Renewable and Sustainable Energy Reviews 76 (2017) 963–973

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Renewable and Sustainable Energy Reviews

journal homepage: www.elsevier.com/locate/rser

Trends and advances in conversion of lignocellulosic biomass to biobutanol: MARK

Microbes, bioprocesses and industrial viability
⁎
Lalitha Devi Gottumukkala, Kate Haigh, Johann Görgens
Department of Process Engineering, University of Stellenbosch, Private Bag X1, Stellenbosch 7602, South Africa

A R T I C L E I N F O A BS T RAC T

Keywords: Biobutanol has gained attention as an alternative renewable transportation fuel for its superior fuel properties
Biobutanol and widespread applications in chemical industry, primarily as a solvent. Conventional butanol fermentation
Clostridia has drawbacks that include strain degeneration, end-product toxicity, by-product formation, low butanol
Lignocellulosic biomass concentrations and high substrate cost. The complexity of Clostridium physiology and close control between
ABE fermentation
sporulation phase and ABE fermentation has made it demanding to develop industrially potent strains. In
ABE recovery
Techno-economic analysis
addition to the isolation and engineering of superior butanol producing bacteria, the development of advanced
cost-effective technologies for butanol production from feedstock like lignocellulosic biomass has become the
primary research focus. High process costs associated with complex feedstocks, product toxicity and low
product concentrations are few of the several bioprocess challenges involved in biobutanol production. The
article aims to assess the challenges in lignocellulosic biomass to biobutanol conversion and identify key process
improvements that can make biobutanol commercially viable.

1. Introduction improvement options under investigation include selection of cheaper

substrates, development of more suitable microorganisms, integrated
There is growing interest in options to produce chemicals and fuels fermentation-product recovery. Research in this area is also focused on
in a way that is deemed more sustainable and beneficial to the isolation of novel solventogenic Clostridia and genetic modification of
environment. In response, options to produce butanol from renewable, existing butanol producers for high yield and product concentrations.
lignocellulosic biomass feedstocks by means of fermentation are being Characteristics of an improved strain include the ability to produce
investigated. Butanol has been shown to have superior fuel properties high butanol concentrations, yield, productivity and improved toler-
and distribution advantages when compared to ethanol. In addition, ance to the feed and product. There are still numerous challenges with
butanol has applications in chemical industries as a finishing agent for regards to developing a solvent resistant butanol producer for ABE
car paint, a solvent for dyes and rubber production, and a feedstock for fermentation and an alternative approach is to remove butanol during
the production of flotation aids [1]. Currently, butanol production is fermentation using in situ techniques. This leads to increased butanol
mainly by means of petrochemical routes based on the oxo- or aldol- formation and reduced energy costs for downstream processing.
processes [2,3]. Lignocellulose has gained attention as an alternative biobutanol
Prior to this butanol was a by-product of the acetone-butanol- feedstock because of its availability and sustainable supply. However,
ethanol (ABE) fermentation process, performed by solvent producing additional processing is required to release the fermentable sugars. The
strains of Clostridium species [1,2] with processes continued until the complex nature of the feedstock and feedback inhibition of enzymes
1980's in places such as China and South Africa [4]. Thus ABE during hydrolysis has led to the consideration of alternative fermenta-
fermentation has been proposed as the starting point for the develop- tion strategies including, simultaneous saccharification and fermenta-
ment of more environmentally benign and sustainable butanol produc- tion (SSF) in batch or fed-batch mode. Various fermentation strategies
tion. Some of the challenges with the traditional ABE fermentation like continuous fermentation, two-stage and multi-stage fermentation
processes are relatively low yield, productivity and product concentra- with high cell density immobilized cultures, have been combined with
tion, thus increasing the process costs and equipment costs. Further integrated solvent recovery systems to investigate the potential to
the traditional feedstocks are sugar, molasses or starch leading to high improve butanol yields and productivity.
feedstock costs and “food vs. fuel” concerns [1]. ABE fermentation

⁎
Corresponding author.
E-mail address: [email protected] (J. Görgens).

http://dx.doi.org/10.1016/j.rser.2017.03.030
Received 17 November 2015; Received in revised form 7 February 2017; Accepted 8 March 2017
1364-0321/ © 2017 Elsevier Ltd. All rights reserved.
L.D. Gottumukkala et al. Renewable and Sustainable Energy Reviews 76 (2017) 963–973

1.1. The aim and scope of present review

The aim and scope of this review is to assess the current status of
research, challenges and advancements with regards to butanol pro-
duction, from lignocellulosic biomass, by means of ABE fermentation
processes. As part of it, advancements and gaps in strain improvement,
process developments with regard to low cost feedstocks, fermentation
strategies, ABE recovery options and techno-economic studies are
discussed. The information that can be used to isolate or engineer
industrial strain, identify biochemical and fermentation improvements
that will lead to the most commercially viable options is considered in
this review.

