Polyhydroxyalkanoates Production From Low-cost Sustainable Raw ...

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Leics, LE12 5RD, UK; The Department of Chemical and Environmental ... polymers due to thier intrinsic biodegradability and biocompatibility, their high price has limited their application signifi- ... The development of copolymer production or.
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Current Chemical Biology, 2012, 6, 00-00

Polyhydroxyalkanoates Production From Low-cost Sustainable Raw Materials Chenyu Dua, Julia Sabirovab, Wim Soetaertb, Sze Ki Carol Lin*,c a

Division of Food Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough Leics, LE12 5RD, UK; The Department of Chemical and Environmental Engineering, Faculty of Engineering, University of Nottingham, University Park, Nottingham, NG7 2RD, UK; b Centre for Industrial Biotechnology and, Biocatalysis, Department of Biochemical and Microbial Technology, Faculty of Bioscience Engineering, Ghent University, Belgium; cSchool of Energy and Environment, The City University of Hong Kong, Hong Kong Abstract: The unnerving price of petroleum will push a major change from a petroleum based economy to a natural feedstock based economy. Production of polyhydroxyalkanoates (PHAs) using industrial and agriculture by-products can allow the use of low-cost feedstock to produce materials with specific monomer composition and therefore, with the appropriate physicochemical properties to be used in a broad range of applications. Depending on the monomer composition, PHAs properties can range from thermoplastic to elastomeric materials. Even though PHA has been described as useful polymers due to thier intrinsic biodegradability and biocompatibility, their high price has limited their application significantly. The raw material cost has been known to contribute significantly to the manufacturing cost of PHA. Therefore, much research has been carried out using renewable cheap raw materials to replace the expensive commercial medium, which should reduce the overall production cost. In this review, the production of PHAs using low-cost sustainable raw materials such as molasses, whey, lignocelluloses, fats and oils, glycerol and wastewater are described. Finally, the physicochemical properties of PHAs produced from various carbon sources are discussed.

Keywords: Fats and oil, glycerol, lignocellulosic raw materials, molasses, whey, polyhydroxyalkanoates, wastewater. 1. INTRODUCTION The increasing worldwide concern of oil shortage not only affects the energy industry, but also changes the chemical industry. For example, plastic has an annual production of 200 million tons and at present, it is predominately derived from petroleum [1]. With the depletion of crude oil resource, the manufacture of conventional plastics becomes increasingly expensive. As a result, there is an imminent need for using alternative, sustainable raw materials to replace fossil resources. One feasible approach is to produce biopolymers using starch, sugars, or cellulose to substitute conventional plastics. Besides derived from sustainable biomaterials, bioploymers are generally bio-degradable, making it an environmental benign process. Polyhydroxyalkanoates (PHAs) are among the top group of biopolymers that have been intensively investigated and commercialized. PHAs are a family of biodegradable polymers produced by a broad range of micro-organisms, including Ralstonia eutropha (formerly called Alcaligenes eutrophus, Wautersia eutropha, or Cupriavidus necator) Alcaligenes latus, Aeromonas hydrophila, Pseudomonas putida and recombinant Escherichia coli [2]. PHAs are usually accumulated as an intracellular energy reserve at nutrient starving conditions, but some bacteria such as Ralstonia eutropha *Address correspondence to this author at the School of Energy and Environment, 2/F Harbour View 2, 16 Science Park East Avenue, Hong Kong Science Park, Shatin, N.T., Hong Kong; Tel: (852) 3442-7497; Fax: (852) 2319-5927E-mail: [email protected] 2212-7968/12 $58.00+.00

and Alcaligenes latus could synthesis PHAs using nutrient non-limiting media [3]. PHAs family can be classified according to the chain length of the branching polymers. Shortchain-length PHAs (scl-PHAs) are composed of 3-5 carbon atoms, while medium-chain-length (mcl-PHAs) and longchain-length (lcl-PHAs) consists of 6-14 and over 14 carbon atoms, respectively [4, 5]. The most extensively studied member of the PHA family is poly(3-hydroxybutyrate) (PHB). It was in the mid 1920s, Lemoigne at the Pasteur Institute in Paris, firstly identified the presence of PHB in Bacillus megaterium [6]. PHB can be accumulated up to 80% of the cell dry weight from various carbon sources by Ralstonia eutropha [7] and near 90% in recombinant E. coli [8]. Biodegradability and biocompatibility are important characteristics of PHAs. PHAs can be degraded to carbon dioxide and water by a large variety of micro-organisms in nature [9]. Having the similar properties to the thermoplastics and bestowed with the biodegradability, materials made from PHAs are expected to replace the traditional petroleumbased plastics. The development of copolymer production or blending PHAs with other monomers has widened their applications. PHAs and their derivatives are now used in the field of agricultural, food and biomedical materials, which has been recently reviewed by Chen [10]. Imperial Chemical Industries (ICI) was the first to successfully commercialised poly(hydroxybutyrate-cohydroxybutyrate) (PHBV) with the trade name of “Biopol” in the 1980s [11]. Since then, several companies in China, © 2012 Bentham Science Publishers

