Insight into Biomass as a Renewable Carbon Source for the

Review pubs.acs.org/IECR

Insight into Biomass as a Renewable Carbon Source for the Production of Succinic Acid and the Factors Affecting the Metabolic Flux toward Higher Succinate Yield Jian Ping Tan,† Jamaliah Md. Jahim,*,‡ Ta Yeong Wu,§ Shuhaida Harun,‡ Byung Hong Kim,∥ and Abdul Wahab Mohammad‡ †

Chemical and Process Engineering Department and ‡Research Centre for Sustainable Process Technology (CESPRO), Faculty of Engineering and Built Environment, and ∥Fuel Cell Institute, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia § Chemical Engineering Discipline, School of Engineering, Monash University, Jalan Lagoon Selatan, Bandar Sunway, 46150, Selangor Darul Ehsan, Malaysia S Supporting Information *

ABSTRACT: The current world demand for succinic acid is around 30 000 tonnes per annum, which is forecast to expand 6fold by 2015, owing to the introduction of biosuccinic acid. An insight into the practical usage of different biomass derivatives as substrates in the commercial bioproduction of succinic acid is discussed. Lignocellulosic crop stalk waste (corn straw, rice straw, and cotton straw) appears, in this case, to be the most promising form of biomass for commercial succinic acid fermentation. Another example of a low cost carbon source with high availability, crude glycerol, on the other hand, shows comparable potentials as a sustainable commercial carbon source for biosuccinic acid. In terms of the metabolic pathway of succinateproducing microbes, a greater availability of substrate CO2 and a lower oxidation/reduction potential (ORP) of the fermentation broth will trigger the microbial metabolic flux toward the generation of highly reduced metabolites (succinate) in order to regain an intracellular redox balance.

1. BIOSUCCINIC ACID: CURRENT TRENDS 1.1. Introduction to Biosuccinic Acid. Rising oil prices, increasing consciousness of environmental implications, sustainable growth in the economy and materials are among the driving forces toward the reconsideration of many petrochemical processes. Climate deterioration and the negative effects of the exploitation of fossil fuels are getting visible.1 The lower cost of chemical production through a petrochemical approach is attributed to the large amount of research and optimization of the process over half a century, as compared to the biological approach. But, this situation will soon be different, because of depleting fossil fuels and the optimization of biological processes for chemical production. Biochemical approaches to converting renewable resources into valuable chemical products is a growing, multibillion dollar industry.2,3 Succinic acid which has the molecular formula of C4H6O4 is also known as butanedioic acid. Conventionally, succinic acid is petrochemically produced on an industrial scale via catalytic hydrogenation of maleic anhydride or maleic acid.4 However, bioproduction of succinic acid is now a rising alternative, which is overtaking the conventional petrochemical approach and gaining the interest of global players. This four-carbon dicarboxylic acid, succinic acid, has been identified as one of the 12 chemical building blocks that can potential be produced commercially through biological conversion, according to the US Department of Energy in 2004.5,6 1.2. Environmental Benefits of Biosuccinic Acid. From an environmental point of view, the current succinic acid bioproduction technology can reduce greenhouse gas (GHG) © 2014 American Chemical Society

emissions by 50% compared to the production of equivalent petrochemical products. Further development of this approach could potentially realize an 80% reduction in GHG emissions.7 Life-cycle analysis showed that bioproduction requires about 30−40% less energy than a typical chemical production process.4 Bioproduction of succinic acid does not only reduce GHG emissions, but it actually absorbs CO2 in the process.4 This biosuccinic acid production technology is aligned with the mission of the United Nation Framework Convention on Climate Change (UNFCCC), which is to minimize the carbon footprint by using green technologies in chemical production. 1.3. World Market for Biosuccinic Acid. The current market volume of succinic acid, reported by the Royal Society of Chemistry in 2014, is around 30 000 tonnes per annum, creating a market capacity of $225 million.10 The world succinic acid market is forecast to grow at an 18.7% compound annual growth rate (CAGR) from 2011 to 2016.8 Succinate can achieve a $15 billion market by producing bulk chemicals such as ethylenediamine disuccinate (a biodegradable chelator), diethyl succinate (a replacement of methylene chloride), 1,4butanediol (a plastic precursor), and adipic acid (nylon precursor).9 It is believed that this could create a market of 180 000 tonnes which is 6-fold the current market size by the market research firm of Frost and Sullivan, owing to the introduction of biosuccinic acid.10 According to James Received: Revised: Accepted: Published: 16123

May 29, 2014 September 10, 2014 September 19, 2014 September 19, 2014 dx.doi.org/10.1021/ie502178j | Ind. Eng. Chem. Res. 2014, 53, 16123−16134

Industrial & Engineering Chemistry Research

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using yeast technology for biosuccinic acid production.15 In addition, US-based Myriant was supported by the US Department of Energy in setting up a commercial-scale facility in Louisiana.10 The development of this exciting technology can be a platform to develop other potential biobased chemical building blocks.