2. Clostridia and ABE fermentation

Fig. 2. ABE fermentation pathway is divided in to cold channel (left) and hot channel
Clostridia are obligate anaerobes and spore forming bacteria with a
(right) and the key molecule involved in butanol formation is showed in green. (For
complex life cycle. Clostridium acetobutylicum and C. beijerinckii are interpretation of the references to color in this figure legend, the reader is referred to the
well-known ABE fermenters, but there are several other Clostridial web version of this article.)
species like C. saccahrobutylicum, C. saccharoperbutylacetonicum, C.
sporogenes, and C. pasteurinum that are reported for butanol produc- condensation to butyrylCoA and its reduction to butanol [11]. The
tion [5–8]. These spore forming bacteria are capable of producing pathway between acetylCoA to butyrylCoA is the backbone for both
volatile fatty acids like acetic acid and butyric acid as bi-products in acidogenesis and solventogenesis and the enzymes involved are func-
ABE fermentation. Acid production occurs during the vegetative phase tional in both phases, except that intracellular enzyme concentrations
of the cells and assimilation of acids to solvents occurs during the onset vary during solventogenesis [10].
of sporulation (Fig. 1). Signal transduction plays a key role in the onset Butyryl phosphate formed from butyrylCoA is considered the key
of solventogenesis. Acetate, butyrate and low pH are the extracellular molecule involved in solventogenesis, chemotaxis and motility. It
signals and acyl phosphates are the intracellular signals for the shift triggers solvent production by acting as a phospho-donor to Spo0A,
towards solvents formation [9]. which is positive regulator of sporulation genes and certain solvent
ABE fermentation is bi-phasic in nature and the shift in acids to genes [12,13]. A study with a butyrate kinase mutant of
solvents production is importantly regulated at the genetic level and is C.acetobutylicum (buk mutant) hypothesized that elevated levels of
highly dependent on the external and internal pH of the cell, nutrient butyryl phosphate was responsible for early onset of solventogenesis. It
limitation and alteration in the electron flow [10]. The fermentation was reported that butyryl phosphate concentrations of 60–70 pmol/g
end-products depend on the function of many enzymes involved in the dry weight of cells is required to initiate solventogenesis and higher
metabolic pathway. Glucose is metabolized via pyruvate to acetylCoA concentrations corresponded to high butanol fluxes. It was also
and enters the central pathway of ABE fermentation. ABE Pathway is suggested that a minimum of 9 mM of intracellular butyric acid is
divided into a “cold” channel and a “hot” channel to differentiate the required to trigger solventogenesis, while intracellular concentrations
metabolic routes responsible for the formation of butanol and ethanol of acetic acid could not be correlated with solvent initiation, though
(Fig. 2). The cold channel represents the pathway where acids are supplementation of low concentrations of acetic acid has been reported
assimilated to acetylCoA, which can be either reduced to ethanol or to enhance solvent formation [12].
condensed to butyrylCoA to form butanol. Hot channel refers to the Considering the complexity of the pathway and close association of
pathway where solvent formation takes a direct route of acetylCoA

Fig. 1. Life cycle of solvent forming clostridia and biphasic nature of ABE fermentation.

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solventogenesis with intracellular and extracellular acid concentra- disrupting the adc gene that codes for acetoacetate decarboxylase
tions, nutrient availability and sporulation, targeting one or few genes (AADC), with a mobile group II intron resulted in decreased butanol
for metabolic engineering cannot address drawbacks like solvent production, unless methyl viologen was added to alter the electron flow
toxicity and low product concentration. So, several approaches were [18]. With several attempts and studies to understand the metabolic
followed aiming to develop a superior butanol producer that can be pathway and physiology of the cells, it was found that acetone
used for commercial scale production of butanol. formation is necessary for cytosolic detoxification from a proton
gradient caused by carboxylic acids. So, an alternative metabolic
3. Development of strains suitable for industrial application engineering strategy was tested to convert acetone to iso-propanol,
since it can be used as a fuel additive. The resulting engineered strain
Metabolic engineering of C. acetobutylicum is difficult due to produced 20.4 g/L mixture of isopropanol, butanol and ethanol (IBE)
complex metabolic regulations involved with the life cycle and degen- [19]. Recently, natural non-acetone forming butanol producers,
erative nature of the strain. Degeneration of the culture naturally C.sporogenes BE01 and C. pasteurinum have been isolated and
happens by loss of the pSOL1 megaplasmid in consecutive vegetative fermentation conditions were optimized for improved butanol produc-
transfers and continuous culture [14]. The loss of the pSOL1 mega- tion [7,8].
plasmid results in non-sporulating cells that are not capable of solvents C. sporogenes is capable of producing 7.3 g/L of total solvents from
production, which is an obstacle for industries that prefer continuous rice straw hydrolysate containing 30 g/L of sugars, of which 5 g/L was
cultivation culture. Solvent formation occurs during the Clostridial butanol. During butanol fermentation, C. sporogenes BE01 was
phase and the rest of the vegetative cells do not contribute to solvent reported to produce volatile fatty acids (VFAs) of 7 g/L and hydrogen
formation. Several approaches are currently under investigation to of 1.2 L/L [20]. Optimizing the conditions for enhanced assimilation of
develop a strain suitable for industrial application for meeting biopro- VFAs to butanol, or metabolic engineering to reduce the formation of
cess objectives which include improved butanol yield, concentration, VFAs and hydrogen, might improve butanol production. C. pasteur-
selectivity and productivity. A few strategies and outcomes are dis- ianum can be grown on glycerol as sole carbon source and thus
cussed below. producing 1,3-propanediol (PDO). Biebl et al. [21] first reported the
ability of C. pasteurianum to produce 17 g/L of n-butanol in glycerol
3.1. Re-enforcing hot channel for butanol formation medium, but a large variation in the product (butanol and 1,3 PDO) is
observed under similar or slightly different conditions. Moon et al.
It was reported recently that the cold channel is less efficient in [22], optimized the medium components to favor n-butanol formation,
butanol formation than the hot channel, because of the increased but weak pathway regulation and multiplicity means stringent condi-
formation of acetone and CO2. Every mole of re-assimilated acid tions are required to focus the metabolism towards butanol from 1,3
generates acetone and CO2 through the decarboxylation of acetoacetate PDO. Sabra et al. [8] reported the highest butanol concentration of
formed during the assimilation process [11]. Hence, researchers are 21.1 g/L with mixed substrate fermentation, when glucose and glycerol
trying to understand the genes involved in metabolic flux and divert the were used in the ratio 1:1. When glucose was replaced with lignocellu-
cold channel towards the hot channel for improved yields of butanol losic biomass hydrolysate, butanol production decreased to 17 g/L.
and ethanol. Jang et al. [15] optimized butanol production through the However, when lignocellulosic biomass hydrolysate was used as the
hot channel by simultaneous disruption of pta and buk genes encoding sole carbon source, butanol production was decreased to 6.8 g/L.
phosphotransacetylase and butyrate kinase respectively and by over- Increased tolerance of the strain to n-butanol in mixed fermentation,
expressing a mutated aad (aldehyde/alcohol dehydrogenase) gene. The when compared to mono substrate fermentation was also reported. The
engineered strain C. acetobutylicum BEKW (pPthlAAD−) produced ability to produce high concentrations of butanol is interesting, but
18.9 g/L of butanol with a yield of 0.71 mol butanol/mole glucose. The improved production with lignocellulosic biomass hydrolysate is ne-
butanol concentrations and yields obtained with the engineered strain cessary to make the process industrially viable.
were 160% and 245% higher than those obtained from the wild strain,
but this was not sufficient to meet the concentration requirements of an 3.4. Butanol tolerance and hyper butanol producers
industrially viable process. Further metabolic engineering is required
for increased butanol production, reduced by-product formation and ABE fermentation is limited with low concentrations, yield and
improved butanol tolerance. productivity due to the end product stress on the microbe. In batch
fermentations, the concentration of total solvents (ABE) above 20 g/L
3.2. Asporogeneous solventogenic strains terminates the fermentation and butanol concentrations rarely exceed
13 g/L [23]. An evolutionary engineering approach for increasing the
Considering that sporulating cells are not suitable or efficient for butanol tolerance of C. acetobutylicum ATCC 824, generated two
continuous fermentations, non-sporulating solventogenic strains have mutants SA-1 and SA-2 and they exhibited a 121% and 27% increase
been developed. Asporogeneous strains (M5 and DG1) without the in butanol tolerance respectively, when compared to the wild type [24].
pSOL1 megaplasmid were generated and complimented by plasmids This did not lead to increase in butanol yield indicating that butanol
carrying the aad gene. With these modifications, selectivity towards yield is not based just on solvent tolerance. In contrast, inactivating the
butanol increased, but these strains produced very low concentrations butyrate kinase (buk) gene and overexpressing the alcohol dehydro-
of butanol without forming acetone [16,17]. Attempts to increase the genase (adh) gene increased butanol production beyond toxic limits.
butanol production in M5 asporogeneous strain by overexpressing aad Inactivation of buk resulted in 16.7 g/L of butanol, higher than the
and thl (thiolase) were not successful. It was hypothesized that electron toxic limit of 13 g/L [25]. Overexpressing groESL, a class I stress
flow affected by the loss of the pSOL1 plasmid was the hindrance in response operon also improved butanol concentrations to 17.1 g/L
generating asporogenic butanol producers without forming acetone [26]. C. beijerinckii BA101 is a well-known hyper butanol producer
[16,17]. developed by chemically mutating C. beijerinckii NCIMB 8052 with N-
methyl-N-nitro-N-nitrosoguanidine. In batch fermentation, C. beijer-
3.3. Non-acetone forming butanol producers inckii BA101 produces 19 g/L butanol [27]. C. acetobutylicum JB200
is a hyper producing mutant derived by adaptive engineering of C.
Acetone can be regarded as a product with no fuel value and thus acetobutylicum ATCC 55025, an asporogenic solvent producing strain.
several approaches to eliminate or reduce acetone production are being It has the ability to produce 19–21 g/L butanol in conventional free-
investigated. In a study aimed to eliminate acetone production by cell fermentation and with a fibrous bed bioreactor (FBB) fermentation,