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Current Chemical Biology, 2012, Vol. 6, No. 1

USA, Austria, Germany, Japan, Brazil and Italy produced PHB or other PHAs at pilot to commercial scales [10]. However, due to the relatively high production cost in comparison to petroleum-based plastics and the lack of high-end market, several companies stopped or sold PHA manufacturing plants, including ICI [10]. It is generally considered that the high raw material cost, together with high recovery cost and low PHA yield contribute significantly to the high price of PHA [12, 13, 14, 15]. Among which, the raw material cost could count for 30-40% if expensive carbon source such as starch was used [16]. Recent research focus therefore has been concentrated on the utilisation of inexpensive renewable raw material for PHA production. In this paper, the use of industrial by-products such as molasses, whey, lignocellulosic raw materials, fats and oils, glycerols and wastewater for the production of PHAs are

reviewed. Fig. (1) shows the low-cost feedstocks discussed in this review paper and its applications. Moreover, the PHAs monomer composition and PHAs physicochemical properties of biopolymers derived from various low-cost feedstock are discussed. 2. PHAs PRODUCTION FROM MOLASSES Molasses is a sugar-rich co-product stream generated in sugar manufacturing industries [17]. In 2004, the global sugar production generated was about 39 million tons of cane molasses and 12 million tons of beet molasses (www.melasse.de/originsofmolasses.html). Molasses have been widely used as a carbon source in industrial scale fermentations due to its relatively low price and its abundance [18]. In 1992, Page firstly reported the production of PHB by Azotobacter vinelandii UWD using sugar beet molasses [19].

F eedstocks

Applications

Lam inates Whey

F ilm s Diaper backsheet

Lignocellulosic raw m aterials

Hydrolysis Biodegradable or com postable personal hygiene articles

M olasses PHA production by M icrobial F erm entation

Latex

Paper - coating applications

Glycerol Bottles F ats , vegetable oils and waste cooking oils

M oulded products Consum er packaging item s

T ransesterification

Cosm etic containers Pens

Wastewater

15

Volatile fatty acid ferm entation

Golf tees

Nonwoven fabrics F ibers Hot -m elt adhesives

Pressure - sensitive adhesive form ulations

Diary cream substitutes F oods F lavor delivery agents in foods T oner and developer com positions

Ion - conducting polym ers

Biodegradable solvents

Fig. (1). Feedstocks and applications of microbial PHA productions by different processing technologies.

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A PHB concentration of 19 to 22 g/L at a productivity of 0.50 to 0.55 g/L.h was achieved. Chen and Page (1997) further improved the PHB production using a two-stage fermentation strategy by Azotobacter vinelandii UWD [20]. In the first stage, a high aeration rate was used to promote cell growth. In the second stage, the aeration rate was lowered to promote PHB production. The resultant PHB concentration of 36 g/L at a productivity of over 1 g/L.h was reported. Albuquerque et al. (2007) reported an interesting work of developing a three-step fermentation strategy to produce PHAs from cane molasses [17]. In the first step, the molasses were fermented to organic acids. Then, the next step triggered PHA accumulation and finally, PHAs were produced in batch fermentation using the fermented molasses and the PHA-accumulating cultures. Pisco et al. (2009) and Bengtsson et al. (2010) further investigated PHAs synthesis from fermented molasses using a consortium of microorganism [21, 22]. The PHA yields were in the range of 0.47 to 0.66 C-mol PHA per C-mol of total carbon substrate. These reports indicated that the PHA could be produced from fermented molasses, or wastewater that contains similar components as fermented molasses such as volatile fatty acids (VFAs). Wu et al. (2001) isolated Bacillus sp. JMa5 from molasses contaminated soil for PHB production using sugar cane molasses [23]. This strain grew at elevated temperatures up to 47°C and was osmotolerant. In a fed-batch fermentation, around 70 g/L CDW was produced containing 25 to 35% PHB. Chaijamrus & Udpuay (2008) investigated PHB production using another Bacillus strain, B. megaterium ATCC 6748 [4]. A maximum of 43% PHB on cell dry weight was obtained with a feed containing 4% sugar cane molasses and 4% corn steep liquor (CSL) as carbon and nitrogen sources, respectively. However, the cell dry weight was only 5 g/L. In other study using B. megaterium BA-019, a high productivity of 1.27 g/L.h was achieved, with 42% of the 72.6 g CDW/L was PHB [25]. Sugar cane molasses and urea were used as cheap carbon and nitrogen sources, respectively. Besides sugar beet molasses and sugar cane molasses, PHAs accumulation was also reported in media derived from soy molasses with high sucrose content. Solaiman et al. (2006a) attempted to produce mcl-PHA from soy molasses using Pseudomonas corrugate, 1.5-3.6 g CDW/L was obtained which contains 5-17% of PHA [26]. The most abundant monomers in PHA production were 3-hydroxyldodecanoate, 3-hydroxyl-octanoate and 3hydroxytetradecenoate. Conversion of these unusual saccharides in soy molasses into PHA seems to be better performed by gram-positive bacteria, such as Bacillus. Sp CL1 [27]. PHAs accumulated up to 90% of CDW in Bacillus. Sp CL1. Law et al. (2001) also approved that two isolated Bacillus strains, HF-1 and HF-2, synthesized PHB from hydrolysed soy and malt wastes [28]. These results were compared with studies using various molasses in Table 1. 3. PHAs PRODUCTION FROM WHEY AND WHEY HYDROLYSATES Whey is the main by-product in the manufacture of cheese. It is estimated that the annual whey formation exceed 40 million tons in the European Union [29]. The main com-

