allows more amenability of cellulase to the carbohydrate skeleton of plant cell wall.15 The low content of ash (1.4%) in SB was found to be highly advantageous over other agricultural residues such as rice straw (17.5% ash) or wheat straw (11.0% ash).4
PRETREATMENT OF SUGARCANE BAGASSE FOR INDUSTRIAL APPLICATIONS An effective pretreatment is to expose the cellulosics by removal of lignin or hemicellulose to improve the overall hydrolysis efficiency.20 In addition to pretreatment, an effective cellulolytic
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enzyme cocktail, the amount of enzyme loading, hydrolyzing conditions and the nature of lignocellulosic material are critical parameters for maximum hydrolysis of lignocellulosic material.15 Substantial increase in lignin removal and hemicellulose depolymerization into simpler sugars has often been reported with pretreated substrate.19 Among classical methods for pretreatment of lignocellulosic materials, alkaline hydrolysis (NaOH, Na2 SO3 , NH4 OH etc.), biological treatment (growth of white rot fungi or delignifying microorganisms over the lignocellulosic residues), and acidic pretreatments (HCl, H2 SO4 , H3 PO4 , oxalic acid, formic acid, etc.) have been known to either depolymerise the hemicellulosic fraction of cell wall into simpler monomeric constituents or remove the lignin.20 Pretreatment is required to make the cellulosics more amenable to further cellulase mediated hydrolytic reactions. Pretreated SB has also been utilized as an inert support material for fungal biomass in the solid-state fermentation process7,21 and as an immobilization carrier.22 The mechanistic application of pretreated SB impregnated with suitable liquid media provides homogenous aerobic conditions throughout the bioreactor, which in turn will yield high product titers with relatively high purity after the completion of a cultivation cycle.22 The acidic hydrolysis of lignocellulosic substrates degrades the hemicellulose fraction into a variety of sugar monomers (xylose, arabinose, mannose, galactose, and glucose) in addition to fermentation inhibitors (furfurals, phenolics, and weak acids). These inhibitory substances must be eliminated from the hydrolysates prior to fermentation to improve the yield of desirable products.9,23 Alkali-based pretreatments and bio-delignification methods remove the lignin, leaving cellulose and hemicellulose. The pretreated material can then be hydrolyzed into simpler sugars using a cellulolytic enzyme cocktail. The cellulolytic cocktail should contain sufficient amounts of exoglucanase, endoglucanase, β-glucosidase, and other ancillary enzymes required for the
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Table 1.
Hydrolytic efficiency of chemically pretreated sugarcane bagasse followed by enzymatic saccharification
Pretreatment conditions
Enzymatic loadings
NaOH treatment (10% NaOH, 90 ◦ C, S : L=1 : 3, 1.5 h) + per acetic acid (10%, 2.5 h, 75 ◦ C) Cellulose dissolution by N-methylmorpholine-N-oxide (NMMO) (5%w/w bagasse/NMMO, 130 ◦ C, 1 h) SO2 catalyzed steam pre-treatment (2% SO2 , 190 ◦ C, 5 min) Peroxide-alkaline pre-treatment (2% H2 O2 , 0.5% MgSO4 , 60 ◦ C, 16 h, pH 11.6) Phosphoric acid (10 min, 160–190 ◦ C, 1% H3 PO4 , enzymatic Calcium hydroxide Formic acid (60% v/v formic acid, 0.6% H2 SO4 , 121 ◦ C, 90 min) Steam explosion ∗
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Hydrolysis efficiency
References
15 FPU g−1
92.04%∗
15
5 FPU g−1
95% ∗
24
2.32 g of Celluclast 1.5L and 0.52 g of Novozyme 188 10 FPU g−1
91.7%∗
25
63.0%∗
26
81 ± 1 g L−1 total sugars
27
392.8 mg total sugars g−1 bagasse
28
0.791 g sugars g−1 bagasse
29
94.6%∗
30
100 FPU g−1 dry weight 3.5 FPU g−1 FPU, 1.0 IU g−1 beta glucosidase NA 3.5 IU mL−1 FPU; 4.0 IU mL−1 beta glucosidase; 75 IU mL−1 CMCase
Based on dry weight of total carbohydrate content available in substrate.
Table 2.
Applications of SB in ethanol production using different microorganisms under various cultivation conditions
Hydrolysate composition (g L−1 ) Glucose, 7.3; Xylose, 65.9; Galactose, 2.2; Acetic acid, 5.9 Glucose, 3.5; Xylose, 25.8; Arabinose 2.4; Acetic Acid 4.6 Glucose, 9.1; Xylose, 42.8; Galactose, 2.3; Arabinose, 4.6; Acetic acid, 0.8 Glucan, 41.63%; Xylan, 17.24%; Arabinan, 0.68% Xylose, 21.5; Arabinose, 2.95; Glucose, 5.84 Glucose, 50.9; Xylose 33.1 Simultaneous saccharification and fermentation (SiSF), Glucose, 80 g L−1
Microorganism
Fermentation conditions ◦
−1
References
E. coli MM160
37 C, pH: 6.5, 150 rpm, 24 h
29.0 g L
27
Candida tropicalis JH030
30 ◦ C, pH: 6.0, 100 rpm, 24 h
3.2 g L−1
31
Pachysolen tannophilus DW06
30 ◦ C, pH: 5 150 rpm
0.34 g g−1
32
S. cerevisiae D5A
30 ◦ C, pH: 4.8, 200 rpm, 48 h
23 g 100 g−1 biomass
33
C. shehatae NCIM 3501
30 ◦ C, 150 rpm, 24 h
0.48 g g−1 , 8.67 g L−1
9
S. cerevisiae 424A LNH-ST Zymomonas mobilis
30 ◦ C, 150 rpm, 120 h Enzymatic hydrolysis at 50 ◦ C, 12 h and fermentation at 30 ◦ C, pH: 5.5
33.7 g L−1 60 g L−1
8 34
efficient breakdown of polysaccharides present in the cell walls of lignocellulosics.15,19 The effects of different enzyme loadings on the hydrolysis efficiency of SB after pretreatments at different conditions are being summarized in Table 1. Different enzyme loadings are required to maximum hydrolysis of SB after pretreatment under different conditions.