Lademarco, chemical company DSM’s Vice President for biobased chemicals and fuels, biosuccinic acid could expand to a market that is 10-fold the capacity of current succinic acid demand.10 Dilum Dunuwila, Vice President of business development at Diversified Natural Products Inc. (DNP), and Jean-Francois Huc, Chief Executive of DNP Green Technology, believe succinic acid is not used much today because of its cost and that bioproduction will change succinic acid from a specialty to a commodity chemical.10 This belief is shared by Will van den Tweel, General Manager of Reverdia.11 Susanne Kleff, Senior Scientist for Michigan Biotechnology Institute, outlined the three largest potential markets for biosuccinic acid. The primary potential opportunity is a replacement for petrochemical maleic anhydride, which currently serves a 1.65 million tonnes capacity annually. This is followed by global demand for polymers, currently derived from butane, which occupy a market capacity of more than £1.6 million per annum. The other potential capacity for biosuccinic acid is for pyrrolidinones which are used in the production of ecofriendly chemicals and green solvents for water treatment, which currently serves a global market capacity of about £100 million annually.12 Cenan Ozmeral, Myriant’s General Manager for specialty chemicals, forecast that the total penetration of the biobased succinic acid market would hit $10 billion.10 1.4. Current Ongoing Commercialized Biosuccinic Acid Plants. Today, bioproduction of succinic acid is no longer a theoretical topic, but it has, in fact, stepped into a commercial scale. Over the past few years, several key players in succinic acid production have started commercializing biobased succinic acid production plants. Commercialised biobased succinic acid production by several companies is summarized in Table 1. BASF,13 Purac, BioAmber,14 Mitsui, and PTT MCC Biochem are among the early players of biosuccinic acid production, as shown in Table 1. Reverdia (joint venture between DSM and Rouquette) also joined this revolution by

2. BIOMASS AS A RENEWABLE CARBON SOURCE FOR SUCCINIC ACID FERMENTATION 2.1. Introduction of Sugar-Based Biomass As Succinate Fermentation Feedstock. In order to create biosuccinate industry, the costs of production have to be made competitive with the maleic anhydride industry. Maleic anhydride is in increasing demand in spite of rising oil prices.17 The economic viability of a bioprocess is governed by three important process parameters: titer, yield, and productivity. The term, yield, or the conversion of raw material into product succinic acid affects significantly the cost of the raw feedstock per kilogram of succinic acid produced which is now in increasing importance due to the rising price of sugar. Productivity and product concentration are linked to the total capital investment.2,3 Low rates imply larger labor and energy costs, and low product concentration will lead to larger initial investment to maintain the plant capacities. The use of sugar-based biomass is aimed at lowering the cost of the raw feedstock that would replace pure glucose in fermentation. The ability of sugar-based biomass to replace pure glucose has been proven and has been a favorite topic of researchers around the world. The discussion in this chapter provides an insight into reported biomass for succinate fermentation and its practicality in commercialization. 2.2. Reported Biomass for Succinic Acid Fermentation. Reducing the cost of carbon sources using biomass will directly affect the production cost of biosuccinic acid per kilogram. Different biomass claims to have its own benefits. Among the benefits that were claimed by different biomass sources were low cost, high availability, high yield, high concentration of fermentable sugars and low reliance on external nutrient sources. Table 2 compiles the reported usage of different biomass in the fermentation of succinic acid. Several fermentation strategies have been reported for biomass fermentation, including simultaneous saccharification and fermentation (SSF),18 hydrolysis of raw material in a separated process followed by batch fermentation,19 solid-state fermentation,20 fed-batch fermentation,21 and continuous fermentation,22 as tabulated in Table 2. Batch fermentation is the most widely used fermentation strategy in succinate production, owing to its benefits in term of ease of handling and low risk of contamination. Moreover, batch fermentation also enables the production of different fermentation products throughout the year by sharing the same facilities. These are among the reasons for batch fermentation to be chosen by most researchers studying succinate fermentation. Succinic acid is a fermentative end-product and an intermediate metabolite of the Krebs cycle.23 This allows microorganisms to be the perfect host for producing succinic acid. Several popular strains that have been reported for the fermentation of sugar-based biomass are Actinobacillus succinogenes, Mannheimia succiniciproducens, Anaerobiospirillum succinoproducens, and Esterichia coli, as tabulated in Table 2. Others, including Corynebacterium glutamicum,24 Bacteroides fragilis,25 Saccharomyces cerevisiae,26,27 Lactobacillus plantarum28 are introduced recently as succinate platform strains. Most of

Table 1. Biosuccinic Acid Production Capacitya company

annual capacity (tonnes)

BASF-Purac JV

25000

BioAmber-ARD

3000

BioAmber Mitsui JV BioAmber Misui JV

65000 17000 (initial stage), 34000 (at full capacity) 65000 13600

BioAmber Mitsui JV Myriant

Myriant-China National BlueStar Myriant

110000

Myriant-Uhde (owner and operator) Reverdia (DSMRouquette) PTT MCC Biochem

500 (first year)

77110

10000 36000

plant location

operational date

Barcelona, Spain Pomacle, France US or Brazil Sarnia, Ontario, Canada

2013

Thailand Lake Providence, Louisiana Nanjing, China

2014 Q1 2013

Lake Providence, Loisiana Infraleuna sit, Germany

Q1 2014

Cassano Spinola, Italy Rayong, Thailand

H2 2012

full capacity by Q2 2012 NA 2013

NA

H1 2012

NA

NA = Not available. Q1= first quarter of the year. H1 = first half of the year. H2 = second half of the year. Source: refs 11 and 16. a

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Table 2. Different Biomass for Succinate Fermentationa carbon source

bacteria

corn straw

A. succinogenes

corn core cotton straw straw hydrolysate rice straw wheat straw gluten-free flour hydrolysate (GFFH) acid-pretreated rapeseed meal sake lees (acid pretreated) waste bread

