Application of pretreatment, fermentation and molecular techniques for enhancing bioethanol production from grass biomass – A review

Renewable and Sustainable Energy Reviews 78 (2017) 1007–1032

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Application of pretreatment, fermentation and molecular techniques for enhancing bioethanol production from grass biomass – A review

MARK

⁎

Sonali Mohapatraa, Chinmaya Mishraa, Sudhansu S. Beherab, Hrudayanath Thatoic, a b c

Department of Biotechnology, College of Engineering and Technology, Biju Pattnaik University of Technology, Bhubaneswar 751003, India Officer at Odisha Public Service Commission, Government of Odisha, India Department of Biotechnology, North Orissa University, Sriram Chandra Vihar, Takatpur, Baripada 757003, Odisha, India

A R T I C L E I N F O

A BS T RAC T

Keywords: Grass biomass Pre-treatment Fermentation Molecular tools

Grasses as lignocellulose biomass are promising feed stocks for renewable bioethanol production, since these raw materials have high productivity, require low agricultural inputs, have positive environmental impacts, are easy to process and do not compete with the food crops. However, bioethanol production from grass biomass requires efficient pre-treatment, enzymatic hydrolysis and microbial fermentation processes which varies with types of grass species and the microorganisms used. Pretreatment is an important process for delignification of lignocellulose biomass and is dependent on the type of lignin present in the biomass and the degradation pathway employed for removal of the specific type of lignin. Further, enzymatic hydrolysis converts the cellulose and hemicellulose into monomers, making it feasible for the fermenting microorganisms to convert it into bioethanol where use of improved strain and biomass can yield higher ethanol on industrial scale. This review paper presents an overview of the types of grass species, their composition and cultivation practices, fermentation process used for bioethanol production and genetic tools used for improvement in bioethanol production from grass biomass on a sustainable basis. The current knowledge and future prospect for industrial bioethanol production from grass biomass along with its economic aspects have also been discussed in this review.

1. Introduction The high dependence on fossil fuels has led to uncertainty of petroleum resources and concern about climatic changes, which mandates for search of an alternative and eco-friendly energy source [1]. It is expected that the global fossil fuel reserves will get depleted by next 40–50 years due to rapid increase in the consumption rate of these non-renewable fuels. Thus, biofuels derived from biomass sources can be an alternate source of energy in future. Among the different biofuels, bioethanol produced from biological sources represents one of the potential renewable resources of energy that can replace fossil fuels and gasoline that are particularly utilised in the transport sector [2]. The fact that bioethanol produces nearly twice as much energy as it

consumes, marks its potential as a sustainable biofuel, that can be utilised as an alternative to fossil fuel in commercial scale [2]. Bioethanol can be produced from different biomass such as sugar or starchy materials as well as lignocellulosic biomass which are rich in hexoses and pentosans [2,3]. While, in one hand the use of sugary and starchy biomass as first generation biofuel production leads to high cost of bioethanol production due to the high price of raw materials [4,5], the use of food stocks like sugarcane, corn and cereal grains on the other hand might possibly lead to the food crisis. Biofuels generated from lignocellulosic biomass (second generation biofuel) represent one of the potential renewable sources of energy that are non-polluting and are sustainable [3]. Lignocellulosic biomass are plentily available and can often be locally produced at low cost feedstock for bioethanol

Abbreviations: ABTS, 2, 2′-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid); AFEX, Ammonia fibre explosion; ARP, Ammonia recycles percolation; CBP, Consolidated bioprocess schemes; CF, Co-fermentation; CMC, Carboxymethylcellulose; CMCase, Carboxymethylcellulase; Crl, Crystallinity index; DBU, 1, 8-diazabicyclo [5.4.0] undec-7-ene; DMC, Direct microbial conversion; DP, Degree of polymerization; FPase, Filter paper activity assay for cellulases; GAXs, Glucuararonoxylans; GCE, Guaiacylglycerol-β-guaiacyl ether; GlcA, Glucuronic acid; HBT, Hydroxybenzotriazole; ILs, Ionic liquids; LHW, Liquid hot water pretreatment; LMS, Laccase mediator system; Mg, Megagallons; MEA, Monoethanolamine; MLG, Mixed-linkage glucan; NREL, National renewable Energy Laboratories; PDC, 2-pyrone-4,6-dicarboxylate; PEF, Pulsed-electric- field; QTL, Quantitative trait loci; SHF, Separate hydrolysis and fermentation; SILs, Switchable ILs like; SmF, Submerged fermentation; SOC, Soil organic carbon; SPORL, Sulfite pretreatment to overcome recalcitrance of lignocelluloses; SSCF, Simultaneous saccharification and co-fermentation; SSF, Simultaneous saccharification and fermentation; SsF, Solid state fermentation; TCA, Tricarboxylic acid; Xyl, Xylose ⁎ Corresponding author. E-mail address: [email protected] (H. Thatoi). http://dx.doi.org/10.1016/j.rser.2017.05.026 Received 14 November 2016; Received in revised form 9 March 2017; Accepted 5 May 2017 1364-0321/ © 2017 Elsevier Ltd. All rights reserved.

Renewable and Sustainable Energy Reviews 78 (2017) 1007–1032

S. Mohapatra et al.

quantity of cell wall (cellulose, hemicellulose and lignin) and other cell components (protein, lipid and sugars) in the grass. It has been reported that while the structural carbohydrates in cell wall increase with the maturity of the grasses, the reverse phenomena is observed for the cell components [16]. Whenever the rate of photosynthesis supersedes the rate of plant growth or the plant gets into a stress, carbohydrate accumulation starts in the plants. In these conditions high concentrations of carbohydrates like starch, sugar and fructans can be seen in dry hay of cool season grasses. The carbohydrates are mostly accumulated in the lower regions of the grass stem like stem bases, stolons, corms, and rhizomes [17,18]. More particularly, substantial amounts of soluble carbohydrates are stored in the parenchyma cells that surround the vascular bundles located within internode tissues [19,20]. Hence, these cells can be good targets for enhanced carbohydrate storage in grass biomass, which would result in increased carbohydrate yields successively, not interfering in the plant growth pattern. Further, depending on the temperature or climatic conditions, grasses are divided into tropical and temperate region grasses. Tropical grasses or C4 grasses can withstand optimum temperatures and are high yielding varieties as compared to temperate or C3 grasses due to their highly efficient mode of photosynthesis. Sucrose and fructose are the predominant reserve constituents of temperate-origin grasses while sucrose and starch, are the major constituents of tropicalorigin grasses [21,22]. The type of grass variety and the environmental conditions in which it is cultivated play an important role in determining the chemical composition of the grasses and thereby it's potential to be considered as a bioethanol crop. Therefore, attentive considerations of the ecological aspect serve as an integral part for bioethanol production from grasses. The consideration of the above mentioned factors will be crucial in utilising many underutilised grass varieties in future for sustainable bioethanol production.

production. Biofuels from lignocellulosic biomass have been shown to offer most environmentally attractive and technologically feasible nearterm alternative bioethanol with 94% lower greenhouse gas emissions than that of gasoline [6,7,8]. In a study by Ryan et al., [9] it has been stated that for every 1000 L of bioethanol from lignocellulosic biomass, approximately 2.6Mg carbon dioxide emission is saved. There are different types of lignocellulosic biomasses such as wood based, non-wood biomasses that include agricultural residues, sugar cane bagasse, switch grass, cotton fibre etc. Among the different lignocellulosic biomasses short rotation crops like grasses have high yields of upto 40 Mg/ha/year as compared to corn feedstocks which have yields of 7 Mg/ha/year [10]. In future, these fast growing plants can be targeted as potential energy crops not only because of their high productivity per hectare but also due to their abundancy, availability and utilisation of the whole plants, high percentage of total cellulose and hemicellulose content and comparatively less lignin content [11]. Further, grasses can grow globally in a wide range of geographies, climate and soil types [12]. However, the main bottle neck in large scale ethanol production from grass as lignocellulosic biomass is the technological impediments of breaking down plant biomass (lignin in the cell walls) and releasing carbohydrate polymers (cellulose and hemicellulose) that can be fermented into fermentable sugars and further refined fuels [11]. In order to obtain bioethanol, lignocellulose biomasses have to be pre-treated followed by enzymatic hydrolysis and fermentation. Pretreatment of grass biomass prior to enzymatic hydrolysis is necessary to break the recalcitrant lignin. But grasses have the advantage of low lignin content, which eventually leads to milder pre-treatment conditions [13]. Further, enzymatic hydrolysis converts the cellulose and hemicellulose into monomers, making it feasible for the fermenting microorganisms to convert it into bioethanol. However, improvement in grass biomass and microorganisms (specifically pentose fermenting) by application of molecular techniques in genetic modification of plant biomass and microbes would play significant role for commercialization of bioethanol production from grasses. Further, biofuel production depends upon the availability of the feedstock, production and supply pathways, availability of the technologies and the cost-effectiveness, which varies from region to region.

2.2. Composition and potential of grass biomass for bioethanol production The most favourable biomass resource for biofuel production should be readily available, should have high yielding biomass per dry weight, unwavering desirable chemical concentrations and should be economical [23]. Other features like elevated carbon and hydrogen concentrations and minimum concentrations of oxygen, nitrogen and other organic components are also crucial for a biomass to be considered for bioethanol [24]. In addition to the above mentioned features the importance of a biomass also lies on the fact that the industries using the biomass should produce less effluent and offer low CO2 emission ability. Grasses have the advantage of possessing possibly all these features. The general composition of grasses along with the process of conversion of grasses to bioethanol is represented in Fig. 1. Grasses grow naturally and do not require any special requirements for cultivation, which makes the biomass growth cost effective, as application of fertilizers and pesticides is not a necessity [25]. It also has good above-ground foliage and much denser growth which maximizes the amount of biomass that an acre of land can produce. Additionally, grasses are composed primarily of carbohydrate polymers (cellulose and hemicellulose) and phenolic polymers (lignin) and lower concentrations of various other compounds, such as proteins, acids, salts, and minerals. These carbohydrate polymers, which typically make up twothirds of cell wall dry matter, are polysaccharides that can be hydrolysed to sugars and then fermented to ethanol. Further the carbohydrate concentration in grasses is directly related to the bioethanol yield from biomass and the maturity of the grass is the key factor that determines its quantity in the grass. Another feature that makes grass an attractive energy crop is its potential to increase carbon storage by increasing above and below ground biomass, specifically in C4 grasses.

2. Grass biomass around the world for bioethanol production 2.1. Types of grass biomass There are around 11,369 accepted grass species that have been known worldwide till now [14]. The habitat of these grasses ranges from infertile land mass to well drained fertile soil in varied climatic conditions. Grasses are composed primarily of carbohydrate polymers (cellulose and hemicellulose) and phenolic polymers (lignin) along with other compounds, such as proteins, acids, salts, and minerals. The accumulation of carbohydrate can be attributed to the photosynthetic cycle in plants. The carbohydrate content is not similar for all the types of grasses, and significantly varies due to a lot of factors such as 1) variety of the grass 2) developmental stage of the grasses and 3) the environmental conditions in which it is grown. Among the different varieties of wild and cultivated grasses, bluestems, Indian grass, and switchgrass are some of the most common examples of wild grasses. The cultivated grasses such as smooth broom grass, timothy, meadow foxtail are some of the species that are derived from wild species of grasses. They are developed through different breeding methods viz., pure line selections, mutants, polyploids and inter-generic/interspecific hybrids. Both wild and cultivated grasses are considered as suitable plant biomass because of their high carbohydrate content, their longevity, redevelopment after the cut off, and effective capability to tolerate the drought [15]. The maturity of the grass is the key factor that determines the 1008

Renewable and Sustainable Energy Reviews 78 (2017) 1007–1032

S. Mohapatra et al.

Fig. 1. The representation of lignocellulose content in grasses. (a) Grass;(b) Plant Cell;(c) Lignocellulose structure in cell wall;(d) Lignin polymer structure;(e) Hemicellulose structure; (f) Cellulose structure. Source:http://www.nature.com/scitable/content/ne0000/ne0000/ne0000/ne0000/14464273/rubin_nature07190-f2.2_1_2.jpg.

grass annual yields of 20–36 Mg/h have been reported [33]. The cellulose, hemicellulose and lignin contents generally vary from 37% to 40%, 25% to 29%, 18% to 25% respectively. Moreover, switch grass requires low maintenance with little or no fertilizer application. Morrow et al. [34] has reported that a mature bioenergy switchgrass crop production system would yield 330–380 l of ethanol per Mg of dry switchgrass. These assessments are consistent with those from the studies of Forde et al. [35] and national renewable Energy laboratory's [36] theoretical ethanol yield that assumes conversion of both hexoses and pentoses. Napier grass (Pennisetum purpureum) is a native to eastern and central Africa and has been introduced to most tropical and subtropical countries. It has high cellulosic fibre content, zero utilisation of nitrogenous fertilizers and fast growing capability is an excellent cheap feedstock for ethanol production. The ability of Napier grass to produce adequate biomass under limited nitrogen levels is linked to the occurrence of diazotrophic nitrogen fixing bacteria with the grass. Presence of these bacteria in soil augments the nitrogen requirement of the plant by fixing atmospheric nitrogen [37]. Due to its highly efficient CO2 fixation, it is capable of producing 60 t/ha/yr. of dry biomass under optimal condition and 30 t/ha/yr. of dry biomass under suboptimal condition. Other features that make this grass suitable for bioenergy purposes include the cellulose content of 40–50% by weight followed by hemicelluloses and lignin which is about 20–40% and 10– 25% respectively [38]. Bermuda grass (Conodont dactyl on) is a warm-season perennial grass grown in tropical and subtropical regions [39] especially in the Southern US [40]. The Bermuda grass also has the advantage of good biomass yield of 14.1–24.2 t/ha [41]. Increase in the nitrogenous content of the soil has been seen to enhance the biomass yield from 1.2 to 16.6 t/ha/yr [42]. Bermuda grass has high carbohydrate content (cellulose and hemicellulose) of 40–55% and low lignin content of 20– 25% [43].