SUGARCANE BAGASSE AND VALUE-ADDED PRODUCTS OF COMMERCIAL SIGNIFICANCE Ethanol SB has long been studied for industrial applications, including ethanol production. Theoretically, a single ton of SB could yield up to 300 L of ethanol.11 However, there are several parameters that directly affect ethanol yield, such as the quality of bagasse and the process employed for ethanol production.11 It has been predicted that ∼12 000 to 15 000 L ethanol ha−1 could be produced if the sugarcane juice and bagasse were processed for ethanol production.11,12 This amount could be even higher if SL was employed in the process.12 Both enzymatic and acidic hydrolysates of SB have been employed for ethanol production using different
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Ethanol production (g L−1 or g g−1 )
ethanologenic strains (Pichia stipitis, Candida shehatae, Pachysolen tanophillus, native and recombinant Saccharomyces cerevisiae, recombinant Escherichia coli, and Zymomonas mobilis) under various cultivation techniques.10 Table 2 summarizes ethanol production from SB hydrolysates using different microorganisms. The ethanol production and yield may vary depending upon the process and the conditions used for fermentation as well as the microbial strain used in the conversion.4 Separate hydrolysis and fermentation (SHF) and simultaneous saccharification and fermentation (SSF) have been implemented using SB for ethanol production.19 Santos et al.34 obtained maximum cellulose-to-ethanol conversions (∼60%) with volumetric productivity 0.29–0.30 g L−1 h−1 in pre-saccharification assisted SSF from SB. In this study, SB was first treated with acid using H2 SO4 (1% (v/v), solid/liquid ratio 1 : 2) at 121 ◦ C for 30 min followed by separation of solid biomass (cellulignin) which was again treated with NaOH (4% (v/v), solid/liquid ratio of 1 : 20) at 121 ◦ C for 30 min. Afterwards, the treated solution was used for SSF. Ferreira et al.35 carried out SSF for ethanol production using a recombinant S. cerevisiae harboring a β-glucosidase gene
c 2011 Society of Chemical Industry
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Bio-industrial benefits of sugarcane bagasse and leaves
Table 3.
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Utilization of SB for production of industrial enzymes under varying cultivation conditions Microorganism
Mode of cultivation
Product titers (g L−1 or g g−1 )
References
Penicillium echinulatum 9A02S1 A. heteromorphus Bacillus subtilis KCC103 Rhizopus homothallicus B. licheniformis KBR6 Penicillium viridicatum RFC3 Kluyveromyces marxianus NRRL Y-7571
SSF SSF SmF SSF SSF SSF SSF
36.38 ± 5.38 U g−1 dry material 2.9 IU mL−1 67.4 U mL−1 826 U g−1 dry material 0.56 ± 0.03 U mL−1 300 U g−1 substrate 391.9 U g−1 dry material
39 40 41 42 43 44 45
Bio-products Xylanase Laccase Alpha-amylase Lipase Tannase Pectate lyase Inulinase
and obtained 60 g L−1 ethanol production. However, studies on consolidated bioprocesses using SB for ethanol production have yet to be conducted. Dias et al.12 suggested the importance of process integration in sugarcane processing mills. Under thermal integration, SB was hydrolyzed in an organosolv process catalyzed by dilute acid and then utilized for conventional production of ethanol from sugarcane juice. These studies revealed the use of SB and lignin as auxiliary fuels to fulfill the energy demands of the biorefinery. In addition, Ojeda et al.13 reported a case study where a simulation of process integration was used to compare biorefinery inputs and outputs considering the residual biomass produced by the sugaralcohol industries, and reported the highest ethanol yield (169.3 L ton−1 of SB) in an integrated process (organosolv + simultaneous saccharification and co-fermentation (SSCF). Xylitol D-xylitol is another value-added product that can be produced from SB/SL by microbial fermentation to cater for its large demand in food and pharmaceutical industries.36,37 It is a five carbon sugar alcohol that is naturally found in various fruits and vegetables. Due to its anti-carcinogenicity, tooth rehardening and remineralization properties, D-xylitol has been widely applied in the pharmaceutical industry, odontological formulations, and in food industries.37 Being a sugar substitute, xylitol has been used in dietary foods especially for insulin-deficiency patients.36,37 The fermentative production of xylitol is possible from hemicellulosic hydrolysates of SB. The acid hydrolysates of SB primarily contain xylose sugar. Other sugars like arabinose, mannose, galactose, and glucose are also present in very low concentrations, along with inhibitors such as furans, phenolics, and weak acids. It is necessary to eliminate fermentation inhibitors from the hemicellulosic hydrolysates prior to fermentation. Several physical (evaporation, membrane separation), chemical (calcium hydroxide overliming, activated charcoal and/or ion-exchange adsorption), and biological methods (microbial or enzymatic treatments) have been applied to eliminate fermentation inhibitors.9,23 Yeast species (mainly Candida sp.) have been known to produce xylitol from pentose-rich SB hydrolysates as reviewed by Prakasham et al.37 SB has also been found an excellent carrier for entrapping Candida guilliermondii cells for the continuous production of xylitol.22 Semi-continuous production of xylitol was also attempted by Carvalho et al.38 using calcium-alginate-entrapped C. guilliermondii FTI 20 037 cells growing on SB hydrolysate, which showed improved xylitol production (g L−1 ) 25.9, 46.8, and 48.7 after three consecutive cycles of fermentation. SB has been reported on multiple occasions in research and development as potential substrate for xylitol production, however, the industrial output of xylitol from SB is yet to come.
