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Polyhydroxyalkanoates (PHAs) in Industrial Applications

  • Palmiro PoltronieriEmail author
  • Prasun Kumar
Reference work entry

Abstract

Polyhydroxyalcanoates (PHAs) are biodegradable polyesters produced by many bacteria that accumulate them as intracellular storage material in the cytoplasm. These polymers are potential candidate for substitution of petrochemical nonrenewable plastics for their biodegradable and nontoxic properties.

Polyhydroxyalkanoate (PHA) can be synthesized by different strategies, such as microbial production by wild type or recombinant microorganisms, in vitro production via PHA synthase-mediated catalysis, or using genetically engineered plants.

PHA accumulation in natural strains is favored by high availability of carbon source and a limited amount of macrocomponents (nitrogen, phosphate, oxygen) or microcomponents (sulfate, magnesium ions, and other trace elements).

PHAs are applied in many fields, such as packaging, medicine, or agriculture, but the extensive application of the bioplastics is constrained by high production costs, especially for raw material, downstream processing, and polymer recovery.

In this chapter, the progresses in production of PHA in natural strains and in engineered E. coli, Pseudomonas spp., Bacillus, Aeromonas, and other bacteria, such as the halotolerant Halomonas spp., are presented.

In addition, the constrains on purification steps and the potential of high value applications are presented.

Abbreviations

PHBHHx

poly-3-hydroxybutyrate-co-hydroxyhexanoate

P(3/4HB)

poly(3-hydroxybutyrate-co-4-hydroxybutyrate)

PHB-co-HV

poly-3-hydroxybutyrate-co-3-hydroxyvalerate

PHBHV

poly(3-hydroxybutyrate-cohydroxyvalerate)