This carbon storage competency helps grasses to eliminate carbon dioxide emission nearly to zero during the fermentation processes for bioethanol production [12]. This have been exemplified in a study by Tan et al., 2008, which shows the carbon sequestering capacity of Miscanthus to be 7–9 Mg C ha−1 in the soil in the first four years of cultivation [26]. Accounting the numerous advantages of different grass varieties many research groups have widely studied the biomass for bioethanol production. Among the different varieties the most commonly used herbaceous biomass are Miscanthus sp. followed by switch grass, Napier grass and costal Bermuda grass. Giant miscanthus (Miscanthus x giganteus) which grows fifteen feet tall and is a sustainable feedstock for cellulosic ethanol production and is mostly considered an Asian grass. It is a new leading biomass crop in the United States and is commercially grown in the European Union as a combustible energy source [27]. It has an annual ethanol production yield of 1198 gal per 0.404 ha [28]. Miscanthus x giganteus is a variety of sawgrass that is capable of producing 5–8 times as much ethanol per acre as corn. The main feature distinguishing giant miscanthus from other biomass crops is its high lignocellulose yields with cellulose (40– 60%), hemicellulose (20–40%) and lignin (10–30%) contents [27]. While harvestable miscanthus yields (dry matter) have been estimated to be in the range of 2–44 t/ha, yields of 27–44 t/ha has been reported in Europe and US Midwestern locations and 10–11 t/ha of small-scale trials at spring harvest in Montreal Canada [29,30]. Switchgrass (Panicum virgatum) is a primary biomass crop in the United States. Switchgrass is a native warm-season grass that has been promoted as a model bioenergy crop because of its high-yield potential, low input requirements on marginal soils, and potential for soil carbon sequestration [31]. It has been reported that switchgrass stores large quantities of carbon, with four farms in Nebraska storing an average of 2590 pounds of soil organic carbon (SOC)/acre/year [32]. Typical yields range between 11–24 t/ha, but with newer varieties of switch 1009

40

36

Asia, Polynesia, and Australia

Europe, Asia and North Africa

1010

Intermediate wheat

Indian grass (Sorghastrum nutans) Indian rice grass (Achnatherum hymenoides)

Giant cane (Arundo donax)

Energy cane (hybrids of Saccharum sp)

Cyper grass (Cyperus compactus) Deenanath grass (Pennisetum pedicellatum) Eastern gama grass (Tripsacum dactyloides)

35–37

India

sandy to heavy clay soil, but better growth is observed in moist type of soil. Although occurring on neutral soils, it favours sandy acidic loams with pH 5.1–6.1. It prefers moist soil grows well in a variety of soils with pH greater than 4.0.

32–35

plains, foothills, mountains, and intermountain basins of the western United States

35–38

NM

39

North America

Europe and Western Asia

29

31

Mediterranean Basin and middle east Asia

29

35

NM

5.9–8.3 Mg/hac

–

4 t/acres

8–10 t/ha

17–19 t/ha

24,965 kg/ha

13–14 t /ha

4–19 t/hac/a

60–127 t/ha

80–100 t/hac

100–120 t/ha

80–150 t/hac

5–7 t/ac.

Production/ha

NM

18

21

43

South Asia and Melanesia

23

22.9–26.4

–

57.2 −64.1(total cellulose and hemicellulose)

Eastern US

Soils which are moist, little drained fertile soil that has an annual precipitation of 900– 1500 mm (35–59 in) and a pH of 5.5–7.5.

soils ranging from highly fertile well drained mollisols, through heavy cracking vertisols, infertile acidoxisols, peaty histosols to rocky andisols. Dense stands, particularly in riparian areas – boundary areas between land and streams. It grows well in deep, well-drained floodplain soils and in welldrained upland sandy loam soils. It prefers sandy, coarse textured soils and can also be found on sands, fine sandy loams, silt loams, clay loams, gravelly, rocky and shale soil textures well drained loamy to clayey

2.9 (ASL)

23

~6

20–22

32

~36

25–27

19–21

6

17–19

18–20

6.5–12

L

India and Africa

33

30–32

24

35

21

28

12

H

Grows well in both dry and wet lands

Afghanistan

Southern USA

37

Central and eastern United States.

Soils with low moisture holding capacity, pH, and phosphorus.

Bigblue stem (Andropogon gerardi) Carrot grass (Parthenium hysterophorus) Chrysopogon aciculatus (Andropogon aciculatus) Cocksfoot grass (Dactalis glomeruta) Costal Bermuda grass (Cynodon dactylon)

Prefers deep soils but produces well on moderately shallow sites. It withstands pH ranges from about 5.0–8.5 and is boron tolerant. Grows best in rich,fertile soil.

27

Area around the Mediterranean Sea

C

Good fertile well drained soil and near neutral pH.

Composition (~)

Alfalfa (Medicago sativa.)

Place Of Origin

Adaptation

Grasses

Table 1 Composition and potential of herbaceous biomass for bioethanol production.

0.41–0.47g/g

NM

400 gal/acre

75 L/ton

75 L/ton

386.1 L/ton

–

498 L/ton

208 L/ton

[288,289]

[286,287]

[285]

[282,283,284]

[279,280,281]

[61,278]

[276,277]

[275,43,41,77,40]

[273,274,44]

[272]

[3]

[271]

[269,270]

References

tolerates slightly acidic to mildly saline [290,291] (continued on next page)

It is tolerant of poor and welldrained soils, acid to alkaline conditions, and textures from sand to clay. drought tolerant

High biomass yield, longevity of established fields for decades, adaptation to different soil and climate conditions, non-invasiveness, carbon sequestration capacity, soil phytoremediation ability, and easy integration into existing farming operations High density of energy, favourable cost of production and delivery, produced under stress conditions and so not to compete with land used for food production high growth rate and productivity even on marginal croplands

But can grow in poor sandy or clay soils of unused lands or in fallow rice fields. It spreads quickly and is tolerant of saline and infertile soil.

Tolerant of shade, high temperatures and drought. High tolerance of aluminium drought tolerant

Can grow on abandoned cultivations on poor sandy soils.

–

2171 L/ha

excessive growth rate and wider adaptability

Mostly the stem fraction is used as a source of fermentable sugars to produce cellulosic ethanol. Potentially increasing profitability per acre. More drought tolerant than other warmseason grasses

Advantage as an energy crop

12.14g/L(Actual yield)

400 gal/acre

300 gal/acre

Theoretical ethanol yield

S. Mohapatra et al.

Renewable and Sustainable Energy Reviews 78 (2017) 1007–1032

1011

forming dense pure stands, usually on neutral or alkaline soils. It can grow in semi-shade (light woodland) or no shade. It prefers moist or wet soil grows best on deep, well-drained silt or clay loam but may also establish itself in sandier soils. Does best on fairly fertilie soil, tolerates very high pH 8.0–9.0) Swamplands, plains, and streams, and along the shores and interstate highways

Saw grass ( Cladium mariscus)

Sudangrass (Sorghum vulgare) Switch grass (Panicum virgatum)

Smooth broom grass (Bromus inermis)

Reed canary grass ( Phalaris arundinacea)

found on lower, poorly drained soils along roadsides, ditches, streams, marshes and potholes. It also occurs in floodplains, wet meadows and back dune areas Wet and humus rich soil

Prairie cordgrass ( Spartina pectinata)

27 25–34

28–37

36

20–25

31–33

20–40

24–32

15–18

31

33

32

Hungary

Tropical and subtropical regions of Eastern Africa Continental United States except California and the Pacific Northwest

25–29

38–45

Europe,Asia and north america

California, Arizona, New Mexico, Nevada

39–41

Northern Canada

28–49

40–50

Asia

Rich, moist, well-drained soil to attain maximum growth potential.

28–31

35

5–23 t/hac

3–4 t/ha

– 9–13

4–7 t/ha

7–13 t/hac/

6–9 t/ha

54–60 t/ha

9–54 t/hac

–

18–21

19

12–19

15–28

2000–4000 L/ha

NM

20g/l

1748–4368 L/ha

2621.06 L/ha/ year

1198 gal/acre

[305,306]

[303,304]

[301,302]

[299,300]

[298,237,15]

[296,297]

[295]

[227]

[140,189,172]

[292,293,294]

References

Tolerates very high pH and salinity, [307] most heat and drought-tolerant High cellulose content,Self-seeding and [308,309] resistant to many diseases and pests, high productivity,Low N,P and K (continued on next page)

Cold and drought tolerance, little water or fertilizer inputs. Can tolerate a variety of poor conditions, including soils of various pH, compacted soils, nutrient poor soils. Perennial, it can be vegetatively propagated and it can withstand repeated cutting/harvesting and regenerates, lower content of sulphur in biomass Grows well on seasonally dry sites, tolerates alkaline conditions and high water tables, chilling tolerance. Tolerates alkaline conditions and high water tables Superior drought and water logging tolerance, confer adaptation to a wide range of soil types, Highly productive yields grows in extremely infertile conditions, carbon neutral, absorbing about the same amount of greenhouse gases while it's growing as it emits when burned as fuel resistant to temperature extremes and drought

Early growth and potential productivity

6–13 t/hac/a

–

11–15

200–300 lb/acre

–

–

grow quickly without requiring any economic input; tolerates many soil types and moisture levels. Resistant to many diseases and pests, and can produce high yields with low applications of fertilizer and other chemicals. It is also tolerant to poor soils, flooding, and drought; It uses less water per gram of biomass produced than other plants broad adaptation to diverse sites

0.44–0.46g/g

–

conditions, is cold tolerant, can withstand moderate periodic flooding in the spring, and is very tolerant of fire salt-tolerant grass

Advantage as an energy crop

23

43

Theoretical ethanol yield

0.39–0.42g/g

Production/ha

20–40 t/hac/a

L

20–22 24

H

45–50

C

Composition (~)

Africa

England and Wales

Moist, fertile soil, avoiding waterlogged or light, dry ground

Grows best in deep, fertile soils through which its roots can forage. Deep, friable loams are preferable.

U.S. and Canada

Pakistan and cholistan desert of India South Asia and occurs throughout India along the sides of the river

Place Of Origin

soils ranging from sandy to clayloam in texture

silt plains created each year by the retreating monsoon floods

Dry soil, drought area

textured soils

Adaptation

Napier grass (Pennisetum purpureum schum)

Little bluestem (Schizachyrium scoparium) Meadow foxtail (Alopecurus pratensis) Miscanthus sp.

Kallar grass (Leptochloa fusca) Kans grass (Saccharum spontaneum)

grass ( Thinopyrum intermedium)

Grasses

Table 1 (continued)

S. Mohapatra et al.

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Renewable and Sustainable Energy Reviews 78 (2017) 1007–1032

[313]

[311,312]

8270g/kg –

11.5

7

30

10

28 US, Canada and Europe

255.27 L/dry metric ton

Very wet conditions and is often common in wetlands. Yellow flag (Iris pseudacorus)

Timothy (Phleum pratense)

It is an invasive species and grows as weed in native grasslands, woodlands and other habitats Cool-season forage grass, adapted to temperate, moist environments Tall fesecue (Festuca arundinacea)

Europe, western Asia and northwest Africa

28

10.5 t /ha

14 25 25 Large parts of Europe, Asia and North Africa

Production/ha Place Of Origin Adaptation

Composition (~)

Produces good yields of high quality forage, high yield and relatively low production cost Tolerates submersion, low pH, and anoxic soils 2211 L/ha l/ha

8–14 t/hac L H

Lignocellulosic biomass has a complex and recalcitarant structure which requires a pretreatment step prior to enzymatic hydrolysis and subsequent fermentation for bioethanol production. This prior step is mainly aimed for the disruption of the recalcitrant material of the plant biomass. This increases substrate porosity with lignin redistribution in the cell wall and enables maximal exposure of cellulose surface area for the enzymes to reach an effective hydrolysis with minimal energy consumption and a maximal sugar recovery. Herbaceous biomass like grasses do not require as much as energy as recalcitrant woody material for removal of lignin since grasses have the lowest contents of lignin. However, pretreatment seems to be a prerequisite for efficient enzymatic hydrolysis of grasses [45]. This is because of the fact that although the content of the lignin is low but the main bond types of grass lignin with the cellulose and hemicellulose are the same as those of lignin in wood [46]. Moreover, it is not possible to determine the best pretreatment method for lignocellulose biomass which however depends on factors such as type of biomass and desired products. Keeping this in view many research groups have developed various kinds of pretreatment techniques which are discussed in the subsequent sections. The flowchart representation which briefly summarises the pretreatment category is given in Fig. 2.