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Industrial enzymes SB has been used for the production of industrial enzymes such as xylanase, cellulase, amylase, and laccase by certain bacteria and fungi, employing solid-state fermentation (SSF) or submerged fermentation (SmF) systems. Table 3 shows that SB has been utilized for production of various enzymes under SSF or SmF conditions. Among others, cellulase and xylanase have been studied extensively for production from SB.5,40 Singhania et al.46 compared cellulase production from SB with production from other lignocellulosic materials such as wheat bran, cassava bagasse, and rice straw under SSF by Trichoderma reesei NRRL 11 460. The maximum production of cellulase (154.58 U gds−1 ) was reported from SB, followed by wheat bran, cassava bagasse, and rice straw. The cost of cellulase plays a vital role in the success of biorefineries. A potential technology has yet to be investigated that can provide a feasible approach to the cost-effective production of cellulase with high titers.
SUGARCANE BAGASSE DERIVED MICROBIAL METABOLIC PRODUCTS OF COMMERCIAL INTEREST SB has also been explored for the production of various organic acids (citric acid, lactic acid, gluconic acid, etc.) using different cultivation techniques and with a variety of microorganisms. Borges and Pereira49 employed SB hemicellulosic hydrolysate for succinic acid production by Actinobacillus succinogenes. Singh et al.48 used SB as an inert support for the growth of fungi Aspergillus niger mycelium for gluconic acid production under SSF and a semi-solid state fermentation (SmSF) system with a stabilized mutant strain ORS-4.410. A plant hormone, gibberellic acid (GA), was produced under SSF conditions by Gibberella fujikuroi, NRRL 2278 using SB. An excellent growth of biomass was observed, but only a trace amount of GA was noted during the fermentation reaction.50 Apart from ethanol, xylitol, enzymes, and organic acids, SB has been employed to make other value-added products of commercial interest such as antibiotics, animal feed, biohydrogen, alkaloids, and pigments.4 Nampoothiri and Pandey50 used SB to produce L-glutamic acid and reported a yield of 80 mg L−1 glutamic acid g−1 dry bagasse under an SSF system. The production of a single-cell protein with Candida langeronii RLJY-019 using SB has also been established under SmF cultivation.53 SB has been employed as an alternative packing material for biofiltration of benzene-polluted gaseous streams. Maximum elimination of benzene was observed using 3.50 and 3.80 gm−3 packing material h−1 with raw and ground SB.52 A summary of various other value-added products of commercial significance is provided in Table 4. SB has
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Table 4.
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Production of value added products of commercial interest from SB under various cultivation conditions
Organic acids
Microorganisms
Lactic acid, acetic acid, formic acid, ethanol Gluconic acid Succinic acid L-glutamic acid Nigerloxin Penicillin G Single-cell protein
Lactococcus lactis IO-1
SmF
A. niger ORS- 4.410 Actinobacillus succinogenes Brevibacterium sp. A. niger van Tieghem Penicillium chrysogenum P2-4 Candida langeronii RLJ Y-019
SSF SmF SSF SSF SSF SmF
Red pigment
Penicillium sp. NIOM-02
SSF
the potential for strong commercialization. Despite this, no significant approach has been developed to harness its commercial potential as a raw substrate. The molecular elements of microbial metabolism using SB have not been established, which may assist in efficient utilization of SB for products of commercial interest.
NON-BIOTECHNOLOGICAL APPLICATIONS OF SUGARCANE BAGASSE SB has also been used in conventional applications, including as a cheaper source of energy. Burning it in boilers for steam generation is the most common application in sugar and alcohol producing industries.4 Apart from steam generation, SB plays major roles in the electricity generation and pulp and paper production industries.55 In one study, SB was fractionated into cellulose, hemicellulose, and lignin by a proprietary steam explosion process, followed by downstream purification, revealing that SB can be utilized to produce high-value plastics.56 In another potential application, Ou et al.57 studied phenolic acids that were released from SB by alkaline hydrolysis at 30 ◦ C and purified with anion exchange resin. The main component of the purified bagasse hydrolysate was revealed to be p-coumaric acid rather than ferulic acid. This purified product showed the same antioxidant activity, reducing power, and free radical scavenging capacity as the standard p-coumaric acid. In another attempt, SB was anaerobically digested to produce methane,55 and the digested residue and fresh bagasse were pyrolyzed separately into biochar at 600 ◦ C in a nitrogen environment. This study suggests that efficient use of SB under anaerobic digestion and pyrolysis to produce biochar may be an economically and environmentally beneficial use of agricultural wastes.55 In a different application of SB, Gonzalez et al.58 developed a novel process for synthesis of diverse nanometric materials (silica oxide) with specific crystal arrays as precursors to agro-industrial wastes by employing vermicompost with annelids (Eisenia foetida). In road transportation, it is a challenge to develop low-emission vehicles with high specific power dealing with specific energy. Super capacitors, or electrochemical double-layer capacitors, are a promising high-power technology that can meet peak power demands in fuel cell electric vehicles. Rufford et al.59 studied the characterization and electrochemical performance of activated carbons prepared by the ZnCl2 activation of sugarcane bagasse. Their study showed that SB carbons prepared with a ZnCl2 ratio of 3.5 were the most stable electrochemical performer at fast charge–discharge rates.59
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Product titers (g L−1 or g g−1 )
Fermentation conditions
10.85 g L−1 , acetic acid, 7.87; formic acid, 6.04 and ethanol, 5.24 106.5 g dm−3 (94.7% yield) 22.5 g L−1 80 mg glutamic acid g−1 dry bagasse 2.95 mg g−1 dry substrate 7000 µg g−1 bagasse 48.2, 1.4, 5.8 and 23.4% of total protein, DNA, RNA and carbohydrate Red Pigment scavenged 91% 2, 2 di-phenyl-1-pycrylhydrazyl radicals
References 47 48 49 50 51 52 53 53
SB has been explored in many other applications, including the removal of heavy metal ions from wastewater, as reviewed by Wan Ngah and Hanafiah.60 These proven non-biological applications suggest that SB could play a pivotal role in best economic utilization, as it is abundantly available in nature as a renewable, cheap, and widespread residue in tropical countries. Therefore, it is important to point out that in the developing world, SB is the raw material for 20% of total paper production. In the entire world, 10% of all the available bagasse is used for paper production (www.innovations-report.com).