Du et al.

ponent of whey is lactose, which exceeds 70% of total dry matter, indicating a good cheap carbon and energy source for the fermentation industry. The application of whey lactose for the PHAs production has been widely explored, as shown in Table 1. Lee et al. (1997) have constructed different recombinant Escherichia coli strains expressing Cupriavidus necator phaC2 gene (also known as Ralstonia eutropha) for the production of PHB from whey [30]. The best isolate grew up to 5.2 g CDW/L, 81% of which was PHB. Lee and his co-workers expressed Ralstonia eutropha PHA biosynthesis genes and E. coli fts Z gene, in which a recombinant E. coli GCSC 6576 was constructed [31]. In a fermentation using whey powder, 109 g CDW/L with 50 g PHB/L in 47 h were obtained. By using a concentrated whey solution containing 210 g lactose/L, 87 g CDW/L with 69 g PHB/L was achieved. In this case, the productivity was as high as 1.4 g/L.h. However, due to low concentration of lactose in the feeding solution, culture broth needed to be removed when the volume became too high. Ahn et al. (2000) used a similar recombinant E. coli strain CGSC 4401 and a whey solution containing 280 g lactose/L, achieved 119.5 g CDW/L with 96.2 g PHB/L in 37.5 hours [32]. In order to overcome the reactor volume problem, Ahn et al. (2001) introduced a cell recycle membrane system [33]. Using this system with the same strain and a lactose concentration of 280 g/L, a cell concentration of 194 g/L with 168 g PHB/L was obtained in 36.5 hours. Park et al. (2002) used the same system in a 30 L fermentor and a 300 L fermentor, in which the resultant biomass concentration were 51 g CDW/L with 70% PHB and 30 g CDW/L with 67% PHB, respectively [34]. Another strategy to achieve a high intracellular PHB concentration in recombinant E. coli was to control the oxygen supply. Kim (2000) demonstrated that an increase of the maximum agitation speed to 500 rpm while keeping a constant air aeration rate resulted in 70–80% PHB in cells without removing culture broth during fermentation [35]. Besides recombinant E. coli, the potential of PHA synthesis from whey has also been exploited using various common PHA producing bacteria, such as Ralstonia eutropha DSM545 [36], Pseudomonas hydrogenovora [29], Thermus thermophilus HB8 [37] and wild strains, such as Methylobacterium sp. ZP24 [38, 39], Hydrogenophaga pseudoflava DSM1034 [40]. However, the PHAs concentrations were relatively low (less than 10 g/L), which was significantly lower than that achieved in recombinant E. coli fermentations (as shown in Table 1). 4. PHAs PRODUCTION FROM LIGNOCELLULOSIC RAW MATERIALS Due to the significant increase of food price in recent years, the usage of food products in bulk biochemicals and biofuels production received increasing criticism. Therefore, the industrial biotechnology development has turned its focus on to the utilisation of non-food biomass, such as lignocellulosic raw materials [41]. Lignocellulosic is generally considered as the most abundant renewable carbon source. Approximate 80 billion tons of woody biomass is generated annually worldwide, contributing to a total annual production of 180 billion tons plant matter [42]. Lignocellulosic biomass consists of 30-50% cellulose, 20-50% hemicellulose and 15-35% lignin. The conversion of glucose, the only

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monomer of cellulose has been well studied. Although it was reported certain bacteria, for example Saccharophagus degradans ATCC 43961, were able to utilize directly cellulose for PHA production [43], the main focus of utilization of lignocellulosic biomass has been on the conversion of the monomer sugars from hemicelluloses, such as xylose, arabinose, mannose, galactose and rhamnose. As many other research using lignocellulosic raw materials in fermentations, one of the main drawbacks in lignocellulose to PHAs is the recalcitrance nature of lignocellulose. Therefore, pretreatment/hydrolysis steps are required to generate the sugar feedstocks used to produce the bioplastics.