References

  1. 1.
    Chanprateep S (2010) Current trends in biodegradable polyhydroxyalkanoates. J Biosci Bioeng 110:621–632Google Scholar
  2. 2.
    Lomas AJ, Webb WR, Han JF, Chen G-Q, Sun X, Zhang Z, El Haj AJ, Forsyth NR (2013) Poly (3-hydroxybutyrate-co-3-hydroxyhexanoate)/collagen hybrid scaffolds for tissue engineering applications. Tissue Eng Part C Methods 19(8):577–585Google Scholar
  3. 3.
    Zhang W, Chen C, Cao R, Maurmann L, Li P (2015) Inhibitors of polyhydroxyalkanoate (PHA) synthases: synthesis, molecular docking, and implications. Chembiochem 16(1):156–166Google Scholar
  4. 4.
    Heinrich D, Raberg M, Fricke P, Kenny ST, Morales-Gamez L, Babu RP, O’Connor KE, Steinbüchel A (2016) Synthesis gas (syngas)-derived medium-chain-length polyhydroxyalkanoate synthesis in engineered Rhodospirillum rubrum. Appl Environ Microbiol 82(20):6132–6140Google Scholar
  5. 5.
    Albuquerque MGE, Eiroa M, Torres C, Nunes BR, Reis MAM (2007) Strategies for the development of a side stream process for polyhydroxyalkanoates (PHA) production from sugarcane molasses. J Biotechnol 130:411–421Google Scholar
  6. 6.
    Bengtsson S, Pisco AR, Johansson P, Lemos PC, Reis MAM (2010) Molecular weight and thermal properties of polyhydroxyalkanoates produced from fermented sugar molasses by open mixed cultures. J Biotechnol 147:172–179Google Scholar
  7. 7.
    Singh G, Kumari A, Mittal A, Yadav A, Aggarwal NK (2013) Poly ß-hydroxybutyrate production by Bacillus subtilis NG220 using sugar industry waste water. Biomed Res Int 2013:952641Google Scholar
  8. 8.
    Zhou XY, Yuan XX, Shi ZY, Meng DC, Jiang WJ, Wu LP, Chen JC, Chen G-Q (2012) Hyperproduction of poly(4-hydroxybutyrate) from glucose by recombinant Escherichia coli. Microb Cell Factories 11:54Google Scholar
  9. 9.
    Getachew A, Woldesenbet F (2016) Production of biodegradable plastic by polyhydroxybutyrate (PHB) accumulating bacteria using low cost agricultural waste material. BMC Res Notes 9(1):509Google Scholar
  10. 10.
    Cerrone F, Davis R, Kenny ST, Woods T, O’Donovan A, Gupta VK, Tuohy M, Babu RP, O’Kiely P, O’Connor K (2015) Use of a mannitol rich ensiled grass press juice (EGPJ) as a sole carbon source for polyhydroxyalkanoates (PHAs) production through high cell density cultivation. Bioresour Technol 191:45–1952Google Scholar
  11. 11.
    Follonier S, Goyder MS, Silvestri AC, Crelier S, Kalman F, Riesen R, Zinn M (2014) Fruit pomace and waste frying oil as sustainable resources for the bioproduction of medium-chain-length polyhydroxyalkanoates. Int J Biol Macromol 71:42–52Google Scholar
  12. 12.
    Haas C, Steinwandter V, Diaz De Apodaca E, Maestro Madurga B, Smerilli M, Dietrich T, Neureiter M (2015) Production of PHB from chicory roots – comparison of three Cupriavidus necator strains. Chem Biochem Eng Q 29:99–112Google Scholar
  13. 13.
    Andreeßen B, Lange AB, Robenek H, Steinbuchel A (2010) Conversion of glycerol to poly (3-hydroxypropionate) in recombinant Escherichia coli. Appl Environ Microbiol 76:622–626Google Scholar
  14. 14.
    de Almeida A, Giordano AM, Nikel PI, Pettinari MJ (2010) Effects of aeration on the synthesis of poly(3-hydroxybutyrate) from glycerol and glucose in recombinant Escherichia coli. Appl Environ Microbiol 76:2036–2040Google Scholar
  15. 15.
    Allen AD, Anderson WA, Ayorinde FO, Eribo BE (2010) Biosynthesis and characterization of copolymer poly(3HB-co-3HV) from saponified Jatropha curcas oil by Pseudomonas oleovorans. J Ind Microbiol Biotechnol 37(8):849–856Google Scholar
  16. 16.
    Mozejko J, Wilke A, Przybylek G, Ciesielski S (2012) Mcl-PHAs produced by Pseudomonas sp. Gl01 using fed-batch cultivation with waste rapeseed oil as carbon source. J Microbiol Biotechnol 22(3):371–377Google Scholar
  17. 17.
    Abid S, Raza ZA, Hussain T (2016) Production kinetics of polyhydroxyalkanoates by using Pseudomonas aeruginosa gamma ray mutant strain EBN-8 cultured on soybean oil. 3 Biotech 6(2):142Google Scholar
  18. 18.
    Ienczak JL, Schmidell W, De Aragão GMF (2013) High-cell-density culture strategies for polyhydroxyalkanoate production: a review. J Ind Microbiol Biotechnol 40:275–286Google Scholar
  19. 19.
    Peña C, Castillo T, García A, Millán M, Segura D (2014) Biotechnological strategies to improve production of microbial poly-(3-hydroxybutyrate): a review of recent research work. Microb Biotechnol 7(4):278–293Google Scholar