BIO-INDUSTRIAL SIGNIFICANCE OF SUGARCANE LEAVES/TRASH SL has yet to be explored for biological processes. The cell walls of SL are composed of 57.5% carbohydrate, demonstrating the potential for the bioconversion of products of commercial significance, including ethanol as biofuel. However, the abundance of lignin (36.1%) and silica (6.96%) may limit the industrial and veterinary acceptability of SL.61 Regardless of the complex chemical composition of its cell wall, SL was hydrolyzed by sulfuric acid at varying temperatures, acid loads, hydrolysis times, and solid : liquid ratios in a fractional factorial and central composite design. The optimal conditions at 130 ◦ C with 2.9% w/v H2 SO4 , solid : liquid ratio (1 : 10) for 30 min residence time allowed formation of xylose (56.5 g L−1 ), corresponding to a recovery of 85.1% from the hemicellulosic fraction of SL (Moutta et al., unpublished work). Krishna et al.6 reported ethanol production (2% w/v) from SL employing SSF with cellulases from Trichoderma reesei QM 9414 and S. cerevisiae NRRL-Y-132. Ferreira-Leit˜ao et al.18 evaluated the saccharification of SL into glucose (97.2% theoretical yield) after pretreatment with steam at 220 ◦ C for 5 min. Silva et al.62 reported enzymatic hydrolysis yield of glucose (77.6%) and xylose (56.8%) based upon the total structural carbohydrates present in ball milled pretreated sugarcane leaves straw and this sugar solution when fermented by S. cerevisiae showed 91.8% ethanol yield under submerged fermentation conditions. Another study of enzymatic digestibility (95–98%) by the coordinated action of cellulases and hemicellulases was conducted using SL.8 The released sugars were converted into ethanol by S. cerevisiae 424A LNH-ST with appreciable ethanol concentration (34–36 g L−1 ) and yield (92%). Singh et al.7 processed dried SL after microbial pretreatment for the reduction of C : N ratio in conjunction with cellulase production by selective bioagents including fungi and bacteria. Microbial pretreatment of sugarcane
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Bio-industrial benefits of sugarcane bagasse and leaves
Table 5.
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Factors and procedural steps governing the commercialization of SB/ST with respect to impact on cost incurred
Mode of application
Procedural steps involved
Cultivation type
Bio-products
Direct
Mild pretreatment, washing
Industrial enzymes, organic acids, pigments, antibiotics etc.
Indirect
Auto hydrolysis, Pretreatment with dilute acid, detoxification Alkaline, biological pretreatment, enzymatic hydrolysis
Solid state fermentation (SSF) or submerged fermentation (SmF) or their modifications SmF
Specialized applications ∗
Mild pretreatment, washing
SHF (Separate hydrolysis and fermentation), Simultaneous saccharification and fermentation (SiSF) Consolidated bio-processing (CBP) Immobilization
Mild pretreatment
Bioremediation
Impact on cost incurred∗
Xylitol, ethanol, 2, 3 butanediol, single cell protein Ethanol
+ ++ ++ ++
Microbial cells attached on pretreated SB Dye decolorization
++ + ++
Impact on cost incurred in the process: + moderate, ++ considerable, +++ strong.