Theoretical ethanol yield

3. Bioethanol production from grasses

Grasses

Table 1 (continued)

Other grasses like cocksfoot grass, reed canary grass, big blue stem grass, alfalfa etc. which are also documented to be potential feedstocks for bioethanol production are listed along with the major bioethanol producing grasses in Table 1. The wide scale adaptability of these grasses, the major structural composition of the cell wall of these grasses, their production on dry mass basis and the their theoretical ethanol yields are presented in Table 2. This reported information from several research findings give us information on many grass varieties that remain unexploited for commercial bioethanol production inspite of good amounts of cellulose and low levels of lignin present in them. Further, some grass varieties have also good amounts of hemicellulose present in them. These grasses can be utilised by extraction of the hemicellulose fraction for a pentose fermentation leading to bioethanol production. An example can be cited from the study done by Njouk et al. [44] who had used the hemicellulose fraction of the cocksfoot grass for bioethanol production with an ethanol yield in the range of 89–158 ml/kg of dry biomass. Similarly other features like good productivity of dry biomass per hectare and adaptability to a variety of soil and climatic conditions can be considered for biomass like big blue stem, deenanath grass, energy cane, giant cane, kallar grass, meadow foxtail, reed canary grass and tall fescue grass. Though their annual production per hectare on dry mass basis is not as attractive as the leading grass varieties, still undoubtedly these grasses with qualities like good carbohydrate content, salt, stress and drought tolerant have good potential as biomass for bioethanol production even in arid lands. With minimum or nearly zero maintenance costs these grasses can be cheap sources of biomass for bioethanol production. However, more laboratory scale and pilot scale studies have to be implemented for technological improvements for better ethanol production in industrial levels.

C

Advantage as an energy crop

requirements,high moisture efficiency heat and drought tolerant.

[78,310]

References

S. Mohapatra et al.

3.1. Pretreatment technologies Pretreatment is aimed mainly for delignification of plant biomass. There are different types of pretreatment techniques such as physical (mechanical comminution) [47], chemical (dilute acid or alkali), ammonia percolation, physio-chemical (steam explosion, ammonia fibre expansion (AFEX) [48]), ultrasonication and microwave pretreatment [49], biological pretreatments (e.g. using white rot fungi), sulfite pretreatment to overcome recalcitrance of lignocelluloses(SPORL) [50], pulsed-electric- field (PEF) pretreatment [45], organosolvic pretreatment [51], ozone and liquid hot water (LHW) pretreatments 1012

Glucose 257.1 mg/g raw biomass Xylose 117.5 mg/g raw biomass Glucose 253.8 mg/g raw biomass Xylose 114.7 mg/g raw biomass Reducing sugar- 57.42%

Bermuda grass

1013

Combination pretreatments Alkali+Extursion

NaOH-1.7%,Incubation time- 30 min, +screw speed −122 rpm Temperature- 114 °C

NH3−1.1g,Temperature−80 °C, Incubation time−86 h

Bermuda grass

Low-moisture anhydrous ammonia (LMAA)

269.9 mg/g Glucose 168.9 mg/g Xylose

Cogon grass

1% NaOH at 121 °C for 60 min

Total sugar−39.98 mg/ml

Switch grass

1% H2SO4,Temperature 150 °C,Incubation time 10 min H2SO4−0.6% v/v, Incubation time−20 min, Temperature−127 °C 1.2% H2SO4, Temperature 140 °C Incubation time 30 min Innoculum size−20 ml,Incubation time−3 weeks, microganism-Phanerochaete chrysosporium

Prairie cord grass

Napier grass-dwarf type

Saccharum ravennae

Saccharum arundinaceum

M. sinensis ‘Gracillimus’,

Miscanthus ×giganteus,

Napier grass

91.4% cellulose recovery(in form of glucose and cellobiose) 337.8 mg/g Glucose, 157.6 mg/g Xylose

Switch grass

H2SO4−1.2%,180 °C,

Total sugar 67.2%

Glucan−34.1% Xylan−11.3% Glucan−30.0% Xylan−13.6% Glucan−38.0% Xylan−18.2% Glucan−32.7% Xylan−15.1% Glucan−39.7%,Xylan−21.4%,

Hollocellulose−76.4%, Cellulose−58.3% `

72% reducing sugar Glucan−39.7%,Xylan−21.4%, Glucose−239.6 mg/g Xylose−127.2 mg/g, and total reducing sugars 433.4 mg/g

Switch grass Napier grass-dwarf type Switch grass

Aquoeus ammonia NH3−1.1 g,Temperature−80 °C, Incubation time−86 h Ca(OH)2−0.1%, Temperature−50 °C,Incubation time−24 h

Average cellulose of 18 grass varities −31.85–38.51%, Average hemicellulose- 31.13–42.61%

Napier grass, Dwarf napier grass, King napier grass, Bana grass, Purple guinea grass, Ruzi grass, Pangola grass, Atratum grass, Vetiver grasses

Guinea grass

Alkaline peroxide

Ozonolysis

Biological

Acid

NM

Prairie cord grass

Switchgrass

Reducing sugar- 113.43 mg/ml

Kans grass Ryegrass, Tall fescue, Bentgrass Napier grass

NaOH-0.5%,Temperature-120 °C,Incubation-120 min NaOH-1%,Incubation time−15 min,Temperature180 °C NaOH-7.29%,Incubation time75.48 mins,Temperature- 43.45 °C (NaOH-1.7%,Incubation time- 30 mins), +Extursion pretreatment (screw speed −122 rpm Temperature- 114 °C) 0.75% NaOH, incubation time 30 min, temperature 121 °C NaOH 1%, 30 mins incubation time, temperature 121 °C NaOH-1%,Incubation time- 127.5 min, Temperature- 110 °C

Hollocellulose-88.46% Cellulose-82.21% Reducing sugar-350 mg/g NMa

Napier grass

NaOH-7%,Incubation time-4 h

Release of sugars after pretreatment

Alkaline

Grass variety

Parametres maintained

Pretreatment technology

Table 2 Total sugar/Reducing sugar yields of different types of grasses with different types of pretreatment.

NM

7.1

20.7–59.9% reduction

NM

NM

NM

NM

NM

[64] (continued on next page)

[186]

[324]

[111]

[77]

[323]

[322]

[193]

[319] [186] [320,321]

[15,318]

Average lignin of 18 grass varities−3.10–5.64

NM NM 13–21

[317]

[316]

[315]

[64]

[314]

[172] [78]

[111]

Reference

NM

NM

NM

56.27% maximum lignin solubilisation NM

< 79% Delignification NM

9.77

Delignification (%)

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[52]. The flowchart representation which briefly summarises the classification of these pretreatment techniques is given in Fig. 2. Physical pretreatments like milling and grinding mostly aim for the size reduction of the substrate of up to 0.2 mm. But, when physical pretreatment processes are amalgamated with other pretreatments the effectiveness of the process is improved to many folds leading to better delignification of the biomass [53]. Chemical pretreatments are more effective in solubilising the lignin and hemicelluloses content thus making the biomass more available for the enzymatic hydrolysis [54]. However, physicochemical pretreatments are highly effective either individually or when combined with chemical pretreatments. But the most effective physicochemical pretreatments are ultrasonication and thermal pretreatment processes where the cell disruption accompanied by degradation of the crystalline complex of the cellulose is achieved. This leads to swelling of biomass with higher availability of the biomass to the cellulose and hemicellulose hydrolysing enzymes during the process of enzymatic hydrolysis [55]. Biological and enzymatic pretreatments are moreover aimed at decomposition of lignin in milder conditions.

[327]

NM-Not mentioned.

Miscanthus

Miscanthus

Miscanthus

NM

H2SO4- 0.73 wt%,Temp-150 °C, Incubation time6 min+Ca(OH)2- 0.024 g/g,Temp-202 °C

Dilute-acid presoaking+Wet explosion Dilute-acid presoaking +Organosolv Acid+alkali

3.1.1. Physical pretreatment for size reduction of grasses Physical pretreatments are mainly aimed at reduction of particle size of grasses, which in turn decreases the degree of polymerization and crystallinity of cellulose. This size reduction also allows in reduction of the heat and mass transfer limitations that occurs due to large particle size of the biomass and increases the bulk density, thus allowing the pretreatment of more concentrated feedstock [53,56]. Physical pretreatment mainly includes chipping, milling, grinding, extrusion and pyrolysis. Chipping processes are mainly required for woody biomasses. The findings of Zhu and Pan [57] emphasizes on the fact that the pretreatment method of woody biomass differs substantially from the herbaceous biomass. This is mainly attributed to the differences in their chemical composition and the low lignin content in herbaceous biomass [57]. Milling and grinding are techniques which can be utilised for size reduction of the biomasses. Though grinding and milling have not been an integral part for grass delignification, but substantial differences have been observed during the enzymatic hydrolysis step if these two techniques are included in the pre-treatment scheme. A significant difference in the hydrolysis yield was observed in switchgrass and alfalfa grass chops when they were subjected to size reduction through grinding process [58,59]. Further, different types of milling processes can be used for size reductions in grasses like ball milling, knife milling and hammer milling [25]. Among all of these, particularly ball milling with different sieve sizes have been seen to be an efficient technique in size reduction of grasses [60]. Ball milled Dennanath and Hybyrid Napier grasses have been shown to improve the alkaline pretreatment for enhanced delignification and cellulose exposure [61]. Menegol et al. [62] also demonstrated enhanced delignification of elephant grass when exposed to physical pretreatment, leading to higher bioethanol production. Extrusion pretreatment is another commonly used pretreatment technique in lignocellulosic biomass which generally includes heating, mixing and shearing of the biomass thereby leading to cell disruption. It is found that single-screw and twin-screw extruders are widely used extrusion techniques in pretreatment process. Among the two, the later is more preferred due to extended control of residence time distribution and mixing as well as superior heat and mass transfer capabilities [63]. In grasses, extrusion pretreatments have been seen to be effective in exposing the cellulose to enzymatic attacks. Extrusion pre-treatment of switchgraas and prairie cord grass resulted in a total sugar recovery of 45.2% and 65.8% respectively [64]. The same authors in 2012, attempted for optimisation of extrusion pretreatment of other varieties of grass biomasses like switchgrass, bluestem and prairie cord grass. The study resulted in significant recovery of fermentable sugars with the highest values of 28.2%, 66.2% and 49.2% for switchgrass, big

a

NM Glucose- 0.4 g/g

[297] 85.1% Glucose-95% xylose-73%

[326] NM Glucose-61% xylose-95%

[325] 6.9 Total sugar 58.7g/100 g biomass Switch grass

Alkali 0.1 g/g of biomass Treatment time: 30 min Temperature: 190 °C 58 g/L solid content NM Alkali+microwave

Pretreatment technology

Table 2 (continued)

Parametres maintained

Grass variety

Release of sugars after pretreatment

Delignification (%)

Reference

S. Mohapatra et al.

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Fig. 2. Classification of Pretreatment techniques. Based on: http://pubs.rsc.org/en/content/articlelanding/2016/ra/c6ra09851g/unauth.

experimented in extruders for long-term usage. Further, low energy requirements will also be a requirement for economical pretreatment of the biomass. Hence, a multidisciplinary approach will be required to achieve an economical output in this type of pretreatment technique.

bluestem and prairie cord grass respectively [65]. The difference in the results for switchgraas and prairie cord grass was probably due to the different parameters, specifically the high screw speed and the higher residence time that were observed to be the most effective parameters. Lamas [66], also had similar conclusions for switchgrass treated with extrusion pretreatment. Brudecki et al. [67], also investigated on ground prairie cordgrass and found more promising results of 87% delignification and 92% glucose yield. Though twin-screw methods have been seen to be more effective for many lignocellulosic biomasses but studies on grasses have been limited using this technique. As saccharification yields of 80% [68], has been achieved with twin-screw extrusion pretreatment of rice straw, equivalent results can also be achieved in grasses. Although physical pretreatments processes have the advantage of producing zero toxic or inhibitory by-products in the substrate, but the high energy requirement makes it a cost intensive process. Secondly, the metal surfaces in extruder's needs constant replacements due to the aberrations observed after two to three cycles of pretreatment. These factors should be taken into account and more durable surfaces can be

3.1.2. Chemical and physico-chemical pretreatments for delignification of grasses In order to increase the elimination of lignin and/or hemicelluloses and decrease the crystallinity index (Crl) and degree of polymerization (DP) of cellulose, chemical and physico-chemical pretreatment methods have evolved as attractive methods [69]. Chemical pretreatments which include the use of acids, alkali, ionic liquids and organic acids such as oxalic acid, acetyl-salicylic acid and salicylic acid as catalysts are mainly used for internal degradation of lignin and hemicelluloses by breaking the internal lignin and hemicellulose bonds [69]. The hemicellulose and lignin bonds mainly refer to the chemical bonds between the lignin, galactose and arabinose residues on the side chains of hemicellulose molecules [70]. In general lignin can be divided into three types of monolignons i.e hydroxycinnamyl aldehyde (H), guaiacyl 1015