Besides utilization of lignocellulosic hydrolysate, PHAs producing strains were also exploited for the removal of inhibitory compounds [55]. By using a large inoculum size, an adapted tolerant strain of Ralstonia eutropha, could grow in diluted bagasse hydrolysates. The strain efficiently removed formic acid, acetic acid, furfural and acid soluble lignin (phenolic compounds) from the bagasse hydrolysate whilst producing PHAs. The polyesters produced were mainly PHB (57% on CDW), but also included PHBV. Since xylose, arabinose and oligosaccharides were not utilised, the treated hydrolysates could be used in the production of other chemicals and biofuels.

In an earlier report in 1990s, Bertrand et al. (1990) showed that Pseudomonas pseudoava was able to grow on the hemicellulosic fraction of poplar wood until 30% of hydrolysate concentration [44]. This strain produced 17 to 22% PHB on the major sugars in the hydrolysate, namely glucose, xylose or arabinose. Ramsay et al. (1995) and Young et al. (1994) reported the ability of Burkholderia cepacia ATCC 17759 to produce 1.6-3.7 g PHB/L from xylose [45, 46]. Production of PHBV from fructose and glucose can also be achieved using propionic acid as a co-substrate [47, 48]. More recently, this strain was used by Keenan et al. (2006a and 2006b) to produce 1.3 - 4.2 g PHBV/L using xylose with levulinic acid as a precursor for HV monomers. When detoxified hemicellulosic hydrolysates from aspen and maple were used, PHBV concentration, content and mol% of 3HV were 2.0 g/L, 40 w/w% and 16-52 mol%, respectively [49, 50].

5. PHAs PRODUCTION FROM FATS, VEGETABLE OILS AND WASTE COOKING OILS

In order to obtain xylose utilizing strains for the PHAs production, Silva et al. (2004) isolated and screened 55 bacteria from soil [51]. Two strains, Burkholderia cepacia IPT 048 and B. sacchari IPT 101 showed good PHB synthesis abilities. In the high cell density cultures on xylose and glucose with phosphorous limitation, 60 g CDW/L containing 60% PHB was produced by both strains with a similar productivity of 0.47 g/L.h. Li et al. (2007) constructed an E. coli phosphotransferase system (PTS) mutant for PHA production on glucose and xylose [52]. The PTS mutation was able to overcome carbon catabolite repression from glucose. When Ralstronia eutropha phaCRe and phaABRe genes were inserted, the new strain produced scl-PHA on the substrate containing mixture of glucose and xylose. With Pseudomonas aeruginosa phaC1 gene inserted into the same parent strain, the recombinant E. coli produced mcl-PHA on this carbon source. Recently, Van-Thuoc et al. (2008) demonstrated that Halomonas boliviensis LC1 could produce PHB on enzymatically hydrolysed wheat bran [53]. A PHB content of 30% and 9 g CDW/L was attained. An increase of PHB production up to 50 w/w % and 4 g PHB/L was achieved by adding butyric acid and sodium acetate, and by decreasing the reducing sugars concentration. Huang et al. (2006) investigated PHA biosynthesis from extruded rice bran and corn starch [54]. Haloferax mediterranei, which could not utilize rice bran and corn starch directly, was able to access the carbon source after the extrusion for the PHA production. This indicated the potential of applying extrusion instead of enzymatic hydrolysis to break down the lignocellulosic raw materials.

Based on the earlier exploitations on the PHA production from long-chain fatty acids [58, 59, 60], Shimamura et al. (1994) firstly demonstrated that Aeromonas caviae could biosynthesize PHAs directly from TAG with hydrolysis pretreatment [61]. Cromwick et al. (1996) showed Pseudomonas resinovorans accumulated PHA to 15% of its cell dry weights from tallow [62]. Ashby and Foglia (1998) further investigated PHAs production by Pseudomonas resinovorans using a whole range of TAGs, such as lard, butter oil, olive oil, coconut oil, and soybean oil for the production of mcl-PHA [57]. In these studies, low PHA concentrations of around 1.2 to 1.9 g/L were reported, with monomers of 4 to 14 carbon atoms. Also, it was observed that the type of monomers had a strong relationship with the type of substrate. When coconut oil containing high levels of saturated fat was used, saturated PHA monomers were produced. Whereas soybean oil containing high levels of unsaturated fat was used, unsaturated PHA monomers were synthesized. Therefore, much research has been carried out on the PHAs production using palm oil [63], olive oil [64], corn oil [65], coconut oil [66], soy bean oil [67, 68], other vegetable oils and animal fats. Both wild strains and genetic modified strains were used and their results are summarized in Table 1. In most of these reports, both the PHAs concentration and CDW are low, usually no more than 10 g/L. However, the CDW could achieve as high as 138 g/L containing 71-74% (w/w) P(3HB-co-3HHx) in the case using soybean oil as the substrate [68].