trash caused the reduction in C : N ratio from 108 : 1 to a varying range of approximately 42 : 1 to 60 : 1. The maximum 61% reduction in C : N ratio was achieved with Aspergillus terreus, followed by Cellulomonas uda (52%), Trichoderma reesei, and Zymomonas mobilis (49%). These microorganisms were also able to produce in situ cellulase by triggering the degradation of sugarcane trash. Maximum cellulase production came from A. terreus (12-fold), followed by C. uda (10-fold), Cellulomonas cartae (9-fold), and Bacillus macerans (8-fold).7 Saad et al.63 reported the impact of fungal pretreatment of sugarcane leaf straw for organosolv pulping resulting in 40% reduction in lignin, which ameliorated 2.4-fold cellulose degradation after enzymatic hydrolysis. Sugarcane trash (SL+Tops) was used for ammonium carboxylate production under long-term air-lime pretreatment/mixed-culture fermentation using marine microorganisms.64 The study revealed over 75% production of ammonium acetate by a mixed culture of marine microorganisms at 55 ◦ C. In another study,65 ST was amended for the vermistabilization of municipal sewage sludge by epigeic Eisenia fetida, showing their optimum growth by reducing organic matter (12.7%) and simultaneously mitigating the metal toxicity of sludge. Jayasinghe et al.66 attempted to improve the growth and nutrition of lettuce using ST-based sewage sludge. These studies promote the utilization of ST-based growth medium in horticulture as an alternative to the widely used and expensive peat. Roopashree et al.67 evaluated the potency of ST as compost under field conditions using chilli as the test crop. The results revealed that combining trash compost with chemical fertilizers on a 50% basis was helpful in improving the growth and yield of green chillies (10.757 to 12.627 ton ha−1 ) compared with applying ST alone (8.44 to 10.239 tone ha−1 ). Among products of commercial significance, Mane et al.68 exploited ST for oxalic acid production (42.9–51.6% w/w) using a nitric oxide oxidation process. SL was explored for the development of a low-density biomass gasification system for thermal applications,69 and the efficacy of this system was assessed for more than 700 h ex situ, generating output levels of 288–1080 MJ h−1 . Rossy et al.70 attempted to develop an essence of SL through a spraying and freeze-drying procedure, and found that this essence improved the taste of flavored calcium supplements, food, beverages, chewing gums, and oral care products. In another promising application, the Appropriate Rural
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Technology Institute (ARTI) developed a technology for producing briquetted charcoal from ST (http://www.arti-india.org).
COMMERCIAL EVALUATION OF BIO-PRODUCTS FROM SB/ST Bio-products derived from SB/ST are considered a breakthrough to replace chemically synthesized products in industries. In particular, they offer tremendous opportunities for chemical industries to develop unique functionality and marketing benefits due to their sustainability, eco-friendly assessment and their vast availability in nature.71 Looking at the copious amount of SB and ST in the world and their practical feasibility for the production of value-added products, this feedstock can be referred as ‘biological or green currency’. Therefore, the importance of SB/ST as a sustainable source of energy or other valuable products has become a subject of intense research and commercial interest.4,10,12,71 However, the market for white biotechnology based products including SB and ST appears to be small (3–4%) on a global industry scale.71 Despite the socio-economic advantages, environmental benefits and technological developments, entrepreneurs are hesitant to invest in agro-based biotechnology units. Recently, corporate business has shown their interest in biofuels promotion with limited investment in research. Table 5 highlights the cost decisive factors of various other applications of SB and ST The bioconversion of SB/ST into value-added products such as xylitol, organic acids, and industrial enzymes is profitable business compared to ethanol production.4 In general, the cost of raw material such as sugarcane and maize single handedly contributes 34% of the total cost of bioethanol production. Tabular data (Table 6) reveals that the cost of biomass and cellulases has maximum impact (nearly 70%) on bioethanol production. The total cost of bioethanol production from SB/ST can be brought down if combined approaches like cellulase production, hydrolysis and fermentation of released sugars into ethanol can be merged in a single unit. Traditional challenges such as detoxification and recovery of sugars, etc. will remain part of the process for ethanol production. Dias et al.12 performed a process simulation study in which bioethanol was produced from sugarcane juice and SB after pretreatment with an organosolv process with dilute acid hydrolysis in a process integration using multi-pressure distillation columns allowing cost reduction of hot utilities requirements. ST
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Table 6. Cost wise impact of main factors on bioethanol production from sugarcane bagasse (Source: Viikari72 ) Parameter Biomass Feed handling Pretreatment Saccharification and fermentation Cellulase Distillation and solid recovery Wastewater treatment Boiler/energy Utilities Storage
Cost incurred (%) 34 5 17.5 8.5 36 11 2 8.5 4 1
and lignin can be utilized as auxillary fuels to fulfill the energy requirements of biorefinery with hydrolysis. Despite the ongoing efforts, a joint venture of research and policy is required to develop the cost-effective production of industrially important bio-products.
FUTURE PERSPECTIVES AND CONCLUSION The byproducts generated during agro-industrial processing of sugarcane, SB and SL, constitute potential sources of carbohydrates that can be used to generate valuable products of commercial interest. Bio-industrial applications appear to provide sustainable, economic, environmental, and strategic advantages, with breakthroughs in micro-biotechnology offering huge potential opportunities. SB has already been successfully converted into many value-added products such as ethanol, xylitol, organic acids, industrial enzymes, and other important specialty chemicals, as summarized in Fig. 2. Scaling up to the pilot scale, however, is still a necessity. Such a step forward in the developing world would be highly rewarding. For instance, it has already been foreseen that 16 times more energy could be produced if the entire sugarcane plant were used by the alcohol industry, including SB in the process. The energy generation could be increased even more if SL were added to the processing cycle. The increasing price of gasoline may be remedied by SB-derived biofuel in the near future. In the sugar- and alcohol-producing industries, integration of process operations like hydrolysis, detoxification, fermentation, and distillation would be an effective strategy to maximize the efficient utilization of raw substrates. Currently, SB is mostly burned in boilers as a cheaper source of energy. The available technology for bioethanol production from SB polysaccharides cannot afford a competitive price for ‘second-generation ethanol’. Therefore, alternative processes to convert SB and SL/ST into value-added products of commercial significance such as xylitol, enzymes, organic acids, antibiotics, and single-cell protein would contribute to economizing the entire process.
ACKNOWLEDGEMENT We are grateful to FAPESP (THEMATIC PROJECT-BIOEN PROC: 2008/57926-4 and 2010/11258-0) and CNPq for financial support. The authors also thank Dr Ellen C. Giese for critical reading of the manuscript and valuable suggestions.