  20. 20.
    Jiang G, Hill DJ, Kowalczuk M, Johnston B, Adamus G, Irorere V, Radecka I (2016) Carbon sources for polyhydroxyalkanoates and an integrated biorefinery. Int J Mol Sci 17(7), pii:E1157Google Scholar
  21. 21.
    Khanna S, Srivastava AK (2005) Recent advances in microbial polyhydroxyalkanoates. Process Biochem 40(2):607–619Google Scholar
  22. 22.
    Chen G-Q, Zhang G, Park SJ, Lee SY (2001) Industrial scale production of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate). Appl Microbiol Biotechnol 57:50–55Google Scholar
  23. 23.
    Anjum A, Zuber M, Zia KM, Noreen A, Anjum MN, Tabasum S (2016) Microbial production of polyhydroxyalkanoates(PHAs) and its copolymers: a review of recent advancements. Int J Biol Macromol 89:161–174Google Scholar
  24. 24.
    Chen G-Q, Hajnal I (2015) The ‘PHAome’. Trends Biotechnol 33(10):559–564Google Scholar
  25. 25.
    Dai Y, Lambert L, Yuan Z, Keller J (2008) Characterisation of polyhydroxyalkanoate copolymers with controllable four-monomer composition. J Biotechnol 134:137–145Google Scholar
  26. 26.
    Le Meur S, Zinn M, Egli T, Thöny-Meyer L, Ren Q (2012) Production of medium-chain-length polyhydroxyalkanoates by sequential feeding of xylose and octanoic acid in engineered Pseudomonas putida KT2440. BMC Biotechnol 12:53Google Scholar
  27. 27.
    Wang Y, Chen G-Q (2017) Polyhydroxyalkanoates: sustainability, production, and industrialization. In: Tang C, Ryu CY (eds) Sustainable polymers from biomass. Wiley-VCH Verlag, Amsterdam, The NetherlandsGoogle Scholar
  28. 28.
    Ojumu TJ, Solomon BO (2004) Production of polyhydroxyalcanoates, a bacterial biodegradable polymer. Afr J Biotechnol 3(1):18–24Google Scholar
  29. 29.
    Ren Y, Meng D, Wu L, Chen J, Wu Q, Chen G-Q (2017) Microbial synthesis of a novel terpolyester P(LA-co-3HB-co-3HP) from low-cost substrates. Microb Biotechnol 10(2):371–380Google Scholar
  30. 30.
    Hiroe A, Tsuge K, Nomura CT, Itaya M, Tsuge T (2012) Rearrangement of gene order in the phaCAB operon leads to effective production of ultrahigh-molecular-weight poly[(R)-3-hydroxybutyrate] in genetically engineered Escherichia coli. Appl Environ Microbiol 78:3177–3184Google Scholar
  31. 31.
    Kabe T, Tsuge T, Kasuya K-I, Takemura A, Hikima T, Takata M, Iwata T (2012) Physical and structural effects of adding ultrahigh-molecular-weight poly[(R)-3-hydroxybutyrate] to wild-type poly[(R)-3-hydroxybutyrate]. Macromolecules 45:1858–1865Google Scholar
  32. 32.
    Wang S, Chen W, Xiang H, Yang J, Zhou Z, Zhu M (2016a) Modification and potential application of short-chain-length polyhydroxyalkanoate (SCL-PHA). Polymers 8:273Google Scholar
  33. 33.
    Jian J, Li ZJ, Ye HM, Yuan MQ, Chen G-Q (2010) Metabolic engineering for microbial production of polyhydroxyalkanoates consisting of high 3-hydroxyhexanoate content by recombinant Aeromonas hydrophila. Bioresour Technol 101(15):6096–6102Google Scholar
  34. 34.
    Zhang HF, Ma L, Wang ZH, Chen G-Q (2009) Biosynthesis and characterization of 3-hydroxyalkanoate terpolyesters with adjustable properties by Aeromonas hydrophila. Biotechnol Bioeng 104(3):582–589Google Scholar
  35. 35.
    Rai R, Yunos DM, Boccaccini AR, Knowles JC, Barker IA, Howdle SM, Tredwell GD, Keshavarz T, Roy I (2011) Poly-3-hydroxyoctanoate P(3HO), a medium chain length polyhydroxyalkanoate homopolymer from Pseudomonas mendocina. Biomacromolecules 12(6):2126–2136Google Scholar
  36. 36.
    Gao J, Ramsay JA, Ramsay BA (2016) Fed-batch production of poly-3-hydroxydecanoate from decanoic acid. J Biotechnol 218:102–107Google Scholar
  37. 37.
    Chung AL, Jin H-L, Huang L-J, Ye H-M, Chen J-C, Wu Q, Chen G-Q (2011) Biosynthesis and characterization of poly(3-hydroxydodecanoate) by β-oxidation inhibited mutant of Pseudomonas entomophila L48. Biomacromolecules 12:3559–3566Google Scholar
  38. 38.
    Tortajada M, da Silva LF, Prieto MA (2013) Second-generation functionalized medium-chain-length polyhydroxyalkanoates: the gateway to high-value bioplastic applications. Int Microbiol 16(1):1–15Google Scholar
  39. 39.
    Chen G-Q, Hajnal I, Wu H, Lv L, Ye J (2015) Engineering biosynthesis mechanisms for diversifying polyhydroxyalkanoates. Trends Biotechnol 33:565–574Google Scholar
  40. 40.