A. A. A. A. A. A.

sugar cane bagasse

E. coli

sugar cane molasses soybean meal soybean solubles whey

succinogenes succinogenes succinogenes succinogenes succinogenes succinogenes

A. succinogenes A. succinogenes A. succinogenes

A. succinogenes A. succinogenes E. coli E. coli E. coli A. succiniciproducens

cheese whey wood hydrolysate

A. succinogenes A. succiniciproducens Mannheimia succiniciproducens

glycerol

A. succinogenes E. coli A. succiniciproducens

strategy

nitrogen source

BF BF SSF BF BF BF BF BF BF BF SoSF

5 g L−1 CSL 10 g L−1 YE 30 g L−1 YE 20 g L−1 CSL 15 g L−1 YE SYC 15 g L−1 YE 30 g L−1 YE 15 g L−1 YE 15 g L−1 YE 15 g L−1 YE 30 g L−1 gluten hydrolysate none 2.5 g L−1 YE 200 mg L−1 FAN 15 g L−1 YE 5 g L−1 YE 10 g L−1 Trp 10 g L−1 Trp 5 g L−1 YE 10 g L−1 Trp 5 g L−1 YE 5 g L−1 CSL 10 g L−1 YE 10.0 g L−1 YE 10 g L−1 Trp 5 g L−1 YE none none 10 g L−1 CSL 10 g L−1 CSL 10 g L−1 CSL 5 g L−1 YE 10 g L−1 CSL 5 g L−1 YE 5 g L−1 YE 5−10 g L−1 YE 10 g L−1 Trp 5 g L−1 YE 2.5 g L−1 YE

SSF BF BF FBF FBF BF DPF BF BF BF BF BF BF FBF CF BF BF BF CF BF BF BF

succinic acid concentration (g L−1)

succinic acid yield (g g−1)

ref

50.24 17.8 47.4 33.70 52.9 32.07 15.8 45.5 17.64 18.96 64.2

0.726 0.66 0.72 0.81 0.68 0.891 1.23 0.807 0.628 0.741 0.81

19 35 18 36 37 36 35 36 36 36 20

15.5 52.3 47.3 53.2 39.3 15.85 18.88 20 46.4 55.8 11.21 36.84 34.3 34.7 19.8 27.9 24 11.7

0.124 0.59 1.16 0.66 0.89 0.96 0.65 0.80 0.96 0.64 0.64 0.8 0.906 0.6 0.57 0.88 0.56 0.55 1.23 1.03 1.33

37 38 39 36 40 40 40 41 42 43 34 34 21 21 21 44 45 22 22 46 47 48

29.3 12.05 4.9

a BF: batch fermentation. SSF: simultaneous saccharification and fermentation. SoSF: solid state fermentation. CF: continuous fermentation. FBF: fed-batch fermentation. DPF: dual-phase fermentation. FAN: free amino nitrogen. SYC: spent yeast cells. YE: yeast extract. CSL: corn steep liquor. Trp: tryptonnee.

Table 3. Cost, Source Availability, and Yield of Biomass As a Function of Succinate Production

a

biomass

cost of raw material ($ tonne−1)

ref

yield (g g−1)

ref

availability (million tonnes y−1)

ref

corn straw glycerol corn core/cob wheat wheat straw cotton straw rice straw rapeseed meal waste bread sugar cane bagasse sugar cane molasses soybean meal whey wood (oak) hydrolysate sake lees

40.5 219.5 40 261 60 38 29 324 60 23 140 506 795 65 NAa

53 55 54 58 59 52, 50 51 57 60 49, 50 61 57 56 62 NA

0.81 1.33 0.89 0.81 0.74 1.23 0.63 0.12 (SSF) 1.16 0.89 0.96 0.64 0.8 0.88 0.59

36 48 36 20 36 35 36 37 39 40 43 34 21 45 38

1015 600 84 704 915 107 800 30.8 0.8 (UK) 73.6 56 151.6 2.45 NA NA

64 63 65, 66 67 67, 68 69 51 57 60 70 71, 72 73 74 NA NA

Not available.

because of its versatility in terms of carbon sources.29 The versatility of carbon sources allows A. succinogenes to be able to

the reported biomass fermentation of succinic acid, as compiled in Table 2, uses A. succinogenes as the fermentation microbe, 16125



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resulting in a lower amount of substrate needed to produce an equivalent amount of succinate. The yields presented in Table 3 are based on the reported yields utilizing biomass in batch fermentation, except for acid pretreated rapeseed meal, which was processed by simultaneous saccharification and fermentation (SSF).37 The highest reported succinate yield was from glycerol and amounted to 1.33 g g−1,48 followed by cotton stalk wastes at 1.23 g g−1 35 and waste bread at 1.16 g g−1,39 according to Table 3. The yield of succinate from these biomass sources was above 1 g g−1 from fermentable sugars. This could be due to CO2 fixation in the process of fermentation.75 iii. Availability of Raw Material. The availability of renewable feed resources is important for the sustainable commercialization of succinic acid. Although it does not affect directly to the cost of succinate production, it is vital to have a sufficient supply of the feedstock to ensure sustainability of the production and plant operability. Availability of biomass here is discussed in terms of global production of the biomass per annum (million tonnes/y). The main biomass that dominate this parameter includes corn straw (1015 million tonnes y−1),64 wheat straw (915 million tonnes y−1),67,68 rice straw (800 million tonnes y−1),51 wheat (704 million tonnes y−1),67 and biodiesel byproductglycerol (600 million tonnes y−1).63 On the other hand, waste bread (0.8 million tonnes y−1)60 in UK, whey (2.45 million tonnes y−1),74 and rapeseed meal (30.8 million tonnes y−1)57 biomass become less important in the aspect of availability as they could be seen in Table 3. The large and continuous supply of biomass allows the continuous operation of succinate fermentation plant. 2.4. Ranking of Biomass Based on Three Parameters. Three studied parameters for commercial biosuccinic acid production accounted for the ranking of potential commercial biomass for biosuccinic acid production. Table 5 presents the score by each biomass source based on the cost of biomass per tonne, the availability of the biomass in tonnes and the yield in grams per gram. The cost and the yield directly affect the cost of biosuccinic acid production (kg−1) and were given a weighting of forty while the availability of biomass had a weighting of twenty. The total score suggests the level of feasibility of the biomass source for commercial succinate fermentation based on these three parameters. The score for each parameter is quantified as shown in Table 4.