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REFERENCES ¨ ¨ 1 Hatti-Kaul R, Tornvall U, Gustafsson L and Borjesson P, Industrial biotechnology for the production of bio-based chemicals a cradleto-grave perspective. Trends Biotechnol 25:119–124 (2007). 2 Somerville C, Youngs H, Taylor C, Davis SC and Long SP, Feedstocks for lignocellulosic biofuels. Science 329:790–792 (2010). 3 Chandel AK and Singh OV, Weedy lignocellulosic feedstock and microbial metabolic engineering: advancing the generation of ‘biofuel’. Appl Microb Biotechnol 89:1289–1303 (2011). 4 Pandey A, Soccol CR, Nigam P and Soccol VT, Biotechnological potential of agro-industrial residues. I: sugarcane bagasse. Bioresource Technol 74:69–80 (2000). 5 Parameswaran B, Sugarcane bagasse. in Biotechnology for AgroIndustrial Residues Utilization, ed. by Nigam P and Pandey A. Springer, Netherlands (2009). 6 Krishna SH, Prasanthi K, Chowdary GV and Ayyanna C, Simultaneous saccharification and fermentation of pretreated sugarcane leaves to ethanol. Process Biochem 33:825–830 (1998). 7 Singh P, Suman A, Tiwari P, Arya N, Gaur A and Shrivastava AK, Biological pretreatment of sugarcane trash for its conversion to fermentable sugars. WorldJMicrobiolBiotechnol 24:667–673 (2008). 8 Krishnan C, Sousa LC, Jin M, Chang L, Dale BE and Balan V, Alkalibased AFEX pretreatment for the conversion of sugarcane bagasse and cane leaf residues to ethanol. Biotechnol Bioeng 107:441–450 (2010). 9 Chandel AK, Kapoor RK, Singh AK and Kuhad RC, Detoxification of sugarcane bagasse hydrolysate improves ethanol production by Candida shehatae NCIM 3501. Bioresource Technol 98:1947–1950 (2007). 10 Soccol CR, Vandenberghe LPS, Medeiros ABP, Karp SG, Buckeridge MS, Ramos LP, Pitarelo AP, Ferreira-Leit˜ao V, Gottschalk LMF, Ferrara MA, Bon EPS, Moraes LMP, Araujo ´ JA and Torres FAG, Bioethanol from lignocelluloses: status and perspectives in Brazil. Bioresource Technol 101:4820–4825 (2010). 11 Cerqueira-Leite RC, Leal MRLVL, Cortez L, Griffin WM and Scandiffio MIG, Can Brazil replace 5% of the 2025 gasoline world demand with ethanol? Energy 34:655–661 (2009). 12 Dias MOS, et al, Production of bioethanol and other bio-based materials from sugarcane bagasse: integration to conventional bioethanol production process. Chem Eng Res Design 87:1206–1216 (2009). ´ 13 Ojeda K, Avila O, Su´arez J and Kafaro V, Evaluation of technological alternatives for process integration of sugarcane bagasse for sustainable biofuels production – Part 1. Chem Eng Res Design 89:270–279 (2010). 14 Chandel AK, Singh OV, Chandrasekhar G, Rao LV and Narasu ML, Key-drivers influencing the commercialization of ethanol based biorefineries. J Comm Biotechnol 16:239–257 (2010). 15 Zhao X, Peng F, Cheng K and Liu D, Enhancement of the enzymatic digestibility of sugarcane bagasse by alkali-peracetic acid pretreatment. Enzyme Microb Technol 44:17–23 (2009). 16 Canilha L, Santos VTO, Rocha GJM, Silva JBM and Giulietti M, A study on the pretreatment of a sugarcane bagasse sample with dilute sulfuric acid. J Ind Microbiol Biotechnol 38:1467–1475 (2011). 17 Hatfield R and Fukushima RS, Can lignin be accurately measured? Crop Sci 45:832–839 (2005). 18 Ferreira-Leit˜ao V, Perrone CC, Rodrigues J, Franke APM, Macrelli S and Zacchi G, An approach to the utilization of CO2 as impregnating agent in steam pretreatment of sugarcane bagasse and leaves for ethanol production. Biotechnol Biofuels 3:1–8 (2010). 19 Chandel AK, Chan ES, Rudravaram R, Narasu ML, Rao LV and Ravidra P, Economics and environmental impact of bioethanol production technologies: an appraisal. Biotechnol Mol Biol Rev 2:14–32 (2007). 20 Kumar P, Barrett DM, Delwiche MJ and Stroeve P, Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind Eng Chem Res 48:3713–3729 (2009). 21 Pandey A, Selvakumar P, Soccol CR and Nigam P, Solid state fermentation for the production of industrial enzymes. Curr Sci 77:149–162 (1999). 22 Santos DT, Sarrouh BF, Rivaldi JD, Converti A and Silva SS, Use of sugarcane bagasse as biomaterial for cell immobilization for xylitol production. J Food Eng 86:542–548 (2008). 23 Parawira W and Tekere M, Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit Rev Biotechnol 31:20–31 (2011).