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bottlenecks of the process. For example, in a recent study, Merino et al. [84] used a series of ionic liquids for pretreatment of Taiwan grass and achieved thirty-five times higher reducing sugar yields after enzymatic hydrolysis in pretreated biomass in only one hour of pretreatment time. This was achieved due to the use of Q-tube which was very efficient as compared to the conventional round bottom flask. Physicochemical pretreatments, which are a combination of both the chemical and physical processes, are mostly useful for dissolving the hemicellulose and altering the lignin structure [85]. In this regard AFEX pretreatment has been effective for higher delignification in alfalfa [86], and for over 90% hydrolysis of hemicellulose in Bermuda grass [87]. Further, combination of pretreatments has been shown to decrease the formation of by-products, thereby decreasing inhibition in the final fermentation step [88]. Ammonia recycle percolation (ARP) has been paired with the AFEX pretreatment process for grasses. Iyer et al. [89] applied the pretreatment process on switchgrass and achieved 85% delignification without the formation of inhibitors. Chan et al. [90] performed a CO2 added AFEX pretreatment on rice straw and achieved a glucose conversion of 93.6% after the pretreatment. CO2 explosion is another physicochemical method which has been experimented on switch grass by Luterbacher and coworkers [91] and has proven to give good glucose yields of up to 81%. Similarly LHW, which are much alike as the steam explosion pretreatment has also been an interesting physicochemical method. Recently, Yu et al. [92] pretreated two varieties of Pennisetum hybrid (I and II) and a switchgrass variety with LHW to enhance the release of sugars and has achieved encouraging results for delignification of the biomasses. SPORL pretreatments which involves the treatment of biomass with calcium or magnesium sulfite followed by significant reduction of size of the pretreated biomass using mechanical disk miller has been effective in removing hemicellulose and lignin [93]. Zhang et al. [94] used sulphuric acid dosage (0.8–4.2%) and sodium sulfite dosage (0.6– 7.4%) followed by size reduction pretreatment on switchgrass biomass. Improved elimination of hemicellulose and partial removal of lignin along with decrease in hydrophobicity of lignin due to sulfonation was observed. Apart from the conventional process of pretreatment, advanced studies have been carried out in the recent past using microwave, ultrasonication pretreatments because of their unique heating mechanism, which selectively heats the more polar parts of the biomass [95]. This unique factor creates a ‘hot spot’ within heterogeneous biomass [96] enhancing the disruption of the recalcitrant structures of lignocellulose. Zhu et al. [97] conducted chemical assisted microwave treatment on Miscanthus and led to the conclusion that the selective heating and electromagnetic field created by the microwave are the prominent factors in efficient pretreatment. Sharma et al. [98] and Hong and Mai [99], attributed higher delignification of switchgrass and Bermuda grass to the similar unique factor of ultrasonication pretreatment. While many researchers have used chemical, physio-chemical and other pretreatment techniques for delignification and higher glucose yields of different grass varieties, the high energy costs and liquid loadings required specifically in physicochemical techniques are still the major draw backs owing to its less preference. Further, though SPORL pretreatment has been popular in the recent times because of its very high conversion rate of cellulose to glucose and maximum removal and recovery of hemicellulose and lignin, but post-pretreatment washing and high cost of recovering pretreatment chemicals need to be addressed. The scalability of the techniques in the commercial production of biofuels is still a challenge that has to be considered.

(G) and syringyl (S) lignin. Lignin of grasses is particularly high in phydroxycinnamates or H-monolignon [71]. The H-monolignols are primarily connected via carbon-carbon and carbon-oxygen bonds among its phenylpropanoid building blocks with aryl ether bonds (βO-4) which are important interunit linkage [72]. It has been demonstrated by Samuel et al. [73] that dilute acid pretreatment led to a thirty-six percent decrease of β-O-4 linkages in lignin of pretreated switchgrass. Focusing mainly on the lignin aliphatic linkages Teramura et al. [74], revealed that dilute sulphuric acid predominantly reduces the lignin aliphatic linkages or ferulate in rice straw. Savy et al. [75] also found similar results for Miscanthus and giant reed grass. Apart from the breakage of lignin bonds, the effect of dilute acids has also been studied for decrease in Crl and DP of grasses. Foston and Ragauskas. [76] during their study on pretreatment, indicated that it is not only the debonding of lignin which determines the effectiveness of pretreatment but the DC and DP of the biomass are equally responsible. The authors concluded that cellulose CrI and DP are altered during dilute acid (H2SO4) pretreatment and can affect biomass recalcitrance in switchgrass. Another important feature in the pretreatment technique is it is greatly affected by the parameters maintained during the process. It has been observed that though high temperature yields higher delignification, but substantial loss of biomass also occurs in the substrates. Redding et al. [77] found similar conclusions after pretreatment of costal Bermuda grass at high temperatures with dilute H2SO4. In analogous studies it has been seen that high acid concentrations and high temperatures during dilute acid process can cause degradation of sugar monomers to furans, which are inhibitory to yeast during fermentation [78]. The importance of alkali pretreatment in grasses is due to the fact that, alkali pretreatment not only offers solubilisation of more than 50% of grass lignins by destruction of alkali-labile ester linkages but also solubilizes high free phenolic content, thus improving the lignin solubility [79]. Alkaline pretreatment also causes less sugar degradation, and are economical as many of the caustic salts can be recovered and/or regenerated [45]. Li et al. [80] in a very interesting study concluded that alkaline hydrogen peroxide effectively reduced total lignin content and the content of p-hydroxycinnamates, which had the maximum effect on enzymatic hydrolysis. The authors also found that the amount of S/G (syringyl to guanicyl) ratios did not appear to contribute much to the enzymatic digestibility or delignification of four different grass cultivars, and the predominant effect of this phenomenon was specifically observed in case of switchgrass cultivar. In a similar study by Savy et al. [75], Miscanthus and giant reed grass were seen to have breakage of C–C bonds between lignin monomers and the degradation of phenolic species using alkaline hydrogen peroxide. Ionic liquids (ILs) have recently attracted substantial attention due to their ability to dissolve a wide range of lignocellulosic materials and have been seen for associated environmental benefits [81]. Soudham et al. [82] conducted IL pretreatment on reed canary grass using new acidic switchable ILs (SILs) like DBU–MEA–SO2 (DBU: 1, 8-diazabicyclo [5.4.0] undec-7-ene; MEA: monoethanolamine) and DBU–MEA– CO2. The authors obtained significant delignification with excellent glucan-to-glucose conversion levels (between 75% and 97%) after the enzymatic hydrolysis of IL-treated substrates. In order to evaluate the efficiency of IL pretreatment on grasses comparative studies have also been performed using acid/alkali and ILs. In one such research, Li et al. [83] compared the efficiency of two pretreatment techniques i.e. dilute acid hydrolysis and dissolution in an ionic liquid. Significance of the pretreatment was seen for delignification and saccharification yields for switchgrass. The authors observed that switchgrass exhibited reduced cellulose crystallinity and lignin content and higher saccharification yields in IL treatment as compared to acid treatment. Even if IL pretreatment have presented promising results as compared to acids and alkalis but the expensive chemicals, with retention time of several days has made the process inconvenient. But, the recent advances in the technique have decreased some of the

3.1.3. Biological delignification of grass Chemical and physicochemical delignification generally leads to high energy demand, corrosions, and by-product formations and adversely effects the environment. Thus, biological delignification which does not produce aforesaid conditions can be a promising 1016

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converted to (1Z, 3Z)-4-hydroxybuta-1, 3-diene-1, 2, 4-tricarboxylate in a route that hasn't been characterized yet. (1Z, 3Z)-4-hydroxybuta1,3-diene-1,2,4-tricarboxylate spontaneously converts to its tautomeric form (1E,3E)-4-hydroxybuta-1,3-diene-1,2,4-tricarboxylate, which is degraded into TCA cycle intermediates by the action of two additional enzymes-4-oxalomesaconate hydratase (lig J) and oxaloacetate βdecarboxylase/4-oxalocitramalate aldolase (lig K) [108]. With the use of these defined pathways, Kuhar et al. [109] used a basidiomycete fungus RCK-1 and pretreated wheat straw under solid state fermentation. The results indicated an increase in the ethanol yield by 33%. However, the residence time observed was more in this study. But, a similar study on wheat straw by Salvachu et al. [110] using fungi Panus tigrinus and Trametes versicolor gave 47% increase in delignification with lowest residence time of 7 days. Liong et al. [111] did a comparative study of pretreatment of Napier grass with a fungus Phanerochaete chrysosporium for three weeks and another one with NaOH. The authors reported that though delignification was higher in biological delignification but 1.5 fold higher ethanol yields was obtained from NaOH pretreated Napier grass. Suhara et al. [112] detailed the study of lignin degrading basidiomycetes on bamboo clums and stated that it was effective in removing 50% of the lignin content. Wan and Li et al. [113] evaluated the biological pretreatment of various feedstocks like corn stover, wood and grass using Cereporiopsis subvemispora. A two to three fold increase in reducing sugar production was observed. Similarly, Cianchetta et al. [114] also reported efficient delignification of wheat straw using Cereporiopsis subvemispora. The addition of external carbon sources, inducers and chemicals like alkalis, acids and AFEX has also been reported to enhance biological degradation of lignin [115]. Recently, Torreiro et al. [116] found that delignification of fungal (Irpex lacteus) pretreated wheat straw increased with addition of a mild alkali pretreatment. Balan et al. [117] also reported a high glucan and xylan conversion rate using biological pretreatment of rice straw (Pleurotus ostreatus) followed by AFEX pretreatment. Many other studies have revealed the high conversion effects of glucans and xylans using combination of biological pretreatments with liquid hot water and acids (H2SO4) in various substrates like poplus, rice hull and water hyacinth respectively [118– 120]. An alternative biological pretreatment method is the method of ensiling or biomass preservation. Ensiling holds potential as an integrated storage and pretreatment method with low cost and low energy requirements plus brings about multiple advantages with regards to agricultural management [121]. Jensen et al. [122] explored the ensiling pretreatment for temperate grasses like Festulolium Hykor. However, the pretreatment effect of ensiling, and the overall effects for further conversion are limited. With a limited number of studies on the mechanism of the delignification processes carried out by micro-organisms, further research is required to completely understand the intermediates obtained during the delignification process. This will be particularly helpful in enhancing of our insight into the conversion pathways, which would further help us in structuring of genes for genetically improved microorganisms. Further organisms can be designed for targeted delignification in grasses with low S/G ratio and higher H lignins. Combination of biological pretreatment with other pretreatments and ensiling pretreatment also seem to be attractive technologies that can be utilised for herbaceous biomass for enhanced delignification, nevertheless more research is required for cost-effective combination biological pretreatments.

alternative. Both, bacteria and fungi can be involved in biological delignification, but the effective depolymerisation of lignin is generally achieved by using white-rot fungi or basidiomycete [100]. A representation of the biological delignification process that has been proposed by different researchers using fungi and bacteria have been amalgamated and presented in a single figure as given in Fig. 3. As mentioned earlier grass lignins have three types of monolignons and the H lignin is the most abundant form of lignin found in grasses. The pathway shows the formation of the specific monolignons from the three major sections of lignin i.e. H, G and S that are formed from coumaryl alcohol, conniferyl alcohol and sinapyl alcohol respectively. The pathway can be divided into three parts which are a) degradation of H into protocatechuate, b) degradation of guaiacyl into vanillin which further degrades into the TCA Cylcle, c) degradation of syringate into the TCA Cycle. The pathway of degradation of H into protocatechuate by Aspergillus flavus (a basidiomycete) was proposed by Gold and Alic [101]. Fungi generally use extracellular and unspecific oxidative enzymatic system for delignification. The process not only involves various enzymatic activities like that of oxidases, reductases and peroxidases but compounds (low molecular weight) that mediate the processing of these enzymes. As given in the Fig. 2, H is first converted back to p-coumarate which is then degraded into p-Hydroxybenzoic acid. The conversion of p-coumarate to p-hydroxybenzoic acid involves a β-oxidation type of reaction. After formation of protocatechuic acid, intradiol cleavage takes place by the enzyme protocatechuate 3,4dioxygenase which gives rise to β-ketoadipic acid and leads to the TCA cycle [102]. Similarly, Guaiacylglycerol-β-guaiacyl ether (GCE) degradation pathway was proposed by using Sphingomonas sp. GCE consists of two diastereomers which needs to be cleaved. But, prior to the cleavage of the ether bond the compounds have to be oxidized by dedicated alcohol dehydrogenases. The organism has multiple such enzymes (ligD, ligL and ligN) with differing selectivity [103,104]. Following oxidation, the compounds are activated and cleaved by the enantioselective glutathione-S-transferase/β-etherase enzymes encoded by ligE and ligF. The glutathione moiety is cleaved by glutathione lyases such as the enzyme encoded by ligG, generating β-hydroxypropiovanillone, a non-stereoactive molecule [105]. β-hydroxypropiovanillone is degraded into vanillin or vanillate in a process that hasn't been defined yet, and those are degraded to central metabolism intermediates as described in super pathway of vanillin and vanillate degradation. Sphingomonas sp. converts vanillin to vanillate by vanillin dehydrogenase (encoded by ligV) [103]. Vanillate is converted in Sphingomonas sp. to protocatechuate by a tetrahydrofolate-dependent demethylase, vanillate/3-O-methylgallate O-demethylase, encoded by ligM [106]. Protocatechuate is degraded by this organism into central metabolism intermediates using the Meta cleavage pathway, as described in protocatechuate degradation I (meta-cleavage pathway) [102]. Protocatechuate is then converted to pyruvate which is then directed into the TCA cycle. The final conversion of S lignin begins with the degradation of syringate with its conversion to 3-O-methylgallate by the tetrahydrofolate-dependent syringate O-demethylase (encoded by desA) [105]. 3O-methylgallate can be degraded further via three different routes that converge back at (1Z, 3Z)-4-hydroxybuta-1, 3-diene-1, 2, 4-tricarboxylate. The main route, via gallate, is catalysed by two enzymes – a second tetrahydrofolate-dependent demethylase, vanillate/3-Omethylgallate O-demethylase (ligM), and gallatedioxygenase (des B) [107]. The other two routes are the result of direct dioxygenation of 3O-methylgallate. This reaction is carried out by two dioxygenases – protocatechuate 4,5-dioxygenase (ligA and ligB) and 3-O-methylgallate 3,4-dioxygenase (des Z), both of which produce a mixture of two different products -2-pyrone-4,6-dicarboxylate (PDC) and 5-carboxyvanillate (CHMOD) [108]. While the first product is hydrolysed by 2pyrone-4, 6-dicarboxylate hydrolase (ligI), the second product is

3.2. Enzymatic delignification of grasses Enzymatic delignification of grasses is an alternative to biological pretreatment where the objective is to increase the rate of reaction and delignification efficiency. This strategy not only offers the possibility of substrate specificity but also reduces the processing time from weeks to 1017

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Fig. 3. Pathways of conversion of the lignins present in grass biomass.