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28 g/L butanol was achieved [28]. It is also interesting to note that C. dilution with water [46,47] and adsorption onto activated carbon and
beijerinckii BA101 exhibited tolerance up to 23 g/L of butanol [27], resins [45,50]. Qureshi et al. [46,47] compared four potential ligno-
whereas C.acetobutylicum JB200 was reported to grow only till 16 g/L. cellulosic biomass feedstocks, wheat straw, corn stover, barley straw
This further shows that increased solvent production cannot be directly and switchgrass to a glucose control. It was found that fermentation
attributed to increased solvent tolerance. with wheat straw hydrolysate produced better results than the glucose
Though various efforts were made for strain improvement, the control including a productivity of 0.60 g L−1 h−1 compared to
average maximum butanol production is close to 20 g/L by batch 0.31 g L−1 h−1 and there was no conversion with the corn stover
fermentation. Considering the complexity of Clostridium physiology hydrolysate [46]. Further investigations showed that over liming of
and metabolism, process parameters for butanol fermentation should hydrolysate for detoxification improved the butanol concentration and
be well studied and optimized. productivity of 26.27 g/L and 0.31 g L−1 h−1 respectively [47]. The
highest concentration and productivity achieved using switchgrass was
14.61 g/L and 0.17 g L−1 h−1 [47]. Thus, indicating the choice of the
4. Process development substrate, pretreatment and detoxification of hydrolysate are important
parameters to be considered for butanol fermentation (Table 2).
4.1. Feedstock While Clostridia can convert lignocellulosic biomass hydrolysates
and other complex substrates, the highest butanol concentrations
For a process to be industrially viable, in addition to an efficient achieved are from starch, without any integrated butanol recovery
microbial strain, selection of the fermentation type and substrates play applied [6,8,38,39]. Utilization of starch and sugars as substrates
a critical role. The cost and availability of substrate is one of the major represents over 70% of the total production costs of biobutanol and
challenges associated with conventional ABE fermentation. Several falls under food vs. fuel category of first generation fuels [58].
studies were done to improve butanol production by media engineering Furthermore, though lignocellulosic biomass is represented as a low-
and various fermentation approaches, however most of these were cost feedstock, the pretreatment and hydrolysis process required for
carried out with glucose as the carbon source in a defined medium conversion to sugars is reported to contribute significant capital and
(Table 1). Though solvent concentrations improved with various operating costs and the enzymes required for the hydrolysis of
process operations, pure glucose as the carbon source is not feasible lignocellulosic biomass is an order of magnitude higher than that
for butanol production at commercial scale. However, glucose is required for starch hydrolysis [59]. This indicates that significant
considered as a model substrate for lignocellulosic biomass hydrolysate improvement and research is required to reduce the costs of lignocel-
and various kinds of butanol fermentation including batch, fed-batch, lulosic biomass processing so that it can be regarded as a true low cost
continuous, two-stage and immobilized cultures have been assessed to feedstock for biofuel conversion.
improve butanol fermentation.
Feedstock is the one of the biggest operating expenses reported for
4.2. Advanced fermentation strategies
ABE fermentation and hence achieving the theoretical maximum
conversion will improve the viability of butanol production. The
Theoretical yield determination for a microbial product is contro-
traditional process of ABE fermentation is well established with sugar
versial, due to the complexity of reaction pathways. For ABE fermenta-
or starch as a substrate and Clostridia can ferment a variety of complex
tion, the maximum theoretical yield of the total solvents is between
feedstocks which includes cheese whey [38] and low grade glycerol
38.6% and 39.9%, under biosynthetic conditions where no intermedi-
[39]. In recent years, one of the most widely investigated types of
ate acids are left in the system [60]. The ratio of solvents varies
feedstock is lignocellulosic biomass with a typical composition of
according to the fermentation conditions and microorganism.
cellulose (40–45%), hemicellulose (20–30%), lignin (10–25%), ash
Integrated butanol recovery with advanced fermentation techniques
and extractives [40,41]. Examples include agricultural waste [42–48]
increased the butanol titres.
and dedicated energy crops [47].
The recalcitrant nature of lignocellulosic biomass feedstocks means
that either thermo-chemical hydrolysis or mild pretreatment and 4.3. Fed-batch
enzymatic hydrolysis is required to release the sugars, which is a major
constraint in making lignocellulosic conversion processes industrially Compared to conventional batch fermentation, fed-batch fermenta-
viable (cost-competitive). Pretreatment processes for butanol produc- tion has an advantage of high substrate concentration, high product
tion include dilute acid, liquid hot water [49] and alkaline processing concentration and a reduced hydraulic load and thus a reduction in the
[44,45,48,49]. Mild pretreatment processes are often used to minimize amount of waste water generated. Ezeji et al. [37] reported that fed-
the formation of inhibitors leading to the formation of a partially batch fermentation with integrated recovery improved the solvent
disrupted substrate subsequently converted to monomeric sugars by productivities by 400% of the control batch fermentation. In 201 h of
enzymatic hydrolysis. An alternative approach is to use a high severity fermentation, 500 g of glucose was utilized to produce 232.8 g of
pretreatment followed by detoxification methods such as overliming, solvents, with an average yield and productivity of 0.47 g/g and