c 2011 Society of Chemical Industry
J Chem Technol Biotechnol (2011)
Bio-industrial benefits of sugarcane bagasse and leaves 24 Kuo CH and Lee CK, Enhanced enzymatic hydrolysis of sugarcane bagasse by N-methylmorpholine-N-oxide pretreatment. Bioresource Technol 100:866–871 (2009). 25 Carrasco C, Baudel HM, Sendelius J, Modig T, Roslander C, Galbe M, ´ G, SO2 -catalyzed steam Hahn-H¨agerdal B, Zacchi G and Liden pretreatment and fermentation of enzymatically hydrolyzed sugarcane bagasse. Enzyme Microb Technol 46:64–73 (2010). 26 Monte JR, Brienzo M and Milagres AMF, Utilization of pineapple stem juice to enhance enzyme-hydrolytic efficiency for sugarcane bagasse after an optimized pre-treatment with alkaline peroxide. Appl Energy 88:403–408 (2011). 27 Geddes CC, Mullinnix MT, Nieves IU, Peterson JJ, Hoffman RW, York SW, Yomano LP, Miller EN, Shanmugam KT and Ingram LO, Simplified process for ethanol production from sugarcane bagasse using hydrolysate-resistant Escherichia coli strain MM160. Bioresource Technol 102:2702–2711 (2011). 28 Rabelo SC, Filho RM and Costa AC, Lime pretreatment of sugarcane bagasse for bioethanol production. Appl Biochem Biotechnol 153:139–150 (2009). 29 Sindhu R, Binod P, Satyanagalakshmi K, Janu KU, Sajna KV, Kurien N, Sukumaran RK and Pandey A, Formic acid as a potential pretreatment agent for the conversion of sugarcane bagasse to bioethanol. Appl Biochem Biotechnol 162:2313–2323 (2010). 30 Adsul MG, Ghule JE, Shaikh H, Singh R, Bastawde KB, Gokhale DV and Varma AJ, Enzymatic hydrolysis of delignified bagasse polysaccharides. Carbohyd Polym 62:6–10 (2005). 31 Huang CF, Jiang YF, Guo GL and Hwang WS, Development of a yeast strain for xylitol production without hydrolysate detoxification as part of the integration of co-product generation within the lignocellulosic ethanol process. BioresourceTechnol 102:3322–3329 (2011). 32 Cheng KK, Cai BY, Zhang JA, Ling HZ, Zhou YJ, Ge JP and Xu JM, Sugarcane bagasse hemicellulose hydrolysate for ethanol production by acid recovery process. Biochem Eng J 38:105–109 (2008). 33 Aita GA, Salvi DA and Walker MS, Enzyme hydrolysis and ethanol fermentation of dilute ammonia pretreated energy cane. Bioresource Technol 102:4444–4448 (2011). 34 Santos DS, Camelo AC, Rodrigues KCP, Carlos LC and Pereira N, Ethanol production from sugarcane bagasse by Zymomonas mobilis using simultaneous saccharification and fermentation (SSF) process. Appl Biochem Biotechnol 161:93–105 (2010). 35 Ferreira V, Faber MO, Mesquita SS and Jr NP, Simultaneous saccharification and fermentation process of different cellulosic substrates using a recombinant Saccharomyces cerevisiae harbouring the β-glucosidase gene. Electron J Biotechnol 13:1–7 (2010). 36 Carvalho W, Canilha L and Silva SS, Semi-continuous xylose-to-xylitol bioconversion by Ca-alginate entrapped yeast cells in a stirred tank reactor. Bioprocess Biosyst Eng 31:493–498 (2008). 37 Prakasham RS, Rao RS and Hobbs PJ, Current trends in biotechnological production of xylitol and future prospects. Curr Trends Biotechnol Pharm 3:8–36 (2009). 38 Carvalho W, Canilha L and Silva SS, Semi-continuous xylitol bioproduction in sugarcane bagasse hydrolysate: effect of nutritional supplementation. Braz J Pharm Sci 43:47–53 (2007). 39 Camassola M and Dillon AJ, Cellulases and xylanases production by Penicillium echinulatum grown on sugarcane bagasse in solid-state fermentation. Appl Biochem Biotechnol 162:1889–1900 (2010). 40 Singh A, Bajar S, Bishnoi NR and Singh N, Laccase production by Aspergillus heteromorphus using distillery spent wash and lignocellulosic biomass. J Hazard Mater 176:1079–1082 (2010). 41 Rajagopalan G and Krishnan C, Alpha-amylase production from catabolite derepressed Bacillus subtilis KCC103 utilizing sugarcane bagasse hydrolysate. Bioresource Technol 99:3044–3050 (2008). 42 Rodriguez JA, Mateos JC, Nungaray J, Gonza’lez V, Bhagnagar T, Roussos S, Cordova J and Baratti J, Improving lipase production by nutrient source modification using Rhizopus homothallicus cultured in solid state fermentation. Process Biochem 41:2264–2269 (2006[My). p. 43 Mohapatra PKD, Mondal KC and Pati BR, Production of tannase by the immobilized cells of Bacillus licheniformis KBR6 in Ca-alginate beads. J Appl Microbiol 102:1462–1467 (2007). 44 Ferreira V, da Silva R, Silva D and Gomes E, Production of pectate lyase by Penicillium viridicatum RFC3 in solid-state and submerged fermentation. Int J Microbiol 2010:1–8 (2010).