    Meng DC, Shen R, Yao H, Chen JC, Wu Q, Chen G-Q (2014) Engineering the diversity of polyesters. Curr Opin Biotechnol 29:24–33Google Scholar
  41. 41.
    Poblete-Castro I, Binger D, Oehlert R, Rohde M (2014) Comparison of mcl-poly(3-hydroxyalkanoates) synthesis by different Pseudomonas putida strains from crude glycerol: citrate accumulates at high titer under PHA-producing conditions. BMC Biotechnol 14:962Google Scholar
  42. 42.
    Wang Q, Yang P, Xian M, Yang Y, Liu C, Xue Y, Zhao G (2013) Biosynthesis of poly(3-hydroxypropionate-co-3-hydroxybutyrate) with fully controllable structures from glycerol. Bioresour Technol 142:741–744Google Scholar
  43. 43.
    Kulkarni SO, Kanekar PP, Jog JP, Patil PA, Nilegaonkar SS, Sarnaik SS, Kshirsagar PR (2011) Characterisation of copolymer, poly (hydroxybutyrate-co-hydroxyvalerate) (PHB-co-PHV) produced by Halomonas campisalis (MCM B-1027), its biodegradability and potential application. Bioresour Technol 102(11):6625–6628Google Scholar
  44. 44.
    Srirangan K, Liu X, Tran TT, Charles TC, Moo-Young M, Chou CP (2016) Engineering of Escherichia coli for direct and modulated biosynthesis of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) copolymer using unrelated carbon sources. Sci Rep 6:36470Google Scholar
  45. 45.
    Yang JE, Choi YJ, Lee SJ, Kang KH, Lee H, Oh YH, Lee SH, Park SJ, Lee SY (2014) Metabolic engineering of Escherichia coli for biosynthesis of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) from glucose. Appl Microbiol Biotechnol 98(1):95–104Google Scholar
  46. 46.
    Zhu C, Nomura CT, Perrotta JA, Stipanovic AJ, Nakas JP (2012) The effect of nucleating agents on physical properties of poly-3-hydroxybutyrate (PHB) and poly-3-hydroxybutyrate-o-3-hydroxyvalerate (PHB-co-HV) produced by Burkholderia cepacia ATCC 17759. Polym Test 31:579–585Google Scholar
  47. 47.
    Li Z-J, Shi Z-Y, Jian J, Guo Y-Y, Wu Q, Chen G-Q (2010) Production of poly(3-hydroxybutyrate-co-4-hydroxybutyrate) from unrelated carbon sources by metabolically engineered Escherichia coli. Metab Eng 12:352–359Google Scholar
  48. 48.
    Hu F, Cao Y, Xiao F, Zhang J, Li H (2007) Site-directed mutagenesis of Aeromonas hydrophila enoyl coenzyme A hydratase enhancing 3-hydroxyhexanoate fractions of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate). Curr Microbiol 55(1):20–24Google Scholar
  49. 49.
    Lee SH, Oh DH, Ahn WS, Lee Y, Choi J, Lee SY (2000) Production of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) by high-cell-density cultivation of Aeromonas hydrophila. Biotechnol Bioeng 67:240–244Google Scholar
  50. 50.
    Tsuge T, Saito Y, Kikkawa Y, Hiraishi T (2004) Y. Biosynthesis and compositional regulation of poly(3-hydroxybutyrate)-co-(3-hydroxyhexanoate) in recombinant Ralstonia eutropha expressing mutated polyhydroxyalkanoate synthase genes. Macromol Biosci 4(3):238–242Google Scholar
  51. 51.
    Wang Y, Chung A, Chen G-Q (2017a) Synthesis of medium-chain-length polyhydroxyalkanoate homopolymers, random copolymers, and block copolymers by an engineered strain of Pseudomonas entomophila. Adv Healthc Mater 6:1601017Google Scholar
  52. 52.
    Xie WP, Chen G-Q (2008) Production and characterization of terpolyester poly(3-hydroxybutyrate- co-4-hydroxybutyrate-co-3-hydroxyhexanoate) by recombinant Aeromonas hydrophila 4AK4 harboring genes phaPCJ. Biochem Eng J 38:384–389Google Scholar
  53. 53.
    Choi SY, Park SJ, Kim WJ, Yang JE, Lee H, Shin J, Sang Y (2016) One-step fermentative production of poly(lactate-co-glycolate) from carbohydrates in Escherichia coli. Nat Biotechnol 34:435–440Google Scholar
  54. 54.
    Pederson EN, McChalicher CWJ, Srienc F (2006) Bacterial synthesis of PHA block copolymers. Biomacromolecules 7:1904–1911Google Scholar
  55. 55.
    Tripathi L, Wu L-P, Chen J, Chen G-Q (2012) Synthesis of diblock copolymer poly-3-hydroxybutyrate -block-poly-3-hydroxyhexanoate [PHB-b-PHHx] by a β-oxidation weakened Pseudomonas putida KT2442. Microb Cell Factories 11:44Google Scholar
  56. 56.
    Kacmar J, Carlson R, Balogh SJ, Srienc F (2005) Staining and quantification of poly-3-hydroxybutyrate in Saccharomyces cerevisiae and Cupriavidus necator cell populations using automated flow cytometry. Cytometry A 69A:27–35Google Scholar
  57. 57.
    Heinrich D, Madkour MH, Al-Ghamdi MA, Shabbaj II, Steinbüchel A (2012) Large scale extraction of poly(3-hydroxybutyrate) from Ralstonia eutropha H16 using sodium hypochlorite. AMB Express 2:59Google Scholar