Table 1
Various fermentation strategies applied to improve butanol production in glucose containing medium.

Substrate Organism Fermentation type Butanol titer (g/L) Refs.

Maltodextrin/Glucose C. beijerinckii BA101 Batch 19 [29]

Glucose C. acetobutylicum ATCC824 Batch 13.86 [30]
Glucose C. acetobutylicum Two stage continuous culture under phosphate limitation 12.97 [31]
Glucose C. acetobutylicum and C. beijerinckii batch with CaCO3 supplementation 14.78 [32]
Glucose C. beijerinckii NRRL B592 Two stage continuous culture 9.1 [33]
Glucose C. acetobutylicum Controlled pH 12.3 [34]
Glucose C. acetobutylicum Cryo gel beads immobilization 14.47 [35]
Glucose C. acetobutylicum Batch fermentation, pervaporation 32.8 ABE [36]
Glucose C. acetobutylicum Fed batch fermentation, pervaporation 165 ABE [36]
Glucose C. beijerinckii BA101 Continuous fermentation, gas stripping 460 ABE [37]

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Table 2
Summary of various pretreatment and detoxification techniques tested with various substrates and the resulted butanol concentrations.

Pretreatment and/hydrolysis Detoxification Organism ABE g/L Butanol g/L Refs.

Rice straw Alkali+Enzyme No C. acetobutylicum 2.85 2 [48]

Concentrated acid+Enzyme No C. acetobutylicum 2.1 1.4 [48]
Acid hydrolysis+Shear stress No C. acetobutylicum NCIM233 20.05 13.5 [51]
Dilute acid+Enzyme No C. sporogenes BE01 6.1 3.3 [7]
Dilute acid+Enzyme Anion exchange resin C. sporogenes BE01 7.78 5.6 [7]
Organo solvent+Enzyme No C. acetobutylicum 12.9 8.3 [52]

Corn stover Steam explosion+Enzyme Activated charcoal C. acetobutylicum ATCC824 12.38 8.2 [53]
Steam explosion+alkaline peroxide No C. acetobutylicum ATCC824 12.1 8.2 [53]
+Enzyme
Alkali extrusion+Enzyme No C. acetobutylicum ATCC824 11.2 7.1 [54]
Dilute acid+Enzyme Dilution of hydrolysate+Glucose C. beijerinckii P260 16 10.4 [47]
supplementation
Dilute acid+Enzyme Over liming C. beijerinckii P260 26.27 14.5 [47]

Corn stover+wheat Dilute acid+Enzyme No C. beijerinckii P260 18.4 12.3 [47]

straw
switch grass Hydrothermolysis+Enzyme No C. acetobutylicum ATCC824 5.63 4.3 [55]
Hydrothermolysis+Enzyme Calcium carbonate C. acetobutylicum ATCC824 7.92 5.46 [55]
Hydrothermolysis+Enzyme Activated carbon C. acetobutylicum ATCC824 16.8 11.3 [55]
Alkali+Enzyme No C. saccharobutylicum DSM13864 22.7 13 [56]
Dilute acid+Enzyme No C. beijerinckii P260 1.48 0.97 [47]
Dilute acid+Enzyme Dilution of hydrolysate+Glucose C. beijerinckii P260 14.61 9.55 [47]
supplementation
Dilute acid+Enzyme Overliming C. beijerinckii P260 Not enough growth of the [47]
culture

switch grass+Wheat Dilute acid+Enzyme No C. beijerinckii P260 8.91 5.79 [47]

straw
Corn fiber Dilute acid No C. beijerinckii BA101 1.7 – [57]
Dilute acid XAD-4 C. beijerinckii BA101 9.3 6.4 [57]
Dilute acid+Enzyme No C. beijerinckii BA101 1.6 – [57]
Hot water+Enzyme No C. beijerinckii BA101 8.6 6.5 [57]

Wheat straw Dilute acid+Enzyme No C. beijerinckii P260 25 12 [42]

Alkaline peroxide+Enzyme No C. beijerinckii P260 2.59 1.26 [43]
Alkaline peroxide+Enzyme Salt removal by electrodialysis C.beijerinckii P260 22.17 12.33 [43]