convert a variety of carbon sources contained in biomass into succinic acid. In a single batch fermentation process, a wild type of A. succinogenes is able to produce 80 g L−1 succinate.30 This natural ability to produce a high succinate concentration is another attribute that leads to the popularity of A. succinogenes in biomass succinate fermentation. Thus, A. succinogenes is considered as among the best biocatalysts for industrial succinate fermentation29−31 Biomass serves as the carbon source for succinate fermentation. However, nitrogen is another important nutrient required for the growth of microorganisms needed in succinate fermentation. Yeast extract and tryptone are among the common added nitrogen sources for succinate fermentation, which can be seen in Table 2. Recent studies have shown that a byproduct of corn starch production, corn steep liquor (CSL), could replace peptone and yeast extract, as its usage has been reported in fermentation with A. succinogenes32 and A. succiniciproducens.33 Another attempt to reduce the nitrogen cost is to use yeast cell hydrolysate (YCH).19 The use of CSL and YCH will help to reduce the cost of the nitrogen source in succinate production. Biomass materials such as wheat,20 soybean meal and soybean solubles,34 see Table 2, do not require an additional nitrogen source, because they have sufficient nitrogen content in the biomass that can accommodate the bacteria growth. Thus, the use of these biomass derivatives can eliminate the cost of a nitrogen source. 2.3. Industrial Feasibility Analysis of Biomass for Commercial Succinic Acid Fermentation. Many researchers have used different biomass sources for succinate fermentation; however, the real application of biomass on an industrial scale requires further investigation. In this section, we focus on the most critical parameters for various biomass sources such as the cost of biomass per tonne, the yield of succinate from biomass and the global availability of biomass per tonne. These findings are discussed and presented in Table 3. These parameters have been identified as being important for the biomass to be used as a feed for commercial succinate production. i. Cost of the Raw Material. The cost of the raw material is of utmost importance in evaluating the potential of biomass in commercial biosuccinic acid fermentation. The cost of the raw material will directly affect the total production cost per kilogram of succinate. In fact, the main reason for finding suitable biomass to replace pure sugars in biosuccinic acid fermentation is to reduce the cost of the raw material. The lower cost of the raw material contributes to the feasibility of biosuccinic acid production on an industrial scale. We considered the cost of the raw material is in U.S. dollars ($) per tonne of biomass as these figures have been reported elsewhere. Sugar cane bagasse ($23 tonne−1),49,50 rice straw ($29 tonne−1),51 cotton stalks ($38 tonne−1),52,50 corn straw ($40.5 tonne−1),53 and corn core ($40 tonne−1)54 are among the potential biomass sources summarized in Table 3. On the other hand, whey ($795 tonne−1),56 soybean meal ($508 tonne−1),57 rapeseed meal ($326 tonne−1),57 and wheat ($300 tonne−1)58 are among the biomass sources that do not have a promising raw material cost for biosuccinic acid fermentation, as shown in Table 3. ii. Succinic Acid Yield. Yield is identified as another crucial parameter to be taken into account in the analysis at the commercial stage as it significantly affects the cost of the raw material per kilogram of the product. Higher yield implies higher conversion of the substrate to the product (succinate),

cost = (highest cost of biomass − cost of boimass per ton) × 40 highest cost of biomass − lowest cost of biomass (1)

yield =

yield of biomass × 40 highest yield of biomass

availability =

(2)

availability of biomass × 20 highest availability of biomass

(3)

Table 4. Score for Each Paramter parameters score weightage 16126

cost

yield

availability

total score

40

40

20

100



Review

annum for both corn and rice straw), and the high yield of succinic acid (g g−1). These crop stalks are categorized as lignocellulosic biomass, which represent the most abundant feedstocks on the planet.65 Despite its strengths, these biomass sources have a major drawback regarding the cost of pretreatment. The sugars in this lignocellulosic biomass are not readily available, since they are stored in the form of complex carbohydrates. Several pretreatment methodologies, including physical pretreatment (milling, extrusion, microwave, and freezing pretreatment), chemical pretreatment (alkaline, acid, ionic liquid, organosolv, and ozonolysis pretreatment), physiochemical pretreatment (steam explosion, ammonia fiber explosion (AFEX), carbon dioxide explosion, liquid hot water (LHW), and wet oxidation (WO) pretreatment), and biological pretreatment (enzymatic pretreatment) are among the approaches that can be used to harvest fermentable sugars from complex carbohydrates (cellulose, hemicellulose, and lignin) in lignocellulosic biomass.79 Sugar cane bagasse (ranking 7) and wood hydrolysate (ranking 11) are lignocellulosic biomass sources that require a pretreatment step as well. iii. Glycerol (Ranking 2). Glycerol, with total score of 82.1, represents a different type of raw material compared to other potential biomass sources as a commercial succinate production feedstock. The global effort in reducing petroleum dependence is the main driving force behind the rise in biodiesel production.46 One kilogram of crude glycerol is produced from the production of 10 kg of biodiesel.77 Glycerol is formed from the production of biodiesel, where vegetable oil or animal fat reacts with alcohol.78 Glycerol is a highly available biomass (∼600 million63 metric tonnes per annum) owing to the increasing production of biodiesel. Despite its strengths, the cost of raw glycerol (75% glycerol) has shot up in the past two years, making it less competitive ($219.5 tonne−1)55 as compared to crop straw wastes.55 However, glycerol can be used in biosuccinic acid production without cost-consuming pretreatment procedures which are needed for lignocellulosic crop straw wastes. In addition to this, the exceptional high yield of succinate from glycerol (1.33 g g−1)48 outshines other types of biomass. Judging from the readily available substrate, high annual availability and high succinate yield, glycerol could be considered considered among the highly promising carbon source for commercial succinate fermentation, after corn straw waste. iv. Waste Bread (Ranking 6). Waste bread possesses a high carbohydrate content (50% w/w)39 and a high biosuccinic acid yield of 1.16 g g−1.39 Waste bread is currently used as animal feed80 with an estimated cost of $60 tonne−1.80 However, waste bread is not highly available compared to other agricultural/ industrial biomass byproducts, as shown in Table 3. Generally, the quality of waste bread varies from one source to another, in which some of the waste bread might include different compositions such as flavorings, cream or fats that will cause a fluctuation in the composition of the this biomass as a raw material. This fluctuating composition will lead to difficulties during fermentation optimization. In order to avoid fluctuations in the composition, only plain waste bread can be used in commercial succinate fermentation which will further reduce the already low availability of waste bread. v. Corn Core/Cob (Ranking 8). Global availability of corn cob is estimated to be 84 million tonnes per annum.65,66 The availability of this biomass is due to the large global corn industry. Corn core had a score of 68.1 in this analysis and a