  58. 58.
    Volova T, Kiselev E, Vinogradova O, Nikolaeva E, Chistyakov A, Sukovatiy A, Shishatskaya E (2014) A glucose-utilizing strain, Cupriavidus euthrophus B-10646: growth kinetics, characterization and synthesis of multicomponent PHAs. PLoS One 9(2):e87551Google Scholar
  59. 59.
    Agrawal T, Kotasthane AS, Kushwah R (2015) Genotypic and phenotypic diversity of polyhydroxybutyrate (PHB) producing Pseudomonas putida isolates of Chhattisgarh region and assessment of its phosphate solubilizing ability. 3 Biotech 5(1):45–60Google Scholar
  60. 60.
    Follonier S, Henes B, Panke S, Zinn M (2012) Putting cells under pressure: a simple and efficient way to enhance the productivity of medium-chain-length polyhydroxyalkanoate in processes with Pseudomonas putida KT2440. Biotechnol Bioeng 109(2):451–461Google Scholar
  61. 61.
    Dietrich D, Illman B, Crooks C (2013) Differential sensitivity of polyhydroxyalkanoate producing bacteria to fermentation inhibitors and comparison of polyhydroxybutyrate production from Burkholderia cepacia and Pseudomonas pseudoflava. BMC Res Notes 6:1–4Google Scholar
  62. 62.
    Chen G-Q, Page WJ (1997) Production of poly-b-hydroxybutyrate by Azotobacter vinelandii in a two-stage fermentation process. Biotechnol Tech 11:347–350Google Scholar
  63. 63.
    Wang X, Li Z, Li X, Qian H, Cai X, Li X, He J (2016b) Poly-β-hydroxybutyrate metabolism is unrelated to the sporulation and parasporal crystal protein formation in Bacillus thuringiensis. Front Microbiol 7:836Google Scholar
  64. 64.
    Bhagowati P, Pradhan S, Dash HR, Das S (2015) Production, optimization and characterization of polyhydroxybutyrate, a biodegradable plastic by Bacillus spp. Biosci Biotechnol Biochem 79(9):1454–1463Google Scholar
  65. 65.
    Sharma P, Bajaj BK (2015) Cost-effective-substrates for production of poly-ß-hydroxybutyrate by a newly isolated Bacillus cereus PS-10. J Environ Biol 36(6):1297–1304Google Scholar
  66. 66.
    Guevara-Martínez M, Sjöberg Gällnö K, Sjöberg G, Jarmander J, Perez-Zabaleta M, Quillaguamán J, Larsson G (2015) Regulating the production of (R)-3-hydroxybutyrate in Escherichia coli by N or P limitation. Front Microbiol 6:844Google Scholar
  67. 67.
    El-sayed AA, Abdel Hafez AM, Hemmat Abdelhady M, Khodair TA (2009) Production of polyhydroxybutyrate (PHB) using batch and two-stage batch culture strategies. Austr J Basic Appl Sci 3:617–627Google Scholar
  68. 68.
    Wang F, Lee SY (1997) Production of poly ß(3-hydroxybutyrate) by fed-batch culture of filamentation-suppressed recombinant Escherichia coli. Appl Environ Microbiol 63:4765–4769Google Scholar
  69. 69.
    Castilho LR, Mitchell DA, Freire DMG (2009) Production of polyhydroxyalkanoates (PHAs) from waste materials and by-products by submerged and solid-state fermentation. Bioresour Technol 100:5996–6009Google Scholar
  70. 70.
    Chen G-Q (2009) A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry. Chem Soc Rev 38(8):2434–2446Google Scholar
  71. 71.
    Jiang XJ, Sun Z, Ramsay JA, Ramsay BA (2013) Fed-batch production of MCL-PHA with elevated 3-hydroxynonanoate content. AMB Express 3(1):50Google Scholar
  72. 72.
    Mahishi LH, Tripathi G, Rawal SK (2003) Poly (3-hydroxybutyrate) (PHB) synthesis by recombinant Escherichia coli harbouring Streptomyces aureofaciens PHB biosynthesis genes: effect of various carbon and nitrogen sources. Microbiol Res 158:19–27Google Scholar
  73. 73.
    Lin Z, Zhang Y, Yuan Q, Liu Q, Li Y, Wang Z, Ma H, Chen T, Zhao X (2015) Metabolic engineering of Escherichia coli for poly(3-hydroxybutyrate) production via threonine bypass. Microb Cell Factories 14:185Google Scholar
  74. 74.
    Inan K, Sal FA, Rahman A, Putman RJ, Agblevor FA, Miller CD (2016) Microbubble assisted polyhydroxybutyrate production in Escherichia coli. BMC Res Notes 9:338Google Scholar
  75. 75.
    Wei XX, Zheng WT, Hou X, Liang J, Li ZJ (2015) Metabolic engineering of Escherichia coli for poly(3-hydroxybutyrate) production under microaerobic condition. Biomed Res Int 2015:789315Google Scholar
  76. 76.
    Tao W, Lv L, Chen G-Q (2017) Engineering Halomonas species TD01 for enhanced polyhydroxyalkanoates synthesis via CRISPRi. Microb Cell Factories 16(1):48Google Scholar
  77. 77.