Triacylglycerides (TAG) and its derived fatty acids attracted great interest for the fermentative PHAs production due to their renewability and their relatively low price in the 1990s. In comparison to carbohydrates, fatty acids deliver more energy per mole when they are converted to PHA [56]. Until recently, the use of TAG as a feedstock for production of PHA is a big challenge, mainly because of its hydrophobic nature and inherent difficulties in the fermentation process. However, it is relatively more desirable to utilize triacylglycerols directly as a carbon source in fermentation, in order to avoid the saponication step involved in the fatty acids production. Moreover, TAGs could be a valuable alternative feedstock for the production of mcl-PHAs and lclPHAs, as the constituents of PHA under these conditions would be directly derived from fatty acids of TAGs [56, 57].

In recent years, the price of edible oils increased significantly due to increasing demand for both cooking oil and

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biodiesel production [69]. As a result, the usage of edible oils for PHAs production is no longer considered as a costeffective way. Therefore, research focus turned to use only non-edible oils [70, 71, 72] and waste/spent cooking oils [73, 74, 75, 76]. The PHAs generated usually have a relative wide range of C4 to C16 monomers. These results were compared in Table 1 with those using pure edible oils. It is clearly showed that the highest PHAs obtained from waste oils was significantly lower than what achieved using soybean oils, which could be due to the presence of impurities in the waste oils. 6. PHAs PRODUCTION FROM GLYCEROL Glycerol is the main by-production for the biodiesel production with about 10% (v/v) of the volume of biodiesel. In 2009, the biodiesel production in Europe exceeded 10 billion litres, resulting in about 1 billion litres of glycerol was coproduced. Due to this large production, the world market price of glycerol has dropped spectacularly, which makes this side-stream an interesting source for microbial production of PHAs [77]. In the early nineties, Pseudomonas putida KT2442 was shown to produce mcl-PHA from glycerol [56]. The produced polymer had characteristics which were similar to the polymer produced by the same strain from glucose or fructose as a carbon source [78]. Bormann and Roth (1999) demonstrated the production of PHB from glycerol and casein hydrolysates as carbon and nitrogen sources, respectively [79]. The two microorganisms separately used in fermentative PHB production were Methylobacterium rhodesianum and C. necator, which produced up to 50% and 65% PHB in 45 h, respectively. The PHB yield on glycerol was only 17%. Ashby et al. 2005 investigated PHA synthesis by Pseudomonas oleovorans NRRL B-14682 and Pseudomonas corrugata 388 [80]. Although these two strains accumulated PHAs intracellularly, the attempts to increase PHA yields by increasing glycerol concentrations have not been successful [80]. Sujatha and Shenbagarathai (2006) constructed a recombinant E. coli strain with the phaC1 gene from Pseudomonas sp. LDC-5 [81]. This recombinant strain produced 3.4 g PHAs/L on glycerol and fish peptone derived medium. Recently, De Almeida et al. (2007) evaluated the effect of PhaP, a phasin, on cell growth and PHB biosynthesis using glycerol as a carbon source [82]. With PhaP, the recombinant E. coli growth was enhanced by a factor of 1.9, while PHB production increased 2.6 times. The maximum production of 7.9 g PHB/L was obtained in 48 h in a batch culture. Apart from pure glycerol, crude glycerol has also been studied for PHAs production. Ashby et al. (2004) used crude glycerol, derived from a soy-based biodiesel production site, for the microbial production of PHA [83]. It was showed that P. oleovorans NRRL B-14682 and P. corrugata 388 could accumulate mcl-PHA from this carbon source in shake flasks. In this case, the Mn value decreased as the initial waste glycerol concentration increased with P. oleovorans, but this effect was not noticed with the P. corrugata strain. Koller et al. (2005) tried to reduce further the process cost, by using crude glycerol as the carbon source, combined with meat and bone meals as a nitrogen source [84]. In this way, 5.9 g PHAs/L was obtained. Interestingly, the investigators

Du et al.