These quantifications reflect the score of the biomass source for each parameter in the analysis. The last column in Table 5 shows the final score of each biomass source out of 100 (full score). Table 5. Ranking of Biomass in Terms of Commercial Feasibility Based on Three Parameters ranking

biomass

1 2 3

corn straw a glycerol cotton straw wheat straw rice straw waste bread sugar cane bagasse corn core wheat sugar cane molasses wood (oak) hydrolysate soybean meal rapeseed meal whey sake lees

5 6 7 8 9 10 11 12 13 14 15

scores for cost (per 40)

scores for yield (per 40)

scores for availability (per 20)

total scores (per 100)

39.1 30.3 39.2 38.1 39.7 38.6 40.0

24.4 40.0 37.0 22.3 18.9 34.9 26.8

20.0 11.8 2.1 18.0 15.8 0.0 1.5

83.4 82.1 78.3 78.3 74.4 73.5 68.2

39.7 27.5 34.4

26.8 24.4 28.9

1.7 13.9 1.1

68.1 65.7 64.4

37.8

26.5

0.0

64.3

15.2

19.2

3.0

37.4

24.8

3.6

0.6

29.0

0.0 NAb

24.1 17.7

0.0 NA

24.1 17.7

a

Glycerol is not considered as a biomass but as a carbon source that was used in succinic acid production; it is used as a comparison in the analysis. bNot available.

i. Cost of Pretreatment for Lignocellulosic Biomass. The National Renewable Energy Laboratories (NREL) reported a detailed economic analysis on the production of ethanol from lignocellulosic crop stalks (corn stover). In the report, the additional cost of pretreatment required for lignocellulosic crop straw was estimated based on the economic analysis done by the NREL. The ratio of the cost of feedstock to the cost of pretreated corn stover in ethanol production was used as a basis for the cost estimation of pretreatment in the current analysis. The amount of $11.07 tonne−1 was estimated as the additional cost needed for the pretreatment of lignocellulosic crop stalks that to be used as the feed in fermentation.76 The calculation was made with the additional cost of $11.07 tonne−1 (estimated cost of pretreatment added to the cost of raw biomass) for all lignocellulosic biomass before the biomass ranking was determined. The calculation of the cost estimation for pretreatments of various lignocellulosic biomass is available in the additional information The criteria for each biomass according to their ranking are discussed in the following section. ii. Lignocellulosic Biomass (Biomass Rankings 1, 3, 5, 7, and 11). Crop straw occupies the top ranking in biomass analysis based on the cost of biomass, the availability of biomass, and the yield. Corn straw (ranking 1), cotton straw (ranking 3), wheat straw (ranking 3), and rice straw (ranking 5) are promising biomass sources as a commercial biosuccinic acid production feedstock. These biomass sources may be better than others in term of the low cost per tonne of biomass (mostly less than $50 tonne−1 except for wheat straw), extremely high availability (∼1 billion metric tonnes per 16127