    Mozejko-Ciesielska J, Dabrowska D, Szalewska-Palasz A, Ciesielski S (2017) Medium-chain-length polyhydroxyalkanoates synthesis by Pseudomonas putida KT2440 relA/spoT mutant: bioprocess characterization and transcriptome analysis. AMB Express 7(1):92Google Scholar
  78. 78.
    Tsuge T, Hyakutake M, Mizuno K (2015) Class IV polyhydroxyalkanoate (PHA) synthases and PHA-producing Bacillus. Appl Microbiol Biotechnol 99(15):6231–6240Google Scholar
  79. 79.
    Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54:450–472Google Scholar
  80. 80.
    Wang Q, Xia Y, Chen Q, Qi Q (2012) Incremental truncation of PHA synthases results in altered product specificity. Enzyme Microb Technol 50:293–297Google Scholar
  81. 81.
    Zheng Z, Li M, Xue XJ, Tian HL, Li Z, Chen GQ (2006) Mutation on N-terminus of poly-3-hydroxyalkanoate (PHA) synthase enhanced PHA accumulation. Appl Microbiol Biotechnol 72:896–905Google Scholar
  82. 82.
    Jia K, Cao R, Hua DH, Li P (2016) Study of class I and class III polyhydroxyalkanoate (PHA) synthases with substrates containing a modified side chain. Biomacromolecules 17(4):1477–1485Google Scholar
  83. 83.
    Chek MF, Kim SY, Mori T, Arsad H, Samian MR, Sudesh K, Hakoshima T (2017) Structure of polyhydroxyalkanoate (PHA) synthase PhaC from Chromobacterium sp. USM2, producing biodegradable plastics. Sci Rep 7(1):5312Google Scholar
  84. 84.
    Wittenborn EC, Jost M, Wei Y, Stubbe J, Drennan CL (2016) Structure of the catalytic domain of the class I polyhydroxybutyrate synthase from Cupriavidus necator. J Biol Chem 291(48):25264–25277Google Scholar
  85. 85.
    Bhubalan K, Chuah JA, Shozui F, Brigham CJ, Taguchi S, Sinskey AJ, Rha C, Sudesh K (2011) Characterization of the highly active polyhydroxyalkanoate synthase of Chromobacterium sp. strain USM2. Appl Environ Microbiol 77(9):2926–2933Google Scholar
  86. 86.
    Chuah JA, Tomizawa S, Yamada M, Tsuge T, Doi Y, Sudesh K, Numata K (2013) Characterization of site-specific mutations in a short-chain-length/medium-chain-length polyhydroxyalkanoate synthase: in vivo and in vitro studies of enzymatic activity and substrate specificity. Appl Environ Microbiol 79(12):3813–3821Google Scholar
  87. 87.
    Sheu DS, Chen WM, Lai YW, Chang RC (2012a) Mutations derived from the thermophilic polyhydroxyalkanoate synthase PhaC enhance the thermostability and activity of PhaC from Cupriavidus necator H16. J Bacteriol 194(10):2620–2629Google Scholar
  88. 88.
    Takase K, Matsumoto K, Taguchi S, Doi Y (2004) Alteration of substrate chain-length specificity of type II synthase for polyhydroxyalkanoate biosynthesis by in vitro evolution: in vivo and in vitro enzyme assays. Biomacromolecules 5:480–485Google Scholar
  89. 89.
    Amara AA, Steinbüchel A, Rehm BH (2002) In vivo evolution of the Aeromonas punctata polyhydroxyalkanoate (PHA) synthase: isolation and characterization of modified PHA synthases with enhanced activity. Appl Microbiol Biotechnol 59:477–482Google Scholar
  90. 90.
    Shozui F, Matsumoto K, Sasaki T, Taguchi S (2009) Engineering of polyhydroxyallanoate synthase by Ser477X/Gln481X saturation mutagenesis for efficient production of 3-hydroxybutyrate-based copolyesters. Appl Microbiol Biotechnol 84:1117–1124Google Scholar
  91. 91.
    Tsuge T, Watanabe S, Shimada D, Abe H, Doi Y, Taguchi S (2007) Combination of N149S and D171G mutations in Aeromonas caviae polyhydroxyalkanoate synthase and impacton polyhydroxyalkanoate biosynthesis. FEMS Microbiol Lett 277:217–222Google Scholar
  92. 92.
    Chen JY, Liu T, Zheng Z, Chen JC, Chen G-Q (2004) Polyhydroxyalkanoate synthases PhaC1 and PhaC2 from Pseudomonas stutzeri 1317 had different substrate specificities. FEMS Microbiol Lett 234:231–237Google Scholar
  93. 93.
    Shen XW, Shi ZY, Song G, Li ZJ, Chen G-Q (2011) Engineering of polyhydroxyalkanoate (PHA) synthase PhaC2Ps of Pseudomonas stutzeri via site-specific mutation for efficient production of PHA copolymers. Appl Microbiol Biotechnol 91(3):655–665Google Scholar
  94. 94.
    Gao X, Yuan XX, Shi ZY, Guo YY, Shen XW, Chen JC, Wu Q, Chen GQ (2012) Production of copolyesters of 3-hydroxybutyrate and medium-chain-length 3-hydroxyalkanoates by E. coli containing an optimized PHA synthase gene. Microb Cell Factories 11:130Google Scholar
  95. 95.
    Nomura CT, Taguchi S (2007) PHA synthase engineering toward superbiocatalysts for custom-made biopolymers. Appl Microbiol Biotechnol 73:969–979Google Scholar