Barley straw Dilute acid+Enzyme No C. beijerinckii P260 7.9 4.8 [46]

Dilute acid+Enzyme overlime C.beijerinckii P260 26.64 18.01 [46]
Dilute acid+Enzyme+Surfactant No C. acetobutylicum DSM1731 10.8 7.9 [46]

1.16 g L−1 h−1 respectively. The hyperbutanol producer, C. acetobuty- 35 °C. In the process, wheat straw was hydrolyzed in fed-batch
licum JB200, produced 108.5 g/L of ABE with cassava bagasse fermentation and a total of 378.9 g sugar was fed together with 86 g
hydrolysate in a fed-batch fermentation integrated with gas stripping of wheat straw. ABE solvent concentration of 192 g/L was obtained
[28]. Guo et al. [61] tried non-detoxified sulfuric acid hydrolysate of with a corresponding yield of 0.44 g/g sugar. It was found that
corn fiber as the substrate in fed-batch fermentation and could achieve supplementing wheat straw with sugar increased productivity from
an ABE yield and concentration of 0.35 g/g sugar and 12.9 g/L, 0.31 to 0.36 g L−1 h−1. However, it is unlikely that sugar supplementa-
respectively, in 72 h by using the inhibitor tolerant C. beijerinckii tion will be appropriate for an industrial scale process.
RT66. Eliminating enzymatic hydrolysis and detoxification after the In simultaneous saccharification and co-fermentation (SSCF),
acid hydrolysis step will benefit process economics. Fed-batch is pentoses from the pretreatment stream are simultaneously fermented
relatively easy to operate for simultaneous saccharification and fer- with the hexoses released by enzymatic hydrolysis of lignocellulosic
mentation (SSF). Promising processes such as consolidated bioproces- biomass. The successful operation of this process depends on the
sing fermentation (CBP) are currently under development [62]. efficiency of the microorganism to utilize both hexose and pentose
sugars for solvent production during fermentation [40]. Shah and Lee
[63] investigated the simultaneous saccharification of pretreated hard-
4.3.1. Simultaneous saccharification and fermentation (SSF)
wood with extractive fermentation in a fed-batch mode at 36 °C in a
The advantage of SSF over separate hydrolysis and fermentation
750 mL bioreactor. An extractive recovery of biobutanol of 81.3% was
(SHF) is no sugar accumulation and feed-back inhibition of enzymes,
achieved, while that of acetone and ethanol were 57.8% and 33.3%
as the sugars released during the hydrolysis of lignocellulosic biomass
respectively. It should be noted that this process is appropriate with
are concurrently fermented by the microorganism in the same reactor.
lignocellulosic biomass as the feedstock pretreatment and subsequent
This improves the hydrolysis and fermentation efficiency by avoiding
enzymatic hydrolysis produce a mixture of hexose and pentose sugars
feed-back inhibition of sugars on the enzymes. However, one of the
This will increase the butanol yield per gram of lignocellulosic biomass
challenges with SSF is the difference in optimum temperatures for the
although the molar conversion of pentoses to butanol is less than
hydrolysis enzymes and fermentation bacteria. Enzymatic hydrolysis is
hexoses.
usually performed with the temperature range of 45–50 °C, while
solventogenic Clostridia require a temperature range of 35–37 °C for
fermentation. Qureshi et al. [44,45] investigated production of butanol
using C. beijerinckii P260 by SSF of dilute acid treated wheat straw at