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ranking of 8. However, it has a high yield (0.89 g g−136) and competitive cost ($40 tonne−154). vi. Sugar Cane Molasses (Ranking 10). Sugar cane molasses is a natural nutritious sweetener harvested from sugar cane during the production of refined sugars. Sugar cane molasses has a global availability of 56 million metric tonnes per annum,71,72 a high yield of 0.96 g g−1,43 and a moderate cost of $140 tonne−1,61 as can be seen in Table 3. This biomass source had a score of 64.4 and was ranked 10th in the current analysis, shown in Table 5. vii. Wheat (Ranking 9) and Soybean Meal (Ranking 12). Wheat and soybean meal are biomass sources that have been claimed to function as both the carbon source and the nitrogen source for biosuccinic acid production. These types of biomass can minimize the cost of adding a nitrogen source. Despite its extra function as nitrogen source, wheat ($261 tonne−1)58 and soybean meal ($506 tonne−1)57 are comparatively costly carbon sources. In terms of availability and yield, wheat is reported to have a large supply at 704 million metric tonnes/annum67 but with a moderate succinic acid yield of 0.81 g g−1.20. The availability and yield of wheat are comparable with the other top ranking biomass sources. Soybean meal, on the other hand, has moderate availability of about 151 million metric tonnes per annum73 and a lower yield of 0.64 g g−1.34 viii. Rapeseed Meal (Ranking 13), Whey (Ranking 14), and Sake Lees (Ranking 15). Rapeseed meal, whey, and sake lees have the potential to reduce the dependence on an external nitrogen source. Rapeseed meal is a byproduct from the oil extraction of rapeseed.37 Whey is the waste from cheese making, which has a high biological oxygen demand (potential pollutant).44 Sake lees is a byproduct from brewing liquefied rice.38 Although it is not mentioned in the literature,37 rapeseed meal or canola meal contains a high protein concentration (35%) as reported by the United States Department of Agriculture57 in their weekly report. This protein content is 12% less than that of soybean meal,34 which does not require an additional nitrogen supply. Considering its high protein concentration, rapeseed meal might have the ability to reduce or eliminate reliance on an external nitrogen source in succinic acid fermentation. In spite of the cost savings on a nitrogen source, rapeseed meal has a relatively lower global availability of 30.8 million metric tonnes per annum.57 Moreover, the cost of rapeseed meal can be as much as $324 tonne−1,57 which is higher than the reported cost of glycerol or straw hydrolysate, thus making this biomass less attractive than glycerol and crop straw wastes. Whey, on the other hand, contains 17−27% protein, which might allow for a reduction in the cost of the nitrogen source, but this, has not been reported in the published journals. The U.S. Dairy Export council has estimated that the global production of dry sweet whey was about 2.45 million metric tonnes per annum in 2013.74 This figure has been flat over the past five years.74 The yield of succinate from whey is reported to be 0.8 g g−1.21 The cost of whey, however, is quite high ($795 tonne−1),56 making whey less competitive than other biomass sources for commercial succinate fermentation. Sake lees is reported to provide a succinic acid yield of 0.59 g g−1,38 and it may allow for reduced addition of a nitrogen source. The yield of succinic acid from sake lees is much lower than that of the other biomass sources (after rapeseed meal). Further research to increase the yield of this biomass might be helpful to make sake lees more competitive and feasible as a

sustainable carbon source in commercial biosuccinic acid production.

3. FACTORS AFFECTING THE METABOLIC FLUX OF SUCCINIC ACID PRODUCTION The cost of biomass and the availability of biomass cannot be manipulated by researchers. The yield, on the other hand, can be significantly enhanced by manipulating several factors governing the metabolic flux toward a higher yield of succinate. A metabolic flux shunt in succinate-producing microbes is governed by several factors. Reports on the optimization parameters of succinate production using different microbes have shown similar phenomena. The understanding of these exciting phenomena enables the manipulation of the fermentation conditions to promote a higher flux toward succinate and to reduce the generation of formate, acetate and ethanol byproducts. Table 6 summarizes several common phenomena governing the metabolic flux shunt in succinate production using different microbes. 3.1. Stoichiometry of Succinic Acid Production. Theoretically, every mole of glucose is able to produce 2 mol of biosuccinic acid when the presence of CO2 is in excess. However, 1 mol of glucose can only synthesize 2 mol of NADH, and the generation of 2 mol of biosuccinic acid needs 4 mol of NADH. Thus, two more extra moles of NADH are needed. Availability of NADH is the bottleneck for higher succinate generation. A greater availability of NADH can be achieved by several methods. The use of lower oxidation state carbon sources, the presence of an external reducing agent and lower oxidation−reduction potentials (ORP) in the medium are among the driving forces toward higher yield of succinate. However, after the consideration of ORP, van Heerden and Nicol have come up with the equation suggesting a mole of glucose reacts with 6/7 mol of carbon dioxide could produce 12/7 mol of succinic acid and 6/7 mol of water.108 Therefore, the maximum yield of succinate becomes 1.71 mol per mole of glucose. When expressed in mass units, the above equation results in a succinic acid yield of 1.12 g succinic acid per gram glucose. This equation ignores the formation of biomass and gives the maximum possible yield of succinate based on 1 mol of glucose after considering the effect of reduction potential. 3.2. Effect of ORP on Metabolic Flux toward Succinate Production. An external redox potential will influence the intracellular reducing equivalents.109 Microbes can be triggered to generate more highly reduced metabolites, such as succinic acid by manipulating the fermentation broth redox potential to a lower level. This is a way for the microbe to dispose excessive electrons to regain the intracellular redox balance. ORP values reflect the amount of available electrons in the fermentation medium. Lower medium’s ORP signifying higher availability of electrons, thereby promoting an increased production of succinate. Lower ORP values, for instance at −300 mV in Corynebacterium crenatum91 and −400 mV in Escherichia coli,83 have been reported to lead to an increase in the NADH/NAD+ ratio, triggering higher succinate producing enzymatic activities in the microorganisms. Enzymatic activities and the NADH/NAD+ ratio affect each other.110 The increase in the NADH/NAD+ ratio will, in turn, increase the metabolic flux of microorganisms toward the generation of more reduced metabolites (e.g., succinic acid) production. In addition, a decrease in the substrate consumption rate is also reported in C. crenatum, as a result of the NADH/NAD+ ratio.81 16128