  96. 96.
    Sznajder A, Pfeiffer D, Jendrossek D (2015) Comparative proteome analysis reveals four novel polyhydroxybutyrate (PHB) granule-associated proteins in Ralstonia eutropha H16. Appl Environ Microbiol 81(5):1847–1858Google Scholar
  97. 97.
    Pfeiffer D, Jendrossek D (2014) PhaM is the physiological activator of poly(3-hydroxybutyrate) (PHB) synthase (PhaC1) in Ralstonia eutropha. Appl Environ Microbiol 80(2):555–563Google Scholar
  98. 98.
    Le Meur S, Zinn M, Egli T, Thöny-Meyer L, Ren Q (2014) Improved productivity of poly (4-hydroxybutyrate) (P4HB) in recombinant Escherichia coli using glycerol as the growth substrate with fed-batch culture. Microb Cell Factories 13:131Google Scholar
  99. 99.
    Insomphun C, Kobayashi S, Fujiki T, Numata K (2016) Biosynthesis of polyhydroxyalkanoates containing hydroxyl group from glycolate in Escherichia coli. AMB Express 6(1):29Google Scholar
  100. 100.
    Ahn WS, Park SJ, Lee SY (2000) Production of poly(3-hydroxybutyrate) by fed-batch culture of recombinant Escherichia coli with a highly concentrated whey solution. Appl Environ Microbiol 66:3624–3627Google Scholar
  101. 101.
    Agus J, Kahar P, Abe H, Doi Y, Tsuge T (2006) Molecular weight characterization of poly(R)-3-hydroxybutyrate synthesized by genetically engineered strains of Escherichia coli. Polym Degrad Stab 91:1138–1146Google Scholar
  102. 102.
    Ahmed A, Rushworth JV, Hirst NA, Millner PA (2014) Biosensors for whole-cell bacterial detection. Clin Microbiol Rev 27:631–646Google Scholar
  103. 103.
    Poltronieri P, Mezzolla V, D’Urso OF (2017) PHB production in biofermentors assisted through biosensor applications. Proceedings (MDPI, Baseline) 1(2):4Google Scholar
  104. 104.
    Wu H, Fan Z, Jiang X, Chen J, Chen G-Q (2016) Enhanced production of polyhydroxybutyrate by multiple dividing E. coli. Microb Cell Factories 15:128Google Scholar
  105. 105.
    Chen G-Q, Jiang X-R, Guo Y (2016) Synthetic biology of microbes synthesizing polyhydroxyalkanoates (PHA). Synthetic Systems Biotechnol 1:236–242Google Scholar
  106. 106.
    Borrero-de Acuña JM, Bielecka A, Häussler S, Schobert M, Jahn M, Wittmann C, Jahn D, Poblete-Castro I (2014) Production of medium chain length polyhydroxyalkanoate in metabolic flux optimized Pseudomonas putida. Microb Cell Factories 13:88Google Scholar
  107. 107.
    Tao Z, Peng L, Zhang P, Li YQ, Wang G (2016) Probing the kinetic anabolism of poly-beta-hydroxybutyrate in Cupriavidus necator H16 using single-cell Raman spectroscopy. Sensors (Basel) 16(8):1257Google Scholar
  108. 108.
    Elain A, Le Fellic M, Corre YM, Le Grand A, Le Tilly V, Audic JL, Bruzaud S (2015) Rapid and qualitative fluorescence-based method for the assessment of PHA production in marine bacteria during batch culture. World J Microbiol Biotechnol 31(10):1555–1563Google Scholar
  109. 109.
    Cui Y, Barford JP, Renneberg R (2006) Determination of poly(3-hydroxybutyrate) using a combination of enzyme-based biosensor and alkaline hydrolysis. Anal Sci 22(10):1323–1326Google Scholar
  110. 110.
    Ghoshdastider U, Wu R, Trzaskowski B, Mlynarczyk K, Miszta P, Gurusaran M, Viswanathan S, Renugopalakrishnan V, Filipek S (2015) Nano-encapsulation of glucose oxidase dimer by graphene. RSC Adv 5(18):13570–13578Google Scholar
  111. 111.
    Kunasundari B, Murugaiyah V, Kaur G, Maurer FH, Sudesh K (2013) Revisiting the single cell protein application of Cupriavidus necator H16 and recovering bioplastic granules simultaneously. PLoS One 8(10):e78528Google Scholar
  112. 112.
    Hajnal I, Chen X, Chen G-Q (2016) A novel cell autolysis system for cost-competitive downstream processing. Appl Microbiol Biotechnol 100:9103–9110Google Scholar
  113. 113.
    Martínez V, Herencias C, Jurkevitch E, Prieto MA (2016) Engineering a predatory bacterium as a proficient killer agent for intracellular bio-products recovery: the case of the polyhydroxyalkanoates. Sci Rep 6:24381Google Scholar
  114. 114.
    Jiang Y, Mikova G, Kleerebezem R, van der Wielen LA, Cuellar MC (2015) Feasibility study of an alkaline-based chemical treatment for the purification of polyhydroxybutyrate produced by a mixed enriched culture. AMB Express 5(1):5Google Scholar
  115. 115.