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4.4. Continuous fermentation of 0.35 g/g and 0.38 g/g, respectively, and continuous two-stage
fermentation without immobilization of cells resulting in
In continuous fermentation, the broth volume is kept constant by 0.84 g L−1 h−1 productivity with a yield of 0.32 g/g [65,74,76].
continuous product removal and feeding of substrate thus reducing the A four-stage continuous fermentation using corn stover hydrolysate
lag phase commonly associated with batch and fed-batch fermenta- and cane molasses was investigated to improve the butanol titer and
tions. Cell wash out is a common drawback in continuous fermentation productivity. A gradient dilution mode (0.15–0.1/h) was applied to
with suspended cells thus limiting the dilution rate. This was observed cane molasses and a total of 13.75 g/L of ABE solvents with a
when saccharified and degermed corn was used for continuous productivity of 0.439 g L−1 h−1 was achieved. Corn stover hydrolysate,
fermentation with suspended cells, and resulted in low ABE concen- at a dilution rate of 0.15/h resulted in total solvent titer and
trations (14.16 g/L) after 504 h [64]. Immobilized cells and cell productivity of 11.43 g/L and 0.429 g L−1 h−1 respectively, which is
recycling can be used to avoid loss of cells during product removal. comparable with cane molasses [77].
Investigated immobilization support materials include brick, wood From the different fermentation strategies discussed fed-batch and
pulp, fibrous matrix, corn stalks, sugarcane bagasse, ceramic beads, continuous fermentations with immobilized cells (high cell density
tygon rings and PVA were tested for continuous fermentation [65]. fermentation) and fermentation integrated with butanol recovery
Continuous butanol fermentation of glucose and xylose with high cell resulted in a comparatively high butanol concentration, yield and
densities achieved by cell recycling doubled butanol productivity to productivity. Most of the immobilization methods reported were by
1.20 g L−1 h−1, when compared to 0.529 g L−1 h−1 for suspended cells adsorption on to cheaper support materials to improve commercial
[66]. Pierrot et al. [67] and Afschar et al. [68] reported solvent potential. However, using immobilized cells for SSF and SSCF pro-
productivities of 6.5 g L−1 h−1 and 4.5 g L−1 h−1 respectively, with cesses would be technically challenging because the substrate leads to
cell recycling. However, from various reports it is clear that cell formation of slurry in the reactor. Fermentation strategies which
immobilization is more efficient for butanol production than cell include integrated product recovery systems increase butanol produc-
recycling. Continuous fermentation with cells immobilized on brick tion by continuous removal of product. However, consideration of
and bonechar achieved the highest solvent productivity of industrial implementation is required in terms of the ease of operation
15.8 g L−1 h−1 and 6.2 g L−1 h−1 respectively with a glucose yield of and energy requirements.
0.38 g/g [69,70]. Lienhardt et al. [71] reported highest productivity of
16.2 g L−1 h−1 with clay brick as a support material for cell immobiliza-
5. Fermentation integrated ABE recovery
tion in packed bed reactor for continuous fermentation with effluent
recycling.
Conventional butanol recovery is by distillation, but this is an
While there are advancements in fermentation strategies particu-
energy intensive process and economically unfeasible for the recovery
larly for fed-batch and continuous processes, most of the studies have
of low butanol concentrations, with every ton of solvent recovered
been carried out using glucose as the carbon source, with limited
requiring approximately 12 t of steam [76,78]. Integrated butanol
reports to date on complex substrates (Table 3). This approach permits
recovery techniques that continuously remove solvents during fermen-
the establishment of reproducible fermentation protocols which can
tation enhance the butanol titres, productivity and yields by reducing
then be replicated using complex, low-cost feedstocks and thus to
the butanol toxicity to cells. As a result the product has a higher
develop feasible industrial processes.
butanol concentration which reduces the downstream processing
energy and thus financial costs. Though integrated recovery methods
4.5. Two stage and multi stage fermentation have several advantages over conventional distillation, they are also
associated with several challenges. Brief technical details, advantages
Two-stage fermentation allows complete utilization of substrate and and disadvantages of various in situ recovery processes is given in
efficient assimilation of acids to solvents. In a two-stage continuous Table 4.
cultivation with C.beijerinckii NRRL B592 an average solvent concen- Gas stripping for butanol recovery is easy to operate however
tration of 15 g/L with a productivity of 0.27 g L−1 h−1 was achieved for butanol selectivity (4–22) is low and thus operation near optimum
a period of steady-state operation of more than 1600 h [33]. Bankar conditions is required [79]. However, phase separation of this mixture
et al. [76] reported optimized continuous two-stage fermentation with could result in an organic phase of more than 60% butanol, which has
integrated liquid-liquid extraction to improve substrate utilization and selectivity of more than 75. Butanol selectivity increases with increas-
ABE production. Two-stage immobilized column reactors with inte- ing in butanol concentration and gas stripping above > 8 g/L will result
grated liquid-liquid extraction achieved a maximum solvent productiv- in a 15% (w/v) butanol condensate [28]. By gas stripping an ABE
ity and yield of 10.85 g L−1 h−1 and 0.38 g/g at a dilution rate of 1.0/h, concentration of 53.7 g/L was achieved in the condensate and the
when compared to a solvent productivity and yield of 2.5 g L−1 h−1 and selectivity was 30.5 [69]. Ezeji et al. [64] reported an increase of 219%
0.35 g/g achieved with a free cell two-stage continuous fermentation in ABE productivity with gas stripping compared to batch fermentation
with a liquid-liquid extraction system. Sugarcane bagasse and wood and an ABE titer of 38.3–99.6 g/L was obtained in the condensate.
pulp as support materials for a two-stage immobilized cell reactor Energy required for gas stripping of butanol from fermentation broth
resulted in 2.47 g L−1 h−1 and 10.85 g L−1 h−1, respectively, with yields with the concentration approximately 5 g/L and subsequent distillation

Table 3
Examples of fermentation strategies for improved butanol yield, concentration and productivities from lignocellulosic biomass.

Feedstock Fermentation type In situ recovery Fermentation microbe Butanol titer (g/L) Yield (g/g) Productivity (g L−1 h−1) Ref.

Wheat Straw Fed-batch Gas stripping C. beijerinckii P260 115.20 0.27 0.22 [45]
Corn Fiber Fed-batch None C. beijerinckii RT66 9.29 0.26 0.13 [61]
Cassava Bagasse Fed-batch+cell immobilization Gas stripping C. acetobutylicum JB200 76.00 0.23 0.29 [72]
Maple Wood Spent Fed-batch None C. acetobutylicum ATCC 824 7.60 0.21 0.047 [73]
Liquor
Spruce Spent Liquor Continuous+cell None C. acetobutylicum DSM 792 7.20 0.16 1.51 [74]
immobilization
Aspen Wood Fed-batch Extraction C. acetobutylicum ATCC 824 13.50 0.08 0.032 [75]

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L.D. Gottumukkala et al. Renewable and Sustainable Energy Reviews 76 (2017) 963–973

was estimated at 14–31 MJ/kg, while stripping butanol above 8 g/L

Mass-transfer limitation, fouling of membrane

Costs associated with separate flash tank. Low

solvents for efficient adsorption and biofouling

an advantage in terms of energy though ABE

emulsions, fouling of solvent in fermentation

High energy requirement. Cyclic vacuum has

with cells, loss of extractant to the aqueous

will reduce the energy requirement to approximately 8 MJ/kg [28]. A

Increased material property requirements,

membrane fouling and limited selectivity
Requirement of a high concentration of
vacuum process for gas stripping accelerates the butanol recovery from
Less selective towards butanol and low

Loss of extractant due to formation of

the fermentation broth. The vacuum can be applied intermittently or
continuously and the maximum ABE productivity of 0.34 g L−1 h−1 was
achieved with an intermittent vacuum and gas stripping [80]. Energy

productivity was decreased

requirements for continuous vacuum fermentation and downstream
distillation was 32.4 MJ/kg which was higher than the batch fermenta-

broth and toxicity

tion and distillation (26.8 MJ/kg). However, for cyclic vacuum fermen-
Disadvantages

tation the total energy requirement was 22 MJ/kg [80]. Total energy
requirements for flash fermentation and butanol distillation ranged
selectivity
efficiency

from 13.4 to 22.3 MJ/kg for butanol concentrations between 10.3 g/L

phase.
and 5.6 g/L, respectively, and the energy requirement was greatly
affected in the butanol concentration range of 8–13 g/L. With the
No fouling, easy operation, no toxicity