managed to produce the PHBV copolymer, without adding any precursor molecule in the feed. The usability of the different crude glycerol streams was evaluated by Mothes et al. (2007) [85]. They also examined the influence of the salt concentration in the glycerol on the PHB production by C. necator JMP134 and Paracoccus denitrificans [86]. It seemed that high NaCl contents (5%) reduced the PHB content dramatically with 48%. However, the K2SO4 contamination had no pronounced effect, indicating that the K2SO4 contaminated waste glycerol streams could be a more suitable stream for the PHA production. Promising results were published by Cavalheiro et al. (2009), in which C. necator DSM 545 was cultivated up to 68.8 g CDW/L on waste glycerol [86]. The cells contained 38% PHB, with a productivity of 0.84 g/L.h. When the accumulation was triggered earlier, by nitrogen limitation, the productivity on waste glycerol could be increased to 1.1 g/L.h with 50% PHB in the dry cells. 7. PHAs PRODUCTION FROM WASTEWATER PHAs production from wastewater provides another alternative approach to reduce the cost of raw materials. Various organic wastewaters, such as municipal wastewater [87, 88, 89], biodiesel wastewater [90], food processing waste effluent [91, 92], brewery waste effluent [93], paper mill wastewater [94] and kraft mill wastewater [95] have been tested for PHAs biosynthesis. In most of cases, the organic carbon sources are converted into volatile fatty acid in aerobic activated sludge in the first step, and then converted into the PHAs by mixing cell cultures in the second step. Although the final PHAs concentrations are still low at the current investigated conditions, PHAs could accumulate to around or even over 50% of the cell dry weight in some cases [93, 94]. In PHAs production using wastewater as starting materials, microorganism consortium is more preferable than pure cell culture due to economic concerns [10]. 8. MATERIAL PROPERTIEs OF PHAS PRODUCED FROM DIFFERENT CARBON SOURCES Material properties of PHAs are very important criteria to determine the type of applications of a particular type of polymer. For example, the mcl-PHAs have elastomeric behaviour with an elongation at break of about 300% [109]. This together with other properties such as high hydrophilicity, mcl-PHAs could be used as a scaffold material in tissue engineering [110, 111]. The physical and thermal properties of PHAs can be regulated by varying their molecular structures and copolymer compositions. In this respect, the monomer composition of PHAs is the determining factor to control its properties and consequently affects its fields of application. It is well known that the compositions of PHAs are highly influenced by the intrinsic nature of the substrate used for its biosynthesis as well as the specificity of PHA synthase presented in the host microorganism [112]. In the production of PHA, several of the monomer precursors used for PHA accumulation can contain unsaturated monomers and a wide variety of functionalized groups in the side chain such as phenoxy, epoxy, hydroxyl, halogens and methylester groups [110]. These groups allow further chemical modifications, leading

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Table 1.

Current Chemical Biology, 2012, Vol. 6, No. 1

PHAs fermentations using various cheap substrates. Carbon sources

Strains

PHAs (g/L)

Cell Density (g/L)

References

Molasses Sugar beet molasses

Sugar cane molasses

Azotobacter vinelandii UWD

PHB, 19-22

N/A

[19]

Azotobacter vinelandii UWD

PHB, 36

N/A

[20]

Bacillus sp. Jma5

PHB, 25-35% dw

30 (batch)

[23]

70 (fed batch) Molasses

Bacterial consortium

PHAs, VFA

0.37-0.5

Cmol/Cmol

2-3

[17]

Bacterial consortium

PHAs, VFA

0.47-0.66

Cmol/Cmol

3.6-5.1

[21, 22]

Bacillus megaterium ATCC 6748

PHB, 2.2 (43% CDW)

5.0

[24]

Bacillus megaterium BA-019

PHB, 30.5 (42% CDW)

72.6

[25]

Pseudomonas corrugata.

mcl-PHA 5-17%

1.5-3.6

[26]

Bacillus sp. CL1

PHAs, 90%

3.42

[27]

Hydrolyzed soy and malt

Bacillus sp. HF-1, HF-2

PHAs, 18.42

32

[28]

Hydrolyzed whey

Ralstonia eutropha DSM545

PHBV, 2.25

4.5

[36]

Pseudomonas hydrogenovora

PHBV, 1.44

1.84

[29]

Recombinant E. coli

PHB, 9.0

58.2 (fed-batch)

[96]

Recombinant E. coli

PHB, 5.2

6.4

[30]

Thermus thermophiles HB8

PHA, 0.51

2.09

[38]

Hydrogenophaga pseudoflava

PHA, N/A

N/A

[41]

Methylobacterium sp. ZP24

PHA, 2.6-5.9

5.1-9.9

[39]

Methylobacterium sp. ZP24

PHB, 6.12

N/A

[40]

E. coli GCSC 6576

PHB, 109

87

[31]

E. coli GCSC 4401

PHB, 96.2

119.5

[32]

Hemicelllosic fraction of poplar wood

Pseudomonas pseudoava

PHB, 6.57

1.50

[44]

Xylose; xylose with propionic acid

Burkholderia cepacia ATCC 17759

PHB; PHBV, 1.6-3.7

2.6

[45, 46]

Xylose with levulinic acid

Burkholderia cepacia ATCC 17759

PHBV, 1.3-4.2

Max. 9.5

[49, 50]

Hemicellulosic hydrolysates

Burkholderia cepacia ATCC 17759

PHB, 2.0

Max. 5.1

[49, 50]

Xylose, glucose from sugar cane bagasse

Burkholderia cepacia IPT 048 and B. sacchari IPT 101

PHB, 34.8

60

[51]

Xylose and glucose

E. coli PTS mutant

PHA, 0.476

2.3

[52]

Wheat bran hydrolysate

Halomonas boliviensis LC1

PHB, 4

9

[53]

Sugar cane molasses

Soy molasses

Whey and whey hydrolysates

Whey

Lignocellulosic raw materials

19

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Du et al. Table 1. Contd….