J Chem Technol Biotechnol (2011)
www.soci.org 45 Mazutti MA, Zabot G, Boni G, Skovronski A, Oliveira D de, Luccio MD, Rodrigues MI, Treichel H and Maugeri F, Optimization of inulinase production by solid-state fermentation in a packed-bed bioreactor. J Chem Technol Biotechnol 85:109–114 (2006). 46 Singhania RR, Sukumaran RK, Pillai A, Prema P, Szakacs G and Pandey A, Solid-state fermentation of lignocellulosic substrate for cellulase production by Trichoderma reesei NRRL 11460. Ind J. Biotechnol 5:332–336 (2006). 47 Laopaiboon P, Thani A, Leelavatcharamas V and Laopaiboon L, Acid hydrolysis of sugarcane bagasse for lactic acid production. Bioresource Technol 101:1036–1043 (2010). 48 Singh OV, Jain RK and Singh RP, Gluconic acid production under varying fermentation conditions by Aspergillus niger. J Chem Technol Biotechnol 78:208–212 (2003). 49 Borges ER and Pereira N Jr, Succinic acid production from sugarcane bagasse hemicellulose hydrolysate by Actinobacillus succinogenes. J Ind Microbiol Biotechnol 38:1001–1011 (2010). 50 Nampoothiri KM and Pandey A, Solid state fermentation for L-glutamic acid production using Brevibacteriumsp. BiotechnolLett 18:199–204 (1996). 51 Hasan HAH, Production and determination of nigerloxin by Aspergillus niger. Int J Agric Biol 9:315–318 (2007). 52 Dom´ınguez M, Mej´ıa A and Revah S, Barrios-Gonz´alez J. Optimization of bagasse, nutrients and initial moisture ratios on the yield of penicillin in solid-state fermentation. World J Microbiol Biotechnol 17:751–756 (2001). 53 Nigam JN, Cultivation of Candida langeronii in sugarcane bagasse hemicellulosic hydrolyzate for the production of single cell protein. World J Microbiol Biotechnol 16:367–372 (2000). 54 Dhale MA and Vijay-Raj AS, Pigment and amylase production in Penicillium sp NIOM-02 and its radical scavenging activity. Int J Food Sci Technol 44:2424–2430 (2009). 55 Inyang M, Gao B, Pullammanappallil P, Ding W and Zimmerman AR, Biochar from anaerobically digested sugarcane bagasse. Bioresource Technol 101:8868–8872 (2010). 56 Shaikh HM, Pandare KV, Nair G and Varma AJ, Utilization of sugarcane bagasse cellulose for producing cellulose acetates: novel use of residual hemicellulose as plasticizer. Carbohyd Polym 76:23–29 (2009). 57 Ou SY, Luo YL, Huang CH and Jackson M, Production of coumaric acid from sugarcane bagasse. Inn Food Sci Emerg Technol 10:253–259 (2009). 58 Gonzalez AE, Martınez-Hernandez AL, Chavez C, Castano VM and Velasco-Santos C, Novel crystalline SiO2 nanoparticles via annelids bio-processing of agro-industrial wastes. Nanoscale Res Lett 5:1408–1417 (2010). 59 Rufford TE, Hulicova-Jurcakova D, Khosla K, Zhu Z and Lu GQ, Microstructure and electrochemical double-layer capacitance of carbon electrodes prepared by zinc chloride activation of sugarcane bagasse. J Power Sources 195:912–918 (2010). 60 Wan Ngah WS and Hanafiah MA, Removal of heavy metal ions from wastewater by chemically modified plant wastes as adsorbents: a review. Bioresource Technol 99:3935–3948 (2008). 61 Patel M and Kumari P, Silicon carbide from sugarcane leaf and rice straw. J Mater Sci Lett 9:375–376 (1990). 62 Silva AS, Inoue H, Endo T, Yano S and Bon EPS, Milling pretreatment of sugarcane bagasse and straw for enzymatic hydrolysis and ethanol fermentation. Bioresource Technol 101:7402–7409 (2010). 63 Saad MBW, Oliveira LRM, Cˆandido RG, Quintana G, Rocha GJM and Gonc¸alves AR, Preliminary studies on fungal treatment of sugarcane straw for organosolv pulping. Enzyme Microb Technol 43:220–225 (2008). 64 Nachiappan B, Fu Z and Holtzapple MT, Ammonium carboxylate production from sugarcane trash using long-term air-lime pretreatment followed by mixed-culture fermentation. Bioresource Technol 102:4210–4217 (2011). 65 Suthar S, Recycling of agro-industrial sludge through vermitechnology. Ecol Eng 36:1028–1036 (2010). 66 Jayasinghe GY, Tokashiki Y, Arachchi IDL and Arakaki M, Sewage sludge sugarcane trash based compost and synthetic aggregates as peat substitutes in containerized media for crop production. J Hazard Mater 174:700–706 (2010). 67 Roopashree DH, Joshi M, Lakshmi TB, Bai SK, Ramesha YM and Krishnamurthy D, Effect of enriched sugarcane trash compost on green chilli yield. Environ Ecol 27:1608–1611 (2009).
c 2011 Society of Chemical Industry
wileyonlinelibrary.com/jctb
www.soci.org 68 Mane JD, Modak HM, Ramaiah NA and Jadhav SJ, Utilisation of sugarcane trash and other cellulosic wastes for production of oxalic acid. Biol Wastes 25:171–76 (1988). 69 Jorapur RM and Rajvanshi AK, Development of sugarcane leaves gasifier for electricity generation. Biomass Bioenergy 8:91–8 (1995). 70 Rossy PA, Davidson RH, Miller KP, Warder IT, Schulman M, Pittet AO, Bolen PL and Hawn RD. Use of spray-dried and freeze-dried sugarcane leaf essence in improving taste of flavored calcium supplements, foodstuffs, beverages, chewing gum, oral care
wileyonlinelibrary.com/jctb
AK Chandel et al.
compositions and calcium supplement. United States Patent 6251463 (2001). 71 Nieuwenhuizen PJ and Lyon D, Anticipating opportunities in industrial biotechnology: sizing the market and growth scenarios. J Comm Biotechnol 17:159–164 (2011). 72 Viikari L, Overcoming technical barriers in bioethanol production from lignocellulosics. European-China Workshop on Liquid Biofuels 4–5 November, Beijing (2004).
c 2011 Society of Chemical Industry
J Chem Technol Biotechnol (2011)