Fermentation at atmospheric pressure

Simple operation and High selectivity

No additional vessel to boil the broth

energy calculations required for recovery of various concentrations of

High flux, high allowable permeate

aqueous phase, reduced toxicity of
Physical separation of organic and
butanol, it was noticed that increase in butanol concentration as less as

pressure, low condensation costs

1 g/L will have significant effects on energy consumption [81].
Adsorbents can be generally

organic phase to the cells. A technique for improving the selectivity of gas stripping towards
and no harm to culture.

regenerated and reused

butanol is by placing a selective membrane in contact with the

under low pressure.

fermentation broth and applying a vacuum or gas purge on the other

side (pervaporation). The flux through the membrane is proportional to
to the culture
Advantages

the concentration gradient between the bulk liquid and bulk permeate
vapor and inversely proportional to the overall resistance [82]. PDMS
composite membranes and silicalite-silicone membranes showed better
performance over various membranes tested for pervaporation [27,83].
Polypropylene membranes have a high flux, a low selectivity (~6)
gas recycle rate, gas bubble size, size and type of

Flash tank pressure, permeate flow rate, product

Stripping temperature, condensing temperature,

membrane for solvents, mass transfer efficiency

composition, temperature and partial pressure.

concentration, inlet flow rate of the flash tank,

Membrane selectivity for solvents, membrane

Selectivity of the extractant, selectivity of the

towards butanol and high water permeability [84]. For silicate-silicone

Pressure in the fermentation vessel, product

extractant, toxicity of the extractant to cells.

concentration, continuous vacuum or cyclic

Type of adsorbent, product adsorption and

composite membranes in an integrated ABE fermentation-product

Broth/extractant ratio, selectivity of the
liquid outlet flow rate of the flash tank.

recovery system, butanol selectivity ranged between 95 and 200. A

surface area and thickness, permeate

maximum total solvent production of 155 g/L with 105.4 g/L of

butanol was reported with pervaporation using a silicalite-silicone
the condenser and anti-foam

composite membrane [27,85].

In liquid-liquid extractive fermentation, the extractant selection
desorption co-efficient
Process variables

needs to take into account cell toxicity. Oleyl alcohol is a well rated
of the membranes.

extractant, while methylated crude palm oil (CPOE) was found to be an

alternative to oleyl alcohol [86]. It was shown that ABE production and
vacuum.

yield is higher with extractive fermentation using methylated CPOE

compared to oleyl alcohol. Biodiesel can be enriched with butanol by
using it as extractant, thus bypassing the expensive process of product
recovery and extractant recycling. The ABE-enriched biodiesel had
passing nitrogen or fermentation gases through the medium

cell separator and the cell-free broth is pumped through the

The solvents dissolve in the extractant with a high partition

The extractant is in direct contact with fermentation broth.

The extractant is separated from the fermentation broth by

It is a membrane based liquid-liquid extraction technique.
and condensing the solvent vapors at temperatures below

Fermentation is performed under vacuum and the vapors

Fermentation broth is circulated to a flash tank, in which
the broth boils under low pressure (6.4–6.8 kPa) and the

Fermentation broth from the reactor is passed through a

Fermentation broth is placed in contact with membrane,

Solvents from the fermentation medium are stripped by

higher octane number and a low cold filter plugging point [87]. Though
while a vacuum or gas purge is applied for diffusion of

energy requirements for liquid-liquid extraction and perstraction are

are recovered by condensation. In cyclic vacuum

low, 7.7 MJ/kg, the selectivity is in the range of 1.2–4100 depending

fermentation, vacuum is periodically applied.

on extractant choice. Nevertheless, it has drawbacks including the large

Various techniques used in ABE fermentation with integrated product removal.

quantity of extractant required for recovery and reduced selectivity

towards acetone [85].
To overcome the effect of extractant toxicity on cells and increase
vapor is subsequently condensed.

a solvent permeable membrane.

solvents through the membrane

selectivity, in perstraction alcohol is separated from water by silicone

rubber membrane and polar or nonpolar solvents. With polar solvents,
the major drawback is permeation of solvent to the fermentation broth
causing solvent loss and cell death. The highest selectivity for butanol/
water separation can be achieved by non-polar solvents or membrane
Technique

solvent extraction with hydrophobic porous membranes such as porous

co-efficient.
resin bed.

Teflon or polypropylene [82]. On a large scale, high fluxes cannot be

10 °C.

obtained due to mass transfer resistance in the solvent phase [88].

Ionic liquids and non-ionic surfactants were also tested as extractants
and were proved to be efficient although they have been not studied in
Vacuum fermentation and

detail with an integrated fermentation system [85].