Carbon sources

Strains

PHAs (g/L)

Cellulose, in tequila bagasse

Saccharophagus degradans ATCC 43961

PHA, 1.5

Formic acid, acetic acid, furfural and acid soluble lignin

Ralstonia eutropha

PHB, 6.1-6.8

Cell Density (g/L)

References

2.55

[43]

10.7-11.1

[55]

N/A

[57, 62]

1.6-2.8

[57]

Fats, vegetable oils and waste cooking oils Unsaponifed olive oil

Aeromonas caviae

mcl-PHA, max. 96 wt%

Lard, butter oil, olive oil, coconut oil, soybean oil

Pseudomonas aeruginosa and Pseudomonas resinovorans

mcl-PHA, 2.1

Olive oil, corn oil and palm oil

C. necator (also known as R. eutropha, A. eutropha)

PHB, 3.4

4.3

[66, 98]

Olive oil, corn oil and palm oil

P. putida; C. necator.

PHA, 1.6

3.0

[65]

Castor seed oil, coconut oil, mustard oil, cottonseed oil, groundnut oil, olive oil, and sesame oil

Comamonas testosteroni

The polymer contained HA units with 6 to 14 carbon atoms, 87.5% CDW

N/A

[64, 66]

Lard and coconut oil

Pseudomonas putida

PHA, 0.9-1.6

2-4 g/l

[100]

Coconut oil and tallow

Pseudomonas saccharophila

mcl-PHA, 0.8

N/A

[101]

Palm kernel oil, palm olein, crude palm oil and palm acid oil

C. necator

PHA, 3.3

8.3

[102]

Palm kernel oil

C. necator

P(3HB-co-3HV-co-3HHx); 6.79

7.9

[103]

C. necator

PHA, 2.5

7.5

[104]

Pseudomonas stutzeri

PHA, 1.4

2.7

[67]

C. necator H16

PHA,102

Max. 138

[68]

C. necator mutants

PHA, 1

Max. 2.2

[105]

Jatropha

Marine bacteria, SM-P-3M

PHA, 0.306

0.404

[70, 71, 72]

Linseed oil

Pseudomonas aeruginosa

PHA, 1.8, 50.2% CDW

3.6

[107]

Brassica carinata oil

Pseudomonas aeruginosa

PHA, 5%

1.0

[97]

Waste cooking oil

Pseudomonas aeruginosa

PHA, 2.3

4.5

[73]

Pseudomonas aeruginosa

PHA, 5.4

19.0

[74]

Pseudomonas aeruginosa

PHA, 3.43

Max. 6.8

[75]

Spent palm oil

Cupriavidus necator

P(3HB-co-4HB), 4.4

5.5

[76]

Waste vegetable oil

Pseudomonas sp. strain DR2

PHA, 23.5% CDW

N/A

[99]

Alpechin, (wastewater from olive oil mill)

Azotobacter chroococcum H23

PHA, 70% CDW

N/A

[106]

Wastewater

Enterobacter aerogenes 12Bi

PHB, 5.2

6.2

[108]

Soybean oil

and recombinant strains

Wastewater

N/A = Not available.

Crucifers: Beneficial and Adverse Effects

Current Chemical Biology, 2012, Vol. 6, No. 1

the biomass yield, but also led to the production of PHAs containing aryl groups.

to novel materials with different properties. Moreover, the side chain length and also the functional group attached to it will have a significant influence in the properties of the polymer such as glass transition temperature, crystallinity and melting point. PHB and PHBV are the most common polyesters produced in large scale in industry [10]. Depending on microorganism and substrate used a wide range of molecular weights can be obtained for scl-PHAs. Typical PHB produced by wild bacteria have a Mw in the range of 88-133  103 kDa with polydispersities (Mw/Mn) of 1.3-2.2, respectively [113]. Maximum Mn reported for biosynthesized PHB is 20 MDa using a recombinant E. coli [114].

9. CONCLUSIONS AND OUTLOOK In response to the increasing public concerns about the unnerving price of petroleum and harmful effects of the petroleum based plastic materials in the environment, this work focuses on the production of biodegradable plastics from low-cost sustainable raw materials. PHA is a biopolymer which can be fully biodegraded into water and carbon dioxide and can be synthesized from sustainable raw materials. Yet, research over decades on PHAs has not made it competitive enough to replace the conventional plastics due to high production costs. This review paper was aimed to provide an overview of the utilization of low-cost waste byproducts such as molasses, whey, lignocellulosic raw materials, fats, oils, waste cooking oil, glycerol and wastewater.