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et al. [140]. 2% NaOH was used as an extractant which was followed by acidification, precipitation and washing by 70% ethanol. A 26.2% yield of pentosans was observed. Another study by Singh et al. [141] used dilute acid for hemicellulose extraction from Kans grass and found a higher yield of xylan sugars in the liquid hydrolysate, which was further used for ethanol production. Njoku et al. [44] applied a different approach by applying wet explosion treatment on cocksfoot grass for extraction of the hemicellulose fraction. The authors concluded that the release of hemicellulose sugars is maximal in the liquid hydrolysate, with application of less severe pretreatment condition. Extraction of the hemicellulose fraction will not only improve the fermentation of pentosans but will also increase the subsequent enzymatic hydrolysis of cellulose. This effect was shown by Spindler and co-workers [141] who observed an increase in cellulose digestibility by five to seven times in wheat straw. Similar results were also given by Kong et al. [142] who observed a major effect on cellulose digestibility by the removal of the hemicellulose content. But, contradictory reports have also been seen. For example, Weimer et al., 2007 [281] advocated that cellulose and xylan association does not restrict the hydrolysis of the polysaccharides. Conversely, the removal of hemicellulose removes acetyl groups which alter the structural form of left lignin, thereby making the isolation of the most influential factors responsible for improving hydrolysis, difficult and time consuming [143]. In a more recent research, xylan and mannan have been reported to produce inhibitory effects on the proceeding cellulose hydrolysis step [125]. With divergent reports on extraction of hemicellulose, it is imperative to focus on the structural characterization of the biomass before and after the extraction of hemicellulose from biomass for better understanding of its chemistry with cellulose with respect to bioethanol production.

hours without consumption of carbohydrate [123]. Enzymes for delignification can either be collected from culture supernatant of lignolytic microorganisms or commercial enzymes which contains purified and concentrated enzymes [124]. Mostly, lignin degrading enzymes like laccase, mannase and peroxidases are produced by P.chyrosporium, Ceriporiala cerata, Cyathus stercolerus, C.subvermispora, Pyconoporus cinnarbarinus, Trametes villosa and P.ostreaus [125]. From various types of lignolytic enzymes, laccase (copper containing oxidase enzymes) in the form of laccase mediator system (LMS) have been extensively used in industrial delignification processes, as without these mediators laccases have limited usage [126]. In LMS, a redox material which is stable in its oxidized and reduced state and does not inhibit the catalytic activity of laccase is used [127]. In this context, Guitierrez et al. [128] observed the synergistic ability of laccase enzyme from Trametes villosa and I-hydroxybenzotriazole (HBT) which is a synthetic mediator, on milled elephant grass. Following the treatment, the delignification increased by 50%, enzymatic hydrolysis by 12% and the ethanol concentration reached 2 g/L. In a similar study by Sidhu. [129], switchgrass was subjected to LMS with different mediators like HBT, ABTS (2, 2′-azino-bis (3ethylbenzothiazoline-6-sulphonic acid) and violuric acid. Reduction of 28% lignin was observed with violuric acid. In another study [130], acid pretreated wheat straw with laccase-HBT in combination with alkaline peroxide extraction was studied. It was observed that LMS increased the saccharification yield by 35% which was attributed to enhanced lignin extraction due to LMS-induced formation of Cα oxidized groups in lignin. The most significant effect of LMS was observed in wheat straw where high delignification yield (up to 97%) was achieved using laccase from Pyconoporus sanguineus and violuric acid as a mediator [131]. LMS is advantageous in terms of significant reduction in pretreatment time, elucidation of sugar consumption and thereby improving the saccharification and fermentation. But, from an economical prospect the main disadvantage is the production cost of the enzyme and the synthetic mediators [127]. Alternatives can be replacement of natural mediators like acetosyringone, syringaldehyde and p-coumeric acid extracted from lignin in place of synthetic mediators [132] and growth of laccase producing microorganisms in lignocellulosic feedstocks, rather than synthetic medium [133,134]. An example of laccase producing microorganism with the capability of enzymatic hydrolysis have been seen in Pycnoporus sp using switchgrass as a substrate [135]. Thus, screening of such microorganisms can not only be beneficial for consolidated bioprocessing approaches leading to reduced processing stages, but will also help in reducing the usage of chemicals which further needs downstream treatment processes in industrial sectors.

3.4. By-products of pretreatment Formation of by-products during pretreatment is mostly observed with the solubilisation and degradation of pentosans and lignin, although other extractives and hexosans also contribute minutely for the formation of inhibitors [144]. In sufficiently high concentrations these inhibitors inhibit fermenting microorganisms, such as yeast and bacteria [145]. Some important inhibitors produced during different pretreatment methods from different type of grasses are exemplified in Table 3. In this context, an intensive study on lignin chemistry is required for the elimination of lignin from the biomass that could potentially affect the subsequent hydrolysis process. Though previously, much importance was not given on hydrolysis process with respect to the lignin components, but recent works are mainly focused on these aspects. This holds true due to the fact that the structure and concentration of the lignin components affects their hydrolysis [146]. More recently it has been studied that the presence of lignin in the biomass leads to higher requirements of cellulases in the subsequent saccharification step. This is because the enzyme binding generates a non-productive attachment with certain components of lignin and limits the accessibility of cellulose to cellulase [147]. Furthermore, phenolic groups are formed from the degradation of lignin. These components substantially create hindrance for cellulolytic enzymes to reach cellulose and hence influence enzymatic hydrolysis. Phenolic compounds that are typically formed in grass processing are pcoumaric, ferulic and diferulic acids. Though these are not representative of lignin components, but contribute to crosslinking with hemicelluloses and esterified to arabinoxylans form ether- or ester-linkages with lignin [148]. To overcome these, grasses with relatively low recalcitrance, which in turn can be pretreated under mild conditions can be employed. To exemplify the positive effects of mild pretreatment Chiaramonti et al. [149] and Larsen et al. [150] carried out hydrothermal pretreatment without addition of acid catalysts for bioconversion of Miscanthus grass and wheat straw respectively. They concluded

3.3. Extraction of hemicellulose fraction in grasses The secondary walls of grasses predominantly consist of xylans, more specifically Glucuararonoxylans (GAXs) and mixed-linkage glucan (MLG). GAXs has a β-(1,4)-linked xylose (Xyl) backbone and ara and glucuronic acid (GlcA) side chains, while MLGs are unbranched chains of ~30% β-(1,3) and ~70% β-(1,4)-linked glucopyranosyl residues [135–137]. The GAXs are immensely underutilised sources for bioethanol [138] and this is mainly due to the economic challenges that limit the extraction and utilisation of these valuable products. Mostly the GAXs are either degraded in the pretreatment step or are present in minimal quantities along with the celluloses. Extraction of the GAXs generally involves the alkali dissolution followed by precipitation using alcohols such as 2-propanol, methanol, or ethanol. Following this an oxidative bleaching is done to remove the contaminating lignin in the precipitate [139]. In one such study, Stoklosa and Hodge. [138] used increasing levels of NaOH followed by precipitation using ethanol on switchgrass biomass. This resulted in high yields of the hemicellulose from the grass. The same approach was also tested in bamboo (generally considered as a woody grass) by Luo 1019

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Table 3 Inhibitors produced during different pretreatment methods from different type of grasses. Pretreatment method

Type of grass used

Chemicals involved

By-products formed

Reference

Mild acid treatment combined with wet-explosion treatment Mild acid with high temperature treatment Mild acid with higher incubation time Mild acid with higher incubation time Mild acid with high temperature treatment Mild acid and alkali aasisted with microwave pretreatment Hydrothermal pretreatment

Cocksfoot grass

H2SO4

[44]

Bermuda grass

H2SO4

High concentrations of acetic acid and low amounts of Furfural, Hydroxymethy furfural Furfural, Hydroxymethy furfural

Bermuda grass Bermuda grass Rice straw

H2SO4 HCl H2SO4

Acetic acid, Furfural, Hydroxymethy furfural

[328]

5- Hydroxymethy furfural and Formic acid

[74]

Miscanthus

H2SO4/NaOH microwave assisted pretreatment High temperature

Furfural, Hydroxymethy furfural

[97]

Formic acid, Acetic acid, Furfural, Hydroxymethy furfural Acetic acid, Furfural, Hydroxymethy furfural

[329] [330]

Gluconic acid

[324]

Wheat sraw

Hydrothermal pretreatment

Prairie cord grass

Ozonolysis

Miscanthus ×giganteus, M. sinensis ‘Gracillimus’, Saccharum

High temperature and low incubation time Low temperature and low alkali concentration

[77]

4.1. Enzymatic saccharification

not have much role in conversion of these complex carbohydrates to simple sugars which can be utilised by the microorganisms. The performance of enzymatic saccharification of lignocellulose strongly depends on many factors such as the diverse species, complex chemical composition, efficiency of the pretreatment technique, the mode of enzyme action and structural characteristics of the feedstock used [155]. Rivers and Emert. [156] in their study on lignocellulosic biomass for bioethanol production, showed that, a specific pretreatment is required for every individual lignocellulosic substrate depending on its composition, if maximum enzymatic hydrolysis is to be achieved. Since the compositions of grasses are significantly different from other lignocellulosic biomasses, the main factors mostly affecting the enzymatic hydrolysis are the cellulose crystallinity and the presence of hemicellulose. In this context, Yoshida et al. [157] studied the effects of cellulose crystallinity, hemicellulose and lignin on enzymatic hydrolysis in Miscanthus sinensis. The authors concluded that yield of monosaccharides increased with decrease in cellulose crystallinity, delignification and complete hydrolysis of hemicellulose by xylanases. This can be attributed to the increase in enzyme absorption capacity of the amorphous cellulose [158]. Hence, during the biochemical conversion of lignocellulosic biomass to fuels, cell wall-deconstructing enzymes are used to convert plant cell wall polysaccharides into fermentable sugars. Cellulases and hemicellulase are the cell wall deconstructing enzymes which are mostly produced in higher quantities by bacteria and fungi. Commercially, cellulases have been commercially available for more than thirty years, and have been used both in academic and industrial researches (Singh, 2007) [159]. But, technological developments have also prompted most of the academicians and research institutes for isolating cellulolytic and xylolytic enzyme producing organisms and further extraction and application of these enzymes for various purposes (Kuhad et al., 2011) [160]. Application of the enzymes on the substrate of interest can be made taking two important things into consideration. The foremost thing is the composition of the biomass i.e. presence of higher crystalline or amorphous cellulose and the amount of hemicellulose present. Other than the composition, the proficiency of the enzyme (i.e. its activity), to hydrolyse the carbohydrate of interest in the biomass is also a vital parameter that has to be considered. With these factors in consideration, this section of the review aims to highlight the work conceded by the research groups on application of both commercial and isolated enzymes for higher saccharification yields of grass biomass.

The foremost objective of enzymatic saccharification is to induce structural changes of cellulose and other carbohydrate polymers in the pretreated biomass into fermentable sugars by using biological or chemical approaches [143]. Though pretreatment is essential in breaking of the bonds that holds lignin with the carbohydrates, but it does

4.1.1. Commercial enzymes for enzymatic hydrolysis The major source of commercial cellulase enzymes are filamentous fungi and mutant strains of Trichoderma (T. viride, T. reesei, T. longibrachiatum) [161,162]. But, production of enzymes from a single

that mild pretreatment produced low concentrations of furan aldehydes and phenols, but the concentrations of acetic acid were reported to reach 17 g/kg/1 for Miscanthus and 5.1 g kg/1 for wheat straw. Lower temperatures have also been reported to yield less inhibitor in grass biomass. In one such study, Redding et al. [77], pretreated coastal Bermuda grass at with acid at temperatures lower than 180 °C and reported much lower formations of formic and levulinic acids. Other effective techniques could be adding of catalysts during the pretreatment process. Jacquet et al., 2012 [151], experimented the use of catalysts like CO2 or SO2 during steam pretreatment of rice straw, bagasse and giant Miscanthus which resulted in significant decrease in inhibitory compounds in the subsequent hydrolysis and fermentation steps. Advanced approaches could be integrated pretreatment processes combining two or more pretreatment techniques. Recently, effect of microwave treatment on NaOH- and H2SO4pretreated Miscanthus was studied by Zhu et al. [97]. An increased (twelve times higher) sugar yield with low concentrations of inhibitors was obtained in half the time compared to single pretreatments. To add advantage to the combined pretreatment techniques, “in-situ detoxification” method wherein organisms like some species of S. cerevisiae, having capacity to transform furfural and HMF into less toxic compounds of furfural alcohol and 2, 5-bishydroxymethylfuran, respectively can be utilised [69]. Further, some species of Pichia stipitis which do not get affected by furfural in low concentrations up to 0.5 g/ L are viable options to overcome the toxic effects of inhibitory compounds in the substrate that are produced during pretreatment [152]. Genetically improved strains for better inhibitor tolerance capacity or adaptability would also be a preferable option. Conversely, lowering the lignin content in grasses by molecular tools has also been experimented. Chen et al. [153] demonstrated that lignin modification via genetically engineering practices targeting its biosynthetic pathways could considerably reduce lignin formation and improve ethanol yield. However, this could be quite challenging as lignin components serve as the major plant defence system to pathogen and insects and its modification could disrupt the plants’ natural protection [154].