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An increase in ATP is reported to enhance the metabolic flux toward succinate production in E. coli.93,94 Genome-scale thermodynamics-based flux balance analysis shows that overexpression of ATP-forming phosphoenolpyruvate carboxykinase (PEPCK) could result in an increase in biomass and succinate flux. Higher growth and xylose utilization were also observed in E. coli,105 showing that the effect of ATP concentration was stimulating growth and enhancing succinate production in E. coli. Another way to decrease the ORP value during fermentation is to supply a more reductive carbon source. This was proven by Li et al., who used three different oxidation-level carbon sources as the feed for succinate fermentation by A. succinogenes.106 Sorbitol, having the oxidation of (−1), glucose (0), and gluconate (+1) were used for the fermentation of A. succinogenes. The results showed that the lower oxidation-state carbon source gave better succinate yield; sorbitol had the highest succinate yield followed by glucose and then gluconate.106 This finding was supported by van der Werf et al., who demonstrated that the usage of highly reduced carbon sources (e.g., D-mannitol, D-sorbitol, D-arabitol) produce higher succinate in A. succinogenes.89 Similar phenomena were shown in E. coli107 and in C. crenatum.81 Different availability of NADH and ORP levels can be manipulated by the usage of carbon sources with different oxidation states. Another phenomenon driven by the redox process is the effect of different alkaline neutralizers on the succinate yield. Studies have shown that magnesium carbonate promotes the highest yield of succinate compared to other alkaline neutralizers, such as NaHCO3, in the fermentation of A. succinogenes.19 This is another phenomenon supporting the effect of the redox process in succinate production. Although sodium is a stronger reducing agent than magnesium, hydrogen has much lower reductivity that will pull down the total reducing power of the compound NaHCO3. This might be the reason for MgCO3 being a better alkaline neutralizer in succinate fermentation medium, even though NaHCO3 has a hydrogen ion, which is required in succinate production. 3.3. Effect of CO2 on Metabolic Flux Shunt toward Succinate Production. The presence of CO2 has been reported to induce succinate productivity in E. coli,95−100 A. succinogenes,89,90,92−94,111 M. succiniciproducens,91,101 K. pneumoniae,102 and A. succiniciproducens,111 as shown in Table 6. CO2 is needed to enhance the flux toward the production of succinic acid. CO2 is fixed into (C3) phosphoenolpyruvate (PEP), (C4) oxaloacetate (OAA) or malate in the anaplerotic reaction pathways, which are critical for succinic acid production. Thus, CO2 has been reported to have positive effect on succinate productivity.81 Recent study has shown that, in addition to PEP, OAA and malate also serve as the branch between succinate-producing C4 and byproduct-producing C3 pathways in A. succinogenes.31 The reason for this flux is to compensate the energy deficiency within the cells. The presence of CO2 and a strong reducing agent, such as H2, will help to balance these fluxes. This phenomenon allows the succinate fermentation to have a perfect combination with the chemical plants that have CO2 as a byproduct, for example, (i) bioethanol98 and (ii) biohydrogen production plants. i. Correlation of Succinate Fermentation with a Bioethanol Production Plant. The effect of CO2 on succinate fermentation allows the succinic acid production to coexist with a bioethanol production plant, bringing mutual benefits.

Table 6. Phenomena Affecting the Flux of Succinate Fermentation phenomena lower ORP level triggers higher flux toward succinate production.

presence of O2 lowers succinate production presence of reducing agent such as H2 enhances the metabolic flux toward increased succinate production

bacteria Corynebacterium crenatum E. coli A. succinogenes Clostridium thermosuccinogenes E. coli A. succiniciproducens A. succinogenes

M. succiniciproducens presence of CO2 in the fermentation broth induces the flux toward the C4 pathway, producing more succinate

A. succinogenes

A. succiniciproducens E. coli

M. succiniciproducens

more ATP in the medium promotes succinate production higher reductivity of carbon source enhances the flux toward succinate production

Klebsiella pneumoniae E. coli

A. succinogenes C. crenatum E. coli

ref 81 82 83 31 84 85 86 87 88 89 90 31 87 91 89 92 93 90 94 86 95 96 97 98 99 100 101 91 102 103 104 105 89 106 81 107

A higher NADH/NAD+ ratio is a sign of a lower intracellular ORP value, stimulating the microbes for higher succinate production. This phenomena has been reported in several succinate-producing microbes including A. succinogenes,31 E. coli,82,83 C. thermosuccinogenes,84 and C. crenatum81 as shown in Table 6. The presence of molecular oxygen lowers succinate production in E. coli,85 because O2 increases the ORP value, thus inhibiting the metabolic flux toward succinate. Most fermentation on succinate is carried out under anaerobic condition to eliminate the presence of O2 and to maintain the fermentation broth at a low ORP value. Strong reducing agents, such as H2, lower the ORP value in the fermentation broth. The presence of H2 has been reported to have a high impact on the absorption of CO2 into pyruvate for succinate production. Succinate-producing bacteria such as A. succinogenes,88−90 A. succiniciproducens,87,111 and M. succiniciproducens87,91 are reported to have enhanced succinic acid yields with an external supply of H2. 16129



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carbon source (e.g., glucose) by fixing carbon dioxide into pyruvate. The effect of CO2 in increasing succinate yield is because it is another substrate/carbon source in the formation of succinate.