In fermentative PHA productions using aromatic groups containing substrates, the PHAs generated bear aromatic groups [115, 116]. The presence of aromatic monomers into the side chain of PHAs allows to have considerable changes in its physical properties because of the probable strong interactions among aromatic rings [115]. Some physical properties of PHAs containing aromatic groups into its side chain are shown in Table 2. The decomposition temperatures and crystallinity of polymers changed as a function of the length of the acyl side chain of substrate used in the fermentations [117]. The incorporation of phenoxy groups in PHAs was reported when Pseudomonas putida and Pseudomonas oleovorans grew in various carbon substrates containing benzyl rings [118]. The PHAs ranged from amorphous polymers with lowest Tg values of -9°C and highest Tg value of 17°C to semi-crystalline polymers with lowest Tg values of -4°C and highest Tg value of 15°C. Curley et al. (1996) reported that crystalline aromatic PHAs copolymer presented two glass transition temperatures at -37°C and 18°C and two melting temperatures at 48°C and 95°C, respectively [116]. In fermentation using Pseudomonas oleovorans, nonanoic acid (NA) was added together with aromatic substrates [116]. The addition of NA as co-substrate not only increased

Polymer

Tg (°C)

Tm (°C)

Xc (%)

TS (MPa)

EB (%)

References

UHMW P3(HB) b

4

185

80

400

35

[101]

P(3HB-co-20 mol% 3HV)

-1

145

56

20

50

[119]

-15.8

103

--

--

--

[120]

14

70

--

--

--

[115]

-10-17

43-97

--

--

--

[118]

-37/ 18

48/95

--

--

--

[116]

-14.3-13.2

nd-52.1

--

--

--

[117]

10.4-14.8

nd

--

--

--

[121]

Polystyrene

100

240

--

--

--

[119]

PP

-10

176

50-70

38

400

[113]

LDPE

-36

130

20-50

10

620

[113]

PHV c PHA-aryl

a

Raw material cost is one of the major reasons for the high price of PHAs. As reviewed by this paper, various cheap carbon sources could be used for the PHAs production. However, the fermentation efficiency and final PHAs concentration of these fermentations are generally significantly lower than what achieved in the fermentations using pure simple sugars, such as glucose. This will lead to an increasing cost in product separation and purification. In terms of the PHAs properties, there is no significantly difference between fermentations using pure substrate and using industrial or agriculture by-products. Therefore, it is always a delicate trade between pros and cons, and decisions should be made based on balanced considerations with efficiency, costs and sustainability. Moreover, the production from upstream to downstream processing should also be considered as a whole since each parts of the process are interconnected and one would influence on another. Considering all the economic, environmental and social issues, the ultimate goal is to ob-

Physical properties of some PHAs and synthetic plastic commoditiesa.

Table 2.

d

21

Tg is the glass transition temperature; Tm is the melting temperature; Xc is the crystallinity; TS is the tensile strength at break and EB is the elongation at break b UHMW: ultra-high-molecular-weight P3(HB) c PHV: homopolymer poly(3-hydroxyvalerate) (PHV) d PHA-aryl: PHA bearing aryl groups

22 Current Chemical Biology, 2012, Vol. 6, No. 1

tain an economically viable PHAs production based on clean and safe processes, such that the final commercial products can be environmentally compatible, leading to a truly sustainable manufacture which will suffice to enhance people’s lifestyle and living quality. ABBREVIATIONS

Du et al. [6] [7]

[8] [9]

CDW

= Cell dry weight

EB

= Elongation at break

[10]

HA

= Hydroxyalkanoates

[11]

lcl-PHAs

= Long-chain-length

mcl-PHAs

= Medium-chain-length

Mn

= Number average molecular weight

Mw

= Weight average molecular mass

PDI

= Polydispersity index

PHA-aryl

= PHA bearing aryl groups

PHAs

= Polyhydroxyalkanoates

PHB

= Poly(3-hydroxybutyrate)

PHBV

= Poly(hydroxybutyrate-co-hydroxybutyrate)

PHV

= Polyhydroxyvalerate

scl-PHAs

= Short-chain-length PHAs

TAG

= Triacylglycerides

Tg

= glass transition temperature

Tm

= Melting temperature

TS

= Tensile strength

VFA

= Volatile fatty acids

Xc

= Crystallinity

CONFLICT OF INTEREST

[12] [13] [14] [15] [16] [17]

[18]

[19] [20] [21]

[22]

Authors declare no conflict of interest. ACKNOWLEDGEMENTS The work described in this publication was substantially supported by a grant from the City University of Hong Kong (Project Nº 72000248).

[23]

[24]

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Received: November 10, 2011

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Revised: January 19, 2012

Accepted: January 20, 2012