4. Enzymatic hydrolysis

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ml),from T.ressei and achieved total reducing sugars of 350 mg/g. Belal, [173] taking rice straw as her lignocellulosic substrate also concluded that T.ressei is an efficient strain for cellulase production and cellulose hydrolysis. In a recent study, Shrestha et al. [174] isolated thirty fungal sp. from decaying leaves of Miscanthus and sugarcane and also produced a variety of cellwall degrading enzymes showing activities for xylanases, exocellulases, endocellulases, and beta-glucosidases. This approach will not only produce value added products but will also utilise the decaying lignocellulosic biomasses and in turn help in restricting environmental pollution. The study also suggested that a majority of fungi tested equalled or exceeded the bioconversion abilities of native T. reesei. Apart, from fungus many bacteria have also been investigated in production of cellulase that has been seen to efficiently saccharify cellulose to reducing sugars. Another advantage of using bacteria as a cellulase source is, mostly the enzymes are thermostable. Zambare et al. [175] isolated cellulase and xylanase from thermophilic consortium of bacteria with maximum activities of 367 U/L and 489 U/L at 60 °C and 70 °C taking prairie cord grass and corn stover as substrates respectively. It was further demonstrated that enzymegenerated using prairie cord grass as a substrate, was a good source for bioethanol production. Sharma et al. [176] used cellulase from isolated bacillus (S3B8) species, with activity of 0.12 U/ml on switch grass for bioethanol production. Higher enzyme activities and saccharification of cellulases from bacterial strains have also been reported by researchers. An example can be cited by the work done by Singh et al. [177], who used CMCase (1.7 mg/ml) from isolated Bacillus amyloliquefaciens for enzymatic hydrolysis of pretreated Parthenium hysterophorus and achieved 187.4 mg/g of fermentable sugars. With the reported results it can be inferred that the isolated enzymes from fungus and bacteria, in the labrotary scale can be a good alternative for hydrolysing herbaceous substrates. Though reducing sugars yields post saccharification is not as promising as commercial enzymes, but application of molecular and genetic tools can further enhance the saccharification yields by many folds. The strategies for using economical substrates like agro-wastes are a good alternative to combat the high cost of the commercial enzymes.

organism leads to variable problems like lower thermostability and lack of specific activities [163]. An example is cellulases from Thrichoderma reesei which produces endoglucanases and exoglucanases in bulky quantities, but has low βglucosidase activity which results in a lower biomass saccharification. To avoid such circumstances, some enzymes producers have marked new cellulase mixtures or multienzyme mixtures which can sustain stability at higher temperatures. A commercial enzyme Accellerase 1500 which is a mixture of cellulases complex (i.e. exoglucanase, endoglucanase, hemi-cellulase and β-glucosidase) produced from a genetically modified strain of T. reesei. was utilised on four perennial grasses ryegrass, tall fescue and bentgrass and high hydrolysis yields (~80%) were observed for all three grasses [78]. Meineke et al. [164] also reported enhanced hydrolysis of switch grass using Accellerase 1500. But, similar results were not obtained by Tut and Olt. [165] who also used Accellerase 1500 on energy grasses like Miscanthus saccharifloris and achieved a low glucose yield of 59.80% after saccharification. The glucose and xylose yields can be enhanced by using accessory enzymes in combination with the above. Examples of such enzymes are Accelerase®XP which enhances both xylan and glucan conversion; Accelerase®XC which contains hemicellulose and cellulase activities and Accelerase® BG which is a β-glucosidase enzyme. Singh et al. [166] studied on the effect of particle size on enzymatic hydrolysis of pretreated Mischanthus sp. Singh and his coworkers performed the enzymatic hydrolysis using Accellerase 1500 in combination with all the accessory enzymes as stated above and found an increased polysaccharide conversion. Badhan et al. [167] experimented Accellerase 1500 with Accelerase®XC in combination with isolated rumen enzymes on alpha alpha hay and barley straw. The authors got some interesting findings and concluded that while a 1.6 fold increase in glucose yield was observed with the addition of complementary rumen enzymes, the xylose yield enhanced to seven fold higher in alfalfa and fivefold higher in barley straw. A variant of the commercial enzyme i.e. Accellerase 1000 has also shown satisfactory results on alkali pretreated cogon grass [168]. Other, commercially important enzymes are Celluclast 1.5 L (Sigma), cellic Ctec and cellic Htec (Novozymes). The latter is used in mixtures and works well on a variety of pretreated feedstocks for converson of the polymeric sugars to monomers [169]. With the advent of the enzymes, Xu et al. [40] performed the enzymatic hydrolysis of pretreated switch grass and costal Bermuda grass using cellic Ctec and cellic Htec. More reducing sugars were obtained from enzyme hydrolysed costal Bermuda grass than switchgrass. Recently, Thomsen et al. [170] used CellicCTec2 and HTec2 in ratio of 90:10 on pretreated wheat straw and achieved higher enzymatic convertibility of both glucan and xylan. Though commercial enzymes, in small quantities, have accelerated the enzymatic hydrolysis processes by many folds, but the economical availability of the same is not yet achieved. Hence, innovative bioprocesses for the production of new generation of enzymes are needed. An alternative, for small scale labrotary preparations can be the use of isolated enzymes from microorganisms like bacteria and fungi.

5. Fermentation of grasses for bioethanol Pretreatment and saccharification processes are designed to optimize the fermentation process. In general many fermentation techniques are employed for bioethanol production depending on the substrate and microorganism used. The general fermentation techniques can be broadly classified into submerged fermentation (SmF) and solid state fermentation (SsF) either in batch, fed-batch or continuous culture systems that can be utilised for different type of substrates. But in order to improve the economic viability of lignocellulose-to-ethanol conversion, both the cellulose and hemicellulose hydrolysates should be utilised for ethanol production. In that regard many improved techniques of fermentation have been developed and been implemented in fermentation of grasses. A number of studies are carried out in switch grass [178], reed canary grass [179], Bermuda grass [180], silver grass [181], kans grass [182], sea grass [183], cocksfoot grass [44], elephant grass [62] and mostly Napier grass [184–186] using the improved fermentation techniques. These outlines are summarized in Table 4. Fermentation of grasses has mostly been carried out by different processes such as separate hydrolysis and fermentation (SHF), simultaneous saccharification and fermentation (SSF) and simultaneous saccharification and co-fermentation (SSCF). In SHF enzymatic hydrolysis is performed separately from the fermentation while in SSF/SSCF cellulose hydrolysis is carried out in the presence of the fermentative microbes [187] like yeasts, bacteria, and fungi which can ferment ethanol in lignocellulosic hydrolysate. SHF is a process where separate hydrolysis and fermentation are carried out in separate units. In a first

4.1.2. Isolated enzymes for enzymatic hydrolysis The high cost of the commercially available cellulolytic enzymes has led to many reports using isolated cellulase and xylanase enzymes either from native or from recombinant strains [171]. In that regard many researchers have come up with promising results for enzymatic hydrolysis of grasses using isolated enzymes. Wongwatanapaiboon et al. [15] used T.ressei for production of cellulase and xylanase with activity of 0.948 ± 0.05 and 92.13 ± 6.86 U/ml. The enzymes were used for saccharification of eighteen varieties of grass cultivars, which showed total reducing sugars of 500–600 mg/g of substrate. The production of reducing sugars by isolated enzymes was quite significant to that of the commercial enzymes. In a similar study, Katarina and Ghosh, [172] achieved a crude enzyme mixture of cellulase and xylanase enzyme (CMCase-1.41, FPase-1.12, and Xylanase-6.23 U/ 1021

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Table 4 Global vision of fermentation process for bioethanol production using divergent grass varieties. Sl no

Substrate

Microorganisms

Process of fermentation

Parameters

Ethanol yield

Reference

1

Dwarf Napier grass (Schumach) Dwarf Napier grass (Schumach) Dwarf Napier grass (Schumach) Dwarf Napier grass (Schumach) Kans grass (Saccharum spontaneum) Napier grass (Merkeron) Napier grass (Pennisetum purpureum) Napier grass (Pennisetum purpureum) Napier grass (Pennisetum purpureum)

Saccharomyces cerevisiae NBRC 2044+Escherichia coli KO11 S. cerevisiae NBRC 2044

SSCF

36 °C, pH 5.0

74.1%

[186]

SSF

35 °C, pH 5.0

121 mg/g

[185]

Saccharomyces cerevisiae NBRC 2044+Escherichia coli KO11 E.coli KO11

SSF

34 °C, pH 6.6

68.9%

[331]

SSF

34 °C, pH 5.0

[184]

S. cerevisiae

SA

E. coli LY01

SSCF

28 °C, pH 5 200 rpm 35 °C, pH 5.5

144 mg/g (44.2%) 0.46 g/g

S. cerevisiae TV2

SA-HF

–

Klebsiellaoxytoca THLC0409

SSCF

Clostridium strain TCW1, Bacillus sp. THLA0409, Klebsiellapneumoniae THLB0409, Klebsiellaoxytoca THLC0409, Brevibacillus strain AHPC8120 Bacillus sp. THLA0409, Klebsiella oxytoca THLC0409 S. cerevisiae (KY3 and KY-NpaBGS)

SSCF

31 °C, pH 7.04 472 rpm 60 °C, pH 7.0–7.2 150 rpm

2 3 4 5 6 7 8 9

10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36

Napier grass (Pennisetum purpureum) Napier grass (Pennisetum purpureum) Napier grass (Pennisetum purpureum) Switch grass (Panicum virgatum) Italian ryegrass (Lolium multiflorum Lam) 11 types of grasses* Purple guinea grass (P. maximum cv. TD53) Grass silage (fibre fraction) Elephant grass (Pennisetum purpureum, Schum.) Elephant grass (Pennisetum purpureum) Switchgrass (Panicum virgatum) Mission grass (Pennisetum polystachion) Elephant grass (Pennisetun purpureum) Reed canary grass (Phalaris arundinacea L.) Thatch grass (Hyparrhenia rufa) Napier grass (Pennisetum purpureum) Sea grass (Cymodocea serrulata) Elephant grass (Pennisetum purpureum) Cocksfoot grass (Dactylis glomerata) Giant miscanthus (Miscanthus x giganteus) Giant reed (C3 grass sp.) (Arundo donax L.) Mission grass (Pennisetum polystachion) Purple elephant grass (Pennisetum purpureum Schum.) Rice grass (Spartina spp.) Elephant grass (Pennisetum purpureum) Cogon grass (Imperata cylindrical L.) Bamboo

SSCF SSF

224.5 mg/g (73%) SA: 91.8% HF: 76.9% 82 mg/g (76.9%) 40 mg/g

[182] [209] [332] [333] [334]

30 °C, 100 rpm 40 °C, pH 5–6

276 g/kg (59%) 3.32 mg/ml

[335]

[194]

[153]

S. cerevisiae

SSF

S. cerevisiae 424 A (LNH-ST)

SSCF

E. coli KO11, S. cerevisiae

SSCF

37 °C, pH 4.8 100 rpm 30–35 °C, pH 4.8–5.5 180 rpm 36 °C, pH 5.6

S. cerevisiae+Pichia stipitis

SSCF

35 °C, 150 rpm

S. cerevisiae TISTR 5596

SHF

30 °C, pH 5.0

162 L/t DM (52%) 32.1g/L (72.7%) 333 mg/g (84.6%) 0.02–0.14 g/g (Max. 32.72%) 5.92 g/L

[336]

Lactobacillus sp. S. cerevisiae CAT-1

SSF SSF

– 6 min at 200 °C

14.6 g/L 107.72 µL/g

[203] [339]

S. cerevisiae CAT-1

SSF

28 °C, 12 h

6.1 g/L

[62]

Kluyveromyces marxianus IMB3

SSF

45 °C, 168 h

[340]

S. cerevisiae TISTR 5596

SHF

pH 10, 24 h

22.5 g/L (86%) 16 g/L

Aspergillus niger and S. cerevisiae

SSF

S. cerevisiae D5A and S. cerevisiae YRH400 Zymomonas mobilis

SSF

pH 5.5, 35 °C, 72 h, 300 rpm 35 °C, 100 rpm,72 h

23.4 g/L (78%) (81–84%)

[179]

SSF

8.8 g/L

[264]

E. coli KO11

SSF

pH 4.3, 30 °C, 120 rpm, 60 h 35 °C, 24 h

18.5 g/g

[111]

S. cerevisiae

SSF

pH 4.5, 28 °C, 24 h

0.047 ml/g

[183]

S. cerevisiae

SSF

37 °C, 36 h, 150 rpm

26.05 g/L

[342]

Pichia stipitis CBS 6054

SSF

158 ml/kg DM

[44]

Scheffersomyces (Pichia) stipitis CBS 6054 S. cerevisiae

SSF

160 °C, 15 min, 87 psi oxygen pH 5.5, 30 °C, 96 h

12.1 g/L

[343]

SSF

37 °C, 200 rpm, 48 h

8.2 g/L

[344]

Saccharomyces cerevisiae TISTR 5596 S. cerevisiae

SHF

pH 10, 30 °C, 24 h

16 g/L

[189]

SSF

1.8g/L (95%) 28.1 g/L

[345] [346]

16.8 g/L

[347] [323]

[337] [338] [15]

[189] [341]

Trichoderma reesei SEMCC 3.217 and S. cerevisiae SEMCC 2.157 Aspergillus niger and S. cerevisiae

SSF

pH 4.5, 30 °C, 4h pH 4.5, 30 °C, 4 h, 150 rpm pH 5, 35 °C, 300 rpm

S. cerevisiae F1BY3

SSF

37 °C, 120 h

9.11 g/L

Zymomonas mobilis

SHF

30 °C, 24 h

4.72 g/L [190] (continued on next page)

1022

SSF

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Table 4 (continued) Sl no

Substrate

Microorganisms

Process of fermentation

Parameters

Ethanol yield

Reference

37

Silver grass (Miscanthus floridulus) Cogon grass (Imperata cylindrical L.)