Liquid-liquid extraction

Adsorption is a simple technique that can be applied for recovery of

Flash fermentation

butanol from fermentation broth. Desorption of butanol from the

Recovery method

cyclic vacuum
fermentation

adsorbents can be carried out by heat treatment or using a low boiling

Pervaporation
Gas stripping

point solvent such as methanol. Several adsorbents like activated

Perstraction
Adsorption

carbon, XAD resins, bonopore, polyvinylpyridine, silicalite, etc., have

been tested for butanol adsorption [81,85,89,90,91]. Silicalite ap-
Table 4

peared to be more effective at concentrating butanol from dilute

solutions [5–810 g/L], when compared with bone charcoal and poly-

969
L.D. Gottumukkala et al. Renewable and Sustainable Energy Reviews 76 (2017) 963–973

vinylpyridine [89]. Heating silicalite to 78 °C desorbs the adsorbed equivalent corn ethanol plant with an NPV of $−26 million hence the
solvents and the recovery of butanol, acetone and ethanol were 100%, focus on alternative, cheaper feedstocks to improve the commercial
95.5% and 80% respectively [92]. Adsorption is incorporated into the viability. In contrast Mariano et al. [100] used the internal rate of
fermentation process either by (i) direct addition of adsorbents to return (IRR) to compare options using the pentose sugars from
fermentation broth or (ii) by packed bed adsorption (PBA). In direct sugarcane biomass and found that lowest rate of return, 11.3% applied
addition of adsorbents, removal for recovery of products and regenera- to the base case where the pentose sugars were converted to biogas.
tion causes process disruption. PBAs can be effective for clarified The lowest rate of return for butanol production was 13.1% for a
broths but cells and medium components of unclarified or partially regular Clostridium strain with butanol sold as a fuel. This can be
clarified broths will lead to fouling. The removal of cells and medium increased to 15.2% when using a modified Clostridium strain with
components by micro filtration and ultrafiltration will increase the butanol sold to the chemical market [100]. Qureshi and Blaschek [97]
capital and energy costs. Expanded bed adsorption (EBA) is a potential found that separation by distillation was more cost intensive than
alternative for PBA, as it eliminates the need for media clarification milling and fermentation and proposed that research relating to the
through fluidization of the adsorbent bed [93]. It has been reported separation process would be beneficial to reduce costs. Van der Merwe
that the hydrophobic polymer resin, Dowex Optipore L-493 is an [101] showed that by using liquid-liquid extraction in place of
efficient EBA adsorbent and can be regenerated by vacuum application distillation it was possible to improve the NPV from $−1858 million
with vapor collection, with an average of 81% butanol recovery. to $−1747 million. It was shown that when a fed-batch fermentation
Continuous fermentation with C. acetobutylicum ATCC824 and inte- was used in conjunction with gas stripping and then followed by liquid-
grated EBA recovery resulted in 27.2 g/L of butanol and total solvents liquid extraction the NPV was improved to a positive $ 958 million thus
of 40.7 g/L in 38.5 h which is a 2.2 and 2.3 fold improvement from making it possible to calculate an IRR of 36%.
conventional fermentation [93].
Qureshi et al. [89] reported that adsorption is more efficient than
other recovery methods due to the requirement of low energy when
compared to steam stripping, gas stripping and pervaporation.
Adsorption-desorption processes have energy requirements as low as 7. Conclusions
1948 kcal/kg (8 MJ/kg). However to develop a more detailed compar-
ison of the integrated recovery techniques a techno-economic study is Butanol is a superior fuel compared to ethanol and fermentative
required to estimate the mass and energy flows and thus assess the production of butanol through ABE fermentation was established over
economic parameters of each process. a century ago. But, the traditional process with starch and sugar as
substrates is currently not feasible. Global interest has shifted towards
6. Process evaluation by means of techno-economics renewable feedstocks such as lignocellulosic biomass to avoid food vs.
fuel and environmental issues associated with first generation feed-
Parameters such as yield, productivity and concentration are useful stocks, and to improve feedstock availability and sustainability. Cost-
for assessing and comparing experiments; however, improvements that effective and industrially feasible methods of lignocellulosic biomass
add substantial cost or complexity need a more thorough assessment to pretreatment and hydrolysis should be developed and optimized for
determine if there is an improvement to the commercial viability of the ABE fermentation for which necessary improvements are discussed
process. To increase the substrate spectrum and reduce feedstock costs, below
unconventional feedstocks like pineapple waste, sago waste residues 1. Lignocellulosic biomass conversion to sugars is currently a
and sweet sorghum juice are tested for biogas production [94–96]. significant contributor to the ABE process cost, but technology devel-
Butanol titres and yields are not promising for pineapple waste and opment for higher solid loadings (≥30% w/w) for pretreatment and low
sago waste residues, but sweet sorghum juice fermentation with enzyme dosage for enzymatic hydrolysis can substantially improve the
integrated gas stripping system yielded high titres of butanol. Such viability of lignocellulosic biomass to butanol process. An impressive
new developments should be tested for process and economic feasi- pretreatment technology would be mild treatment with a high solid
bility at industrial scale. loading resulting in minimal fermentative inhibitors and increased
Techno-economic modelling provides useful tools for investigating digestibility of lignocellulosic biomass.
this. Typically the overall process is simulated using a mass and energy 2. Although, strain improvement is not considered to have a
balance and this information is used to calculate the economic significant impact on process economics, it should be noted that an
parameters. These economic parameters can be used to assess com- increase in butanol concentration in the fermentation broth by using
mercial viability in a number of ways with one of the simplest hyper butanol producers will significantly reduce the energy consump-
approaches being to determine the cost of butanol production. tion for the product recovery and will therefore improve down-stream
It was determined that when hyper butanol producing C. process economics. Hence, more research on developing solvent
Beijerinckii BA101 was used for a butanol facility annexed to an tolerant-hyper butanol producers by either chemical mutagenesis or
existing corn milling facility in the mid-west region of the United States by genetic engineering is required.
of America (USA) that in 1998 the cost of butanol production would 3. Furthermore, improvements in fermentation with robust strains,
have been 0.55 US$/kg [97]. Tao et al. [98] used the minimum fuel capable of producing high titres of butanol with no or very less acetone
selling price (MFSP) and showed that in the USA cellulosic ethanol had No acetone in the mixture will avoid solvent separation costs in the
the lowest MFSP of 2.15 $/gal followed by corn butanol with 2.31 $/gal downstream processing, as ethanol and butanol in combination can be
and then the cellulosic butanol options of 3.08 and 3.33 $/gal for ABE used as fuel..
ratios of 0.5:9:0.5 and 3:6:1 respectively. When the MFSP was 4. An appropriate integrated solvent recovery system is required to
compared on a gasoline equivalent it was found that the corn butanol reduce or avoid product toxicity and to reduce the downstream
option was lower than that for cellulosic ethanol with MFSPs of 2.79 processing costs by concentrating the product stream. Well-known
and 3.27 $/gal respectively. integr`ated recovery systems like gas stripping and vacuum stripping
This approach provides data that is only relevant for a specific point are not efficient enough, while perstraction and pervaporation are
in time and an alternative analysis which considers the life time of the facing membrane fouling problems. Hence, a combination of recovery
project includes the use of a discounted flow sheet. Pfromm et al. [99] systems like gas stripping or vacuum stripping fitted with membrane
used a dynamic modelling approach to show that the net present value systems or gas stripping with liquid- liquid extraction is worth trying to
(NPV) of a corn butanol plant would be $306.6 million compared to an bring biobutanol to fuel market.

970
L.D. Gottumukkala et al. Renewable and Sustainable Energy Reviews 76 (2017) 963–973

Acknowledgements continuous culture studies. J Ind Microbiol Biotechnol 2001;27:18–26. http://

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