Succinate fermentation using E. coli is reported to work well when coupled with ethanol fermentation, in which the emitted CO2 from bioethanol production is absorbed by succinate fermentation using E. coli.98 However, most of the studies on bioreactors show low utilization of CO2 and most of the sparged CO2 was released into the environment. A feasible method suggested by Wu et al. to overcome this problem was to continuously withdrawing the CO2 gas from the headspace of the bioreactor to purge back into the fermentation broth by a self-induction agitator.98 This could promote CO2 to transfer from the gas phase to the liquid medium and thus reducing CO2 emission from the bioreactor. A perfect gas dispersion could be obtained.112−114 ii. Perfect Combination of Succinate Fermentation and Biohydrogen Production. A. succinogenes producing less formate, acetate, and ethanol but higher succinate in response to high CO 2 and H 2 concentrations. High NaHCO 3 concentrations decrease the flux shunted by the C4-to-C3 formate-, acetate-, and ethanol-producing pathway.100 Therefore, A. succinogenes fermentation is perfect for purifying biohydrogen in a biohydrogen production plant. This is because the succinate yield in A. succinogenes will increase with increasing amounts of both CO2 and the reductant (e.g., H2).99 A combination of a 0.8 mmol of H2 and a high (100 mmol compared to 25 mmol) CO2 concentration increases the metabolic flux toward higher succinate and reduces fluxes of CO2-producing reactions, resulting in a 2.7 times higher CO2 consumption rate.100 This approach of bubbling biogas from biomass, which is concentrated in H2 and CO2 through the bioreactor fermenting A. succinogenes, allows the absorption of CO2, which is fed into PEP to form OAA that follows the C4 pathway, producing succinic acid. It purifies the biogas by increasing the H2 purity, reducing the CO2 concentration and, at the same time, increasing the efficiency of succinic acid fermentation. 3.4. Effect of Energy Balance on Succinate Productivity. The metabolic flux shunt of succinic acid is governed by a fundamental thermodynamic principle; the energy balance. The redox-potential difference between two chemicals implies the energy potential when they come into contact. Energy balance is the reason behind these fluxes in succinate fermentation. When a high energy-level chemical compound is to be formed from a lower energy-level chemical compound, an external driving energy is required. This phenomenon is observed in photosynthesis where high-energy glucose is formed from low-energy molecules, CO2 and H2O, with the capturing of light energy from the Sun. The light energy actually pushes CO2 and H2O into the more reduced C6H12O6 and more oxidized O2 molecules, as the energy is stored in a redox level between the two compounds. Another simple example is how electrolysis can generate highly reduced H2 and highly oxidized O2 from H2O with an external supply of electrical energy. All these chemical transformation are related to a basic thermodynamic principle, the energy balance, as does the metabolic flux in succinate fermentation. Succinate is a higher energy (more reduced) metabolite compared to formate, acetate and ethanol. In other words, succinate generates more energy when it is oxidized compared to formate, acetate or ethanol. The presence of energy-rich molecules such as H2, ATP, NADH, and NADPH drive the fixation of CO2 into pyruvate, generating high-energy succinate. If this energy is supplied externally by bubbling H2 through succinate fermentation broth, it will reduce the burden of the main

4. CONCLUSION Biosuccinic acid transcends petrochemical succinic acid in terms of economic, environmental and sustainability factors. The production of succinic acid by means of a biological approach as an alternative to the petrochemical method has already been exploited. There are 12 commercial biosuccinic acid production plants (Table 1) throughout the world, which are either operating or in the commissioning state. The major microbes involved in succinate production are A. succinogenes, A. succiniciproducens, M. succiniciproducens, and E. coli. Sugar from biomass has been shown to be able to replace pure commercial sugars as substrates in the fermentation of succinic acid, which could reduce the cost of raw materials. Lignocellulosic crop wastes (corn straw, cotton straw, rice straw and wheat straw), in this case, represents the best and most promising choice as a carbon source. Crop stalk wastes excel in terms of its cheap cost (mostly below $50 tonne−1 except for wheat straw), extremely high availability (∼1 billion metric tonnes for both corn straw and rice straw) and competitive yield. Glycerol on the other hand, appears to have comparable potential as a commercial biosuccinic acid feedstock for succinate fermentation due to its high global availability of ∼600 million metric tonnes per annum and its high conversion up to 1.33 g succinate per gram of glycerol. However, due to the cost of crude glycerol (75%) has shot up to $220 tonne−1, putting this source to be less attractive than crop straw wastes. The yield, which is one of the three parameters considered in the present analysis of biomass, can be significantly enhanced by manipulating the factors governing it. The effect of the fermentation redox balance on the succinate flux allows for the manipulation of fermentation to increase the succinate yield. A more reducing fermentation broth (with a lower ORP value) and a higher concentration of CO2 drive the metabolic flux toward the production of more reduced metabolites such as succinate.

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ASSOCIATED CONTENT

S Supporting Information *

Several calculations made in the manuscript which might interest some readers. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: +603-8921 6427. Fax: +603-8911 8345. E-mail: [email protected]. Funding

This research is funded by the Ministry of Higher Education, Malaysia, under LRGS/2013/UKM-UKM/PT/01 on the project entitled “Biochemical Platform for Conversion of Diversified Lignocellulosic Biomass to Priceless Precursor and Biobased Fine Chemicals”. Notes

The authors declare no competing financial interest. 16130



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ACKNOWLEDGMENTS The authors wish to thank the Ministry of Higher Education, Malaysia, for financial support of this work.

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ABBREVIATION AFEX = ammonia fiber explosion ATP = adenosine triphosphate BASF = chemical company BioAmber-ARD = chemical company CAGR = compound annual growth rate CSL = corn steep liquor C3 = three carbon metabolic pathway which will leads to byproduct production C4 = four carbon metabolic pathway which will leads to succinic acid production DSM = chemical company DNP = Diversified Natural Products Inc. (chemical company) GDP = gross domestic product GFFH = gluten free flour hydrolysate GHG = greenhouse gas H1 = first half of the year H2 = second half of the year JV = joint venture kg = kilogram LHW = liquid hot water Mitsui = chemical company MPOC = Malaysia Palm Oil Council Mt = metric tonne Myriant = chemical company Myriant-China National BlueStar = chemical company NA = Not available NADH = nicotinamide adenine dinucleotide NADPH = nicotinamide adenine dinucleotide phosphate OAA = oxaloacetate OPF = oil palm fronds ORP = oxidation−reduction potential PEP = phosphoenolpyruvate PEPCK = phosphoenolpyruvate carboxykinase Purac = chemical company PTT MCC Biochem = chemical company Q1 = first quater of the year Q2 = second quarter of the year Reverdia = chemical company (joint venture between DSM and Rouquette) Sime Darby Plantation Sdn Bhd, Malaysia = plantation company SSF = simultaneous saccharification and fermentation TAPPI = Technical Association of Pulp and Paper Industry UNFCCC = United Nations framework convention on climate change WO = wet oxidation YCH = yeast cell hydrolysate $ = U.S. dollar

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