Candida shehatae

SHF

pH 5.5, 24 °C, 150 rpm

(55.8%) (64.3%)

[181]

S. cerevisiae

SSF

37 °C, 72 h

38

19.08 g/L (76.2%)

[202]

Abbreviation: [SA: Saccharification of cellulosic components; SSF: Simultaneous saccharification and fermentation; SHF: Separate hydrolysis and fermentation; SA-HF: Saccharification of cellulosic components/hexose fermentation; SSCF: Simultaneous saccharification and co-fermentation; DM: Dry matter; *11 types of grasses: Napier grass (Pennisetum purpureum), Dwarf napier grass (P. purpureum cv. Mott), King napier grass (P. purpureum cv. King Grass), Bana grass (P. purpureum × P. americanum), Purple guinea grass (Panicum maximum TD 58), Ruzi grass (Brachiaria ruziziensis), Pangola grass (Digitaria decumbens), Atratum grass (Paspalum atratum) and Vetiver grasses]

have been experimented by Yasuda et al. [184], which resulted in an ethanol concentration of 144 mg/g of untreated Napier grass. This technique is also beneficial for the diauxic behaviour (inability to use xylose in presence of hexose) of the pentose fermenting microorganism in the fermentation medium [188]. Further to enhance the ethanol yields amalgamations of SHF and SSF with co-cultures and immobilized cultures have also been proposed by Chen. [70]. The major advantage that a co-culture offers is the flexibility of combining a pentose fermenting microorganism with a hexose fermenting microbe [208]. Since the xylan or pentose sugar is relatively low in grasses and are mostly removed in the pretreatment step, using of a relatively not so efficient pentose strain in combination with a highly efficient hexose fermenting microorganism can also be advantageous in achieving high ethanol yields. These techniques have been reported to produce high titters of ethanol production from Napier grass [209], Bermuda grass and bunch grasses [210] through a SHF process involving the enzymatic saccharification and co-fermentation (CF) of hexose and pentose sugars by a recombinant E. coli LY01 (a derivative of E. coli KO11). Fermentation efficiency has also been seen to have increased by almost 20% using immobilized yeast and broth supplemented with Mg, Zn, Cu or capantothenate [211]. Since a fermenting organism shares the same pathway for both glucose and xylose utilisation, and the affinity for xylose is 200-fold less than that of glucose, the transport of xylose into the cell is inhibited by high amounts of glucose [207]. To overcome this, low glucose concentrations should be maintained in the fermentation slurry. Lee and his co-workers suggested fed-batch and immobilization techniques can be utilised to overcome the aforesaid problem. Another modified form of immobilization is co-immobilization of both hexose and pentose fermenting organisms in a single immobilized bead. This allows hexose fermenting organisms to be fixed outside the beads and the xylose fermenting microbes inside the bead allowing early utilisation of hexose with simultaneous consumption of xylose [212]. New techniques have led to immobilization of fermenting microorganisms like yeasts with natural lignocellulosic materials like sugarcane bagasse [213], alginate-chitosan beads [214], sweet sorghum pith [215], corncob pieces [216], cashew apple bagasse [217],, dried spongy fruit of luffa (Luffa cylindrica) [218], carboxymethylcellulose (CMC) grafted with N-vinyl-2-pyrrolidone [219], sodium alginate grafted with N-vinyl-2-pyrrolidone [220], lentikat discs [221] and rice flour and white glutinous rice flour [222]. Sugarcane bagasse and agar-agar cubes have been successfully recycled with ethanol yields of 0.44 g/g and 0.33 g/g in sugarcane bagasse [223]. Saccharum spontaneum pith, which are not toxic to microorganisms have also been used as immobilization matrixes for lignocelluloses [224]. In recent years focus has been made on emerging approaches in bioethanol production for reduction of production costs. This approach aims at developing consolidated bioprocess schemes (CBP) wherein the same microorganism is accomplished for cellulase production, substrate hydrolysis, and fermentation in a single step [225]. CBP is advantageous as it employs microbes to perform all the four biologically-mediated transformations viz. the production of saccharolytic

unit pretreated grasses are degraded to monomeric sugars by cellulases and xylanases and thereafter fermented to ethanol in a separate unit. The main advantage is that the two processes (hydrolysis and fermentation) can be performed at their own individually optimal conditions. This is quite essential because cellulases are efficient at temperature between 45 and 50 °C while commonly used fermenting organism perform at an optimum temperature of 30–37 °C [188]. Recently Prasertwasu et al. [189] conducted SHF on Mission grass (Pennisetum polystachion) with maximum ethanol yield of 16 g/L. But many researchers have also reported low ethanol yields using SHF [47]. He et al. [190] used SHF for bamboo residues and achieved an ethanol concentration of 4.72 g/L. This was attributed to the unutilised reducing sugar (25.0–40.0%) that was produced during the enzymatic hydrolysis and was not fermented to ethanol. Other possible reasons of obtaining low ethanol concentration are the end product inhibition that occurs, when glucose and cellobiose released in cellulose hydrolysis strongly inhibits the cellulase efficiency. Further, microbial contaminations in the medium may also lead to low ethanol yields [191]. To achieve a reasonable ethanol yield, lower solid loadings and higher enzyme additions could be needed [192]. SHF studies have been conducted on switch grass and purple guinea grass by Chung et al. [193] and Ratsamee et al. [194] with an ethanol yield of 0.44 g/g and 5.92 g/L respectively. An alternative to overcome the end product inhibition in SHF is simultaneous saccharification and fermentation (SSF) in which sugar concentrations are kept low [195–198]. SSF can be carried out in two different routes viz. either by processing the liquid pentose stream produced after pretreatment separately or by a co-fermentation step [199]. Considering SSF as an efficient technique as compared to SHF, Yasuda et al., [186] performed fermentation of Napier grass using E. coli KO11 in SSF conditions and obtained an ethanol yield of 74.1%. Similarly, Das et al. [200] reported seven fold increases in ethanol concentration from thatch grass in SSF as compared to SHF using Zymomonas mobilis as the fermenting organism. SSF has also been highly effective for high solid loadings or in scale-up processes. This has been demonstrated by Santos et al. [201] using sugarcane bagasse as a substrate where an ethanol concentration of 60 g/L was obtained using 30% (w/w) substrate loading. Lin and Lee. [202] conducted SSF experiments on cogon grass in both shake flask (7 g) and 5 L rotary drum reactor (1 kg) and obtained an ethanol yield of 80.3% and 76.2% respectively. Similar results of obtaining higher ethanol yields have also been observed by Suryawati et al. [204] and Isci et al. [205] from switchgrass using SSF. Sieker et al. [203] used SSF for grass silage and obtained an ethanol concentration of 14.6 g/L and also stated that enzyme hydrolysis is an essential requirement before fermentation. The finding of Sieker et al. [203] was well evidenced, when low ethanol yield from SSF of switchgrass was reported by Wymann [206]. The low yield of ethanol was reported because of the use of strategies like direct microbial conversion (DMC), with evasion of enzymes during saccharification process. Recently, techniques like SHF followed by pentose fermentation

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The success of grass biomass as an energy crop for bioethanol production in large scale will depend mainly on two factors i.e. the biomass yield and the level of biomass recalcitrance including other properties of the cell wall. In the following section, we discuss about the improvements that have been carried out till date on either the crop or the microorganism involved in bioethanol production, by means of genetic and molecular processes. This will not only update the findings of the researchers in this area but will also improve our insights to the modern technologies that have been implemented for developing grass biomass as a potential candidate for bioethanol production.

genetic tools or markers have also been developed in which the initial stages of plant growth can predict its yield. Recently, this robust technique has been applied on Miscanthus. This technique was used to identify links between early establishment traits and biomass yield in Miscanthus. This marker-assisted selection technique could save years of waiting for Miscanthus plants to establish and become mature [240]. The technique can be used to reliably select higher-yielding plants earlier in the grass life cycle. A new approach of gaining control over the lignocellulosic recalcitrance is gaining insight into the molecular dynamics simulations of the lignocellulosic structure. Molecular dynamics simulations have been used to investigate decrystallization of cellulose, the interactions between cellulose and noncellulosic components of plant cell walls, and the structure and dynamics of lignin. Molecular dynamics simulations are mostly used for addressing both solvation structure and thermodynamics of effective interactions in cell walls based on molecular forces [241]. Silveira et al. [241] employed the statisticalmechanical, 3D reference interaction site model with the Kovalenko– Hirata closure approximation (or 3D-RISM-KH molecular theory of solvation) to reveal the supramolecular interactions in this network and provide molecular-level insight into the effective lignin–lignin and lignin−hemicellulose thermodynamic interactions. The research group found that such interactions are hydrophobic and entropy-driven, and arise from the expelling of water from the mutual interaction surfaces. The molecular origin of these interactions was carbohydrate–π and π–π stacking forces, whose strengths are dependent on the lignin chemical composition and the methoxy substituents in the phenyl groups of lignin, promote substantial entropic stabilization of the lignohemicellulosic matrix. A study on glucuronoarabinoxylan (mainly consists of glucuronic acid and arabinose) an abundant hemicellulose in grasses has been carried out using similar techniques by Mortimer et al. [242,243], where genetic manipulation of glucuronic acid branching has been shown to significantly improve xylan extractability from cell walls without impairing plant growth.

6.1. Genetic improvements in grasses

6.2. Molecular Improvements

With thousands of grass genotypes being deposited in seed banks, only few varieties have been accessed and screened for identification of bioenergy traits [229]. Transgenic manipulation or plant breeding programs can be employed to achieve genetic development in grasses. In order to design the biomass for higher biomass yields ploidy level and genome architecture are important factors that are to be considered [230]. In this regard, leaf yield, stem yield and total plant height in Miscanthus, have been identified [231] leading to potential increases in total biomass. Other studies on genetic development of Miscanthus spa with identification of ploidy levels have also been reported [232,233]. Similarly genome sizes of various bioenergy grasses like switchgrass (1.88 pg), maize (2.73 pg), sorghum (1.21 pg) [234] and various species of Miscanthus [235] have been identified which can be utilised towards the genetic development. Another approach of crop development is QTL mapping. QTL mapping has been employed by Liu et al. [236] to develop a high density genetic map for switchgrass. Other research groups like Ma et al. [237] and Swaminathan et al. [238] have also developed high resolution linkage maps for Miscanthus sinensis. The development of these maps has made QTL mapping studies easier. This can be well illustrated from the intense studies done by Feltus and Vandenbrink. [229] on Miscanthus. Their studies revealed that sorghum (a variety of grass) has the closest syntenous relationship to Miscanthus. These genetic maps which are made using QTL studies will allow scientists to sequence genome via synteny relationships from sorghum to Miscanthus. On the other hand undetected QTLs also form a valuable method to identify DNA markers, often in multiple genome positions and can be used to select improved feedstock varieties before a crop development cycle is complete [239]. Apart from QTL studies novel

Molecular techniques can be employed to either minimize the recalcitrance of the grasses or in increasing the efficiency of microorganisms in increasing the enzymatic digestibility of lignin, cellulose and hemicelluloses.

enzymes, the hydrolysis of carbohydrate components present in biomass to simple sugars, the fermentation of hexose sugars and finally the fermentation of pentose sugars in a single step [226,227]. Thus, this process can substantially lower the production cost and enhances the efficiency of bioethanol production, as compared to independent hydrolysis and fermentation steps. Fusarium oxysporum is one such fungus that is capable of degrading and fermenting a wide variety of different lignocellulosic substrates including grasses under CBP [228]. Little has been studied on co-immobilization and CBP techniques on grasses. Hence, more research with these modern techniques in grasses could lead to better substrate utilisation and higher ethanol yields. Further, the interaction mechanism of the aforesaid biological matrices with the fermenting organisms can be studied intensively to examine any toxicity effects of these matrices on the organisms. Since, pore size is also an important aspect in immobilization studies, the matrix chosen for immobilizing a particular microbial species should also be considered. Undoubtedly, CBP processes are the next generation technologies in commercial ethanol production from herbaceous biomasses. Therefore, identification of microorganisms capable of carrying out the CBP process in grasses remains an important area of research that is yet to be exploited. 6. Improvements in bioethanol from grasses

6.2.1. Molecular Improvements in grasses Molecular improvements in grasses have been mostly targeted to eliminate the use of the pretreatment step or the enzymes, both of which contribute to the high processing cost of bioethanol from grasses. In this context, enzymes from the plants itself are an attractive alternative which can be utilised in grasses for converting the polysaccharides into monosaccharides. Approaches like promoter modifications for enhancing the accumulation of enzymes, accumulation of enzymes in specific tissues or organs and production of induced expressible enzymes have been widely used in case of monocots like rice and maize [244], for enhancing the hydrolysis of the carbohydrates in the cell wall. Promoters that are used are generally derived from either monocot or dicot or from viral vector that can target a monocot or dicot species. But a promoter is much effective if it is expressed in the same type of plant from where it has been derived [245]. Another molecular approach is apoplast targeting using pathogenesis-related protein signal peptides which has been successfully accomplished in maize [246–248], rice [249,250] and alfalfa [251] without disturbing cell wall integrity and with reasonable enzyme yields (1.2–6.1%). One recent approach which has gained much attention is the auto hydrolysis of the plant biomass using internally generated enzymes [252–255]. In this case, no further pretreatment of the substrate is required and the biomass is auto hydrolysed using either heterologous enzymes pro1024

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for first generation biofuel production while switchgrass and organic residues are used for second/next generation biofuel production. Unlike first generation feedstocks, the market value of second generation feedstock is not known since residue markets are not yet developed in many countries. Also, little commercial production has been experienced in developing countries of energy crops such as switchgrass and thus their market value is not known. So, the cost analysis of second generation biofuel can be made only based on production cost. The cost that are taken into account include land preparation to harvesting biomass incorporating labour, material expenses, land rent, fertilisers and other supplies. Another important aspect that will affect the cost of biofuel production is cost development of biofuel conversion technology for second generation biofuels. Grasses, as discussed previously in this review, have high levels of cellulose and hemicellulose with the total sugar content between 55% and 70% of the total cell wall content on an average. It has been documented that grasses have very high production rate leading to around 80–150 t of grass biomass production per hectare (Zhao et. al. 2015) [266]. Various studies have been conducted over the world to optimize and reduce the cost of the end product from grasses. One such example is that of switchgrass that is grown in Argentina and the process economics has been studied by Eijck et al., 2014 [267]. The production costs of switchgrass are estimated to be 3.2 $/GJ in 2020 and is proposed to decrease to 3.0 $/GJ by 2030. These prices include the land rent in Argentina (100– 300 $/ha/year), labour wages (2.18–3.18 $/h), export of switchgrass seeds from US (20$/kg) and fertiliser costs (0.13–0.48 $/kg). Mostly, the decrease in the costs of production can be obtained by local production of the seeds of switch grass which would can be available at 10 $/kg. Further, the ethanol cost of switchgrass in 2014 was 18.3$/GJ as compared to Eucalyptus that has production costs of 16.8 $/GJ in Brazil and 19.8 $/GJ in Mozambique. Compared to the first generation feedstock like cassava, where the production costs of bioethanol are around 15 $/GJ, the second generation ethanol production still requires more improvements (Chum et al., 2011) [268]. A comparative analysis of the feedstock cost and their ethanol yield are given in Table 5. Although, ethanol production from first generation feedstocks have been commercialized in many countries but the unavailability of feedstocks restricts its use in the future generations. In this context, bioethanol from grasses, though in the present scenario are still in the process of optimisation for cost-effective ethanol production in many developing countries, but the present production costs are at par with the first generation feedstocks. Further, the technological developments for production of enhanced grass biomass and efficient microorganisms will be helpful in achieving lower ethanol production costs in the near future.

duced within the plant or in combination with some other additional enzymes [256]. However, variation in the conversion efficiency of herbaceous biomasses does not solely rest on the lignin content and composition. Numerous studies on biomass recalcitrance have investigated the impact of differences in the composition and structure of cell wall polysaccharides, and the interactions between polysaccharides and other cell wall components. These demonstrated how cell wall characteristics other than lignin— including the degree of cell wall porosity, cellulose crystallinity, polysaccharide accessible surface area and the protective sheathing of cellulose by hemicellulose—can also contribute to the natural resistance of plant biomass to enzymatic degradation [257–259]. Consequently, strategies to develop novel genotypes, with reduced recalcitrance, through targeted modifications of cell wall biosynthesis genes are beginning to gain momentum. For instance, alterations in the cellulose synthesis machinery—or its accessory complexes— may lead to modifications in the structure of cellulose micro fibrils, with, for example, reduced crystallinity, a lower degree of polymerization and/or a higher degree of porosity. Vandenbrink et al. [260] demonstrated a large variation in cellulose crystallinity within a diverse association mapping panel in sorghum, and reaffirmed that genotypes with lower cellulose crystallinity exhibit higher enzymatic hydrolysis rates, as has been reported for pure microcrystalline cellulose samples [261] and ground Miscanthus powder [155]. Thus, the robust genetic and/or molecular tools that have been widely studied in other monocots for improving the biomass yield and reducing lignin recalcitrance and cellulose crystallinity with successful results, can also be implemented in grass biomass. Though some research have been conducted on some varieties of Miscanthus and switchgrass, but the other potential grass varieties which can be sustainable source for bioethanol production requires substantial research. 6.2.2. Molecular Improvements in microorganisms Engineered microorganisms can be utilised for improved biomass processing, which would allow the use of bioethanol from grasses commercially. Many researchers have approached for recombinant microorganisms with either higher delignification rates or enzyme production capacity and high fermenting capacities. In this regard, Ogawa et al., 1998 [262] introduced cDNA of Postreatus in Coprinus cineresus which resulted in high MnP production of the later followed by increased delignification after 16 days. Similarly, increased saccharification have been reported by Mutreja et al. [263] who used recombinant cellulase for bioethanol from wild grass using E. coli BL21 cells which were transformed with CtLic26A-Cel5-CBM11 fulllength gene from Clostridium thermocellum. In a similar study, Das et al. [264] developed a recombinant strain of Escherichia coli strain by expressing GH5 cellulase and GH43 hemicellulase genes from Clostridium thermocellum for increasing the cell biomass production and enzyme activity from wild grass. In a more recent approach, researchers from the University of Georgia and Tennessee's Oak Ridge National Laboratory engineered the thermophilic bacterium Caldicellulosiruptor bescii to directly convert switchgrass into ethanol [265]. The engineered microbe was successfully experimented for ethanol production from switchgrass without the use of any pretreatment or enzymatic hydrolysis step. Though ethanol production was on the lower side but this has elucidated the potential of the next steps that has to be taken in this field.

8. Research gaps in bioethanol production The conversion of lignocellulosic biomass into bioethanol with utmost productivity/yields is a crucial biochemical process in biorefinery. However, the lack of industrially robust strain for converting biomass into bioethanol has been a major issue for the success of bioethanol industries. The major bottlenecks in bioethanol productions are lack of consistency in the composition of lignocellulosic biomass in divergent grasses varieties, non-uniformity in environmental conditions, instability of the performance of the microorganisms involved in biological fermentation processes, optimizing process parameters and above all, constraints in modelling/designing the appropriate bioreactors.

7. Economic analysis 9. Critical comments and future prospective Economic evaluation of biofuel production include a detail analysis of the viability of feedstock production and total production cost (in terms of net present value-NPV) and total production cost (TPC) which includes conversion, transport and distribution. The most commonly used feedstocks in developing countries include sugarcane and palm oil

The outlook for global bioethanol will depend on number of interrelated factors such as, (i) continuous hike of oil price; (ii) availability of feed stocks; (iii) technological breakthroughs and (iv) sustainable policies by government. Keeping in mind the above 1025

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Table 5 Minimal ethanol selling price (MESP) of grasses as compared to various feedstocks with their production(on dry ton basis) and their ethanol yields. Sl No.

Type of Feedstock

Production of feedstock (dry ton/ day)

Feed stock cost ($/dry ton)

Ethanol yield (gal/dry ton)

MESP ($/gal)

References

1. 2. 3. 4. 5. 6.

Corn stover Corn stover Eucalyptus Hardwood Rice straw Straw, Eucalypatus and poplar Sugarcane Switchgrass Switchgrass Wheatstraw

2200 2200 4.5 −35 tdm/ha 2200 1000–1200 1760–2200

51 59 78 65 35–68 57–127

90 79 130–142 75 60–80 70–84

1.49 2.15 1.35 3.43–4.03 – 2.12–2.91

[348] [36] [349] [350] [267] [351]

100 (t/ha/yr) 5000 4600 1200–1700

102–108 44 30.6 38–45

116 97–105 80–85 50–70

0.88–1.16 0.63–0.83 1.26–1.28 2.36

[267] [352] [353] [353]

7. 8. 9. 10.

our understanding in enhancement of bioethanol production from grasses which are at present considered as the most important lignocellulosic substrate.

discussed outlooks and constraints, genome mining of compassionate microorganisms can be an important step in suitable conversion of lignocellulosic biomass into bioethanol for improving the productivity. For example, suitable gene from remote sources are traced and cloned into host organism to obtain optimum bioethanol production. The future of cellulosic fuel will continue to emphasize on group of C4 grasses for sustainable large scale production of biomass to support cellulosic fuel industries. The C4 plants mainly grasses which use C4 photosynthesis are important sources of bioethanol due to their high yield potential, wide adaptability across diverse environments, low water requirement, high carbohydrate content and low fertiliser requirement. The success of C4 grasses in the cellulosic ethanol production will depend on effective pretreatment and effective fermentation technologies. However, keeping in view the sustainable production of bioethanol, the scientists throughout the world should stand on one platform to manage the constraints for the production of bioethanol from cellulosic grass varieties. Furthermore, an international law should be implemented and sustainable policies by government should be imposed in favour of reduction of the cost of biomasses for bioethanol production and competition from unconventional fossil fuel alternatives.

Acknowledgement Authors are grateful to the authorities of college of engineering and technology, BPUT, Bhubaneswar for providing necessary facilities to carry out this research. References [1] Thatoi HN, Dash PK, Mohapatra S, Swain MR. Bioethanol production from tuber crops using fermentation technology: a review. Int J Sustain Energy 2014;35:443–68. [2] Zabed H, Sahu JN, Suely A, Boycee AN, Faruq G. Bioethanol production from renewable sources: current perspectives and technological progress. Renew Sustain Energy Rev 2017. [3] Singh S, Cheng G, Sathitsuksanoh S, Wu D, Varanasi P, George A, Balan V, Gao Xi, Kumar R, Dale BE, Wyman CE, Simmons BA. Comparison of different biomass pretreatment techniques and their impact on chemistry and structure. Front Energy Res 2015. [4] Balat M, Balat H. Recent trends in global production and utilization of bio-ethanol fuel. Appl Energy 2009;86:2273–82. [5] Kazi FK, Fortman JA, Anex RP, Hsu DD, Aden A, Dutta A, Kothandaraman G. Techno-economic comparison of process technologies for biochemical ethanol production from corn stover. Fuel 2010;89:520–8. [6] Chundawat SPS, Donohoe BS, da Costa Sousa L, Elder T, Agarwal UP, Lu F, Ralph J, Himmel ME, Balana V, Dale BE. Multiscale visualization and characterization of lignocellulosic plant cell wall deconstruction during thermochemical pretreatment. Energy Environ Sci 2010;4:973–84. [7] IEA. From 1st -to 2nd –generation biofuel technologies. An overview of current industry and RD & D activities; IEA-OECD; 2008. [8] Sun Y, Cheng J. Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresour Technol 2002;83:1, [1]. [9] Ryan L, Convery F, Ferreira S. Stimulating the use of biofuels in the European Union: implications for climate change policy. Energy Policy 2006;34:3184–94. [10] Adekunle A, Orsat V, Raghavan V. Lignocellulosic bioethanol: a review and design conceptualization study of production from cassava peels. Renew Sustain Energy Rev 2016;64:518–30. [11] Jinaporn W, Kangvansaichol K, Burapatana V, Inochanon R, Winayanuwattikum P, Yongvanich T. The potential of cellulosic ethanol production from grasses in thailand. J Biomed Biotechnol 2012;303748:1–10. [12] Tye YY, Lee KT, Abdullah WNW, Leh CP. The world availability of non-wood lignocellulosic biomass for the production of cellulosic ethanol and potential pretreatments for the enhancement of enzymatic saccharification. Renew Sustain Energy Rev 2016;60:155–72. [13] Álvarez C, Sosa FMR, Díez B. Enzymatic hydrolysis of biomass from wood. Microb Biotechnol 2016;9:149–56. [14] Clayton WD, Vorontsova MS, Harman KT, Williamson H. GrassBase – the online world grass flora; 2016. [15] Wongwatanapaiboon J, Kangvansaichol K, Burapatana V, Inochanon R, Winayanuwattikun P, Yongvanich T, Chulalaksananukul W. The potential of cellulosic ethanol production from grasses in Thailand. J Biomed Biotechnol 2012:10. [16] Seppala M, Paavola T, Lehtomaki A, Rintala J. Biogas production from boreal herbaceous grasses – specific methane yield and methane yield per hectare. Bioresour Technol 2009;100:2952–8. [17] Antony E, Taybi T, Courbot M, Mugford ST, Smith JAC, Borand AM Cloning. localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple). J Exp Bot 2008;59:1895–908.

10. Conclusion Lignocellulosic material like grass is a promising feedstock for bioethanol production which is an alternative to the present fossil fuel. The grass biomass is ideal because being a non-food crop; grasses do not interfere in the normal food cycle and hence do not possess a threat to the human population. On the other hand its production is easy and production is cost effective for industrial bioethanol production as it does not depend on any agronomic input of fertilisers. However, the main drawback lies on the efficient removal of lignin and bioconversion of remaining cellulosic content into fermentable sugar. The technologies for industrial scale bioethanol production requires consolidated bioprocessing approach using pretreatment, enzymatic degradation and fermentation which can efficiently use the substrate into product with complete utilisation of the substrate. Developments of such technologies are still under process. Other approaches like using advanced techniques in genetic and molecular improvements (e.g. 3D-RISM-KH molecular theory of solvation process in grasses) to eliminate the use of the pretreatment step or the enzymatic hydrolysis, both of which contribute to the high processing cost of bioethanol from grasses can be implemented on different varieties of grasses to achieve cost-effective end product. Biomass based ethanol industry requires a continuous and reliable supply of raw materials and efficient technology to maintain a low cost ethanol production. Though at present the cost of production is at par with first generation feedstock, it can be reduced with commercial production of the feedstock and development of bioconversion technologies in future. The conferred information on pretreatment and genetic improvement techniques will help to extend 1026

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