    Bugnicourt E, Cinelli P, Lazzeri A, Alvarez V (2014) Polyhydroxyalkanoate (PHA): review of synthesis, characteristics, processing and potential applications in packaging. Express Polym Lett 8(11):791–808Google Scholar
  116. 116.
    Chen W, Tong YW (2012) PHBV microspheres as neural tissue engineering scaffold support neuronal cell growth and axon dendrite polarization. Acta Biomater 8:540–548Google Scholar
  117. 117.
    Lomas AJ, Chen GGQ, El Haj AJ, Forsyth NR (2012) Poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) supports adhesion and migration of mesenchymal stem cells and tenocytes. World J Stem Cells 4(9):94–100Google Scholar
  118. 118.
    Oryan A, Alidadi S, Moshiri A, Maffulli N (2014) Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res 9:18Google Scholar
  119. 119.
    Liu H, Pancholi M, Stubbs J, Raghavan D (2010) Influence of hydroxyvalerate composition of polyhydroxybutyrate valerate (PHBV) copolymer on bone cell viability and in vitro degradation. J Appl Polym Sci 116:3225–3231Google Scholar
  120. 120.
    Webb WR, Dale TP, Lomas AJ, Zeng G, Wimpenny I, El Haj AJ, Forsyth NR, Chen G-Q (2013) The application of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) scaffolds for tendon repair in the rat model. Biomaterials 34:6683–6694Google Scholar
  121. 121.
    Pourmollaabbassi B, Karbasi S, Hashemibeni B (2016) Evaluate the growth and adhesion of osteoblast cells on nanocomposite scaffold of hydroxyapatite/titania coated with poly hydroxybutyrate. Adv Biomed Res 5:156Google Scholar
  122. 122.
    Rodríguez-Contreras A, García Y, Manero JM, Rupérez E (2017) Antibacterial PHAs coating for titanium implants. Eur Polym J 90:66–78Google Scholar
  123. 123.
    Collins MN, Birkinshaw C (2013) Hyaluronic acid based scaffolds for tissue engineering – a review. Carbohydr Polym 92:1262–1279Google Scholar
  124. 124.
    Peng Q, Zhang ZR, Gong T, Chen GQ, Sun X (2012) A rapid-acting, long-acting insulin formulation based on a phospholipid complex loaded PHBHHx nanoparticles. Biomaterials 33:1583–1588Google Scholar
  125. 125.
    Peng Q, Sun X, Gong T, Wu CY, Zhang T, Tan J et al (2013) Injectable and biodegradable thermosensitive hydrogels loaded with PHBHHx nanoparticles for the sustained and controlled release of insulin. Acta Biomater 9:5063–5069Google Scholar
  126. 126.
    Dong Y, Li P, Chen CB, Wang ZH, Ma P, Chen G-Q (2010) The improvement of fibroblast growth on hydrophobic biopolyesters by coating with polyhydroxyalkanoate granule binding protein PhaP fused with cell adhesion motif RGD. Biomaterials 31:8921–8930Google Scholar
  127. 127.
    Heathman TR, Webb WR, Han J, Dan Z, Chen GQ, Forsyth NR, El Haj AJ, Zhang ZR, Sun X (2014) Controlled production of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) (PHBHHx) nanoparticles for targeted and sustained drug delivery. J Pharm Sci 103(8):2498–2508Google Scholar
  128. 128.
    Nishizuka T, Kurahashi T, Hara T, Hirata H, Kasuga T (2014) Novel intramedullary-fixation technique for long bone fragility fractures using bioresorbable materials. PLoS One 9(8):e104603Google Scholar
  129. 129.
    Ashby RD, Solaiman DK, Strahan GD, Levine AC, Nomura CT (2015) Methanol-induced chain termination in poly(3-hydroxybutyrate) biopolymers: molecular weight control. Int J Biol Macromol 74:195–201Google Scholar
  130. 130.
    Beckers V, Poblete-Castro I, Tomasch J, Wittmann C (2016) Integrated analysis of gene expression and metabolic fluxes in PHA-producing Pseudomonas putida grown on glycerol. Microb Cell Factories 15:73Google Scholar
  131. 131.
    Bidart GN, Ruiz JA, de Almeida A, Méndez BS, Nikel PI (2012) Manipulation of the anoxic metabolism in Escherichia coli by ArcB deletion variants in the ArcBA two-component system. Appl Environ Microbiol 78(24):8784–8794Google Scholar
  132. 132.
    Cesário MT, Raposo RS, de Almeida MCMD, van Keulen F, Ferreira BS, da Fonseca MMR (2014) Enhanced bioproduction of poly-3-hydroxybutyrate from wheat straw lignocellulosic hydrolysates. New Biotechnol 31:104–113Google Scholar
  133. 133.
    Hamieh A, Olama Z, Holail H (2010) Microbial production of polyhydroxybutyrate, a biodegradable plastic using agro-industrial waste products. Global Adv Res J Microbiol 2:054–064Google Scholar
  134. 134.
    Higuchi-Takeuchi M, Morisaki K, Toyooka K, Numata K (2016) Synthesis of high-molecular-weight polyhydroxyalkanoates by marine photosynthetic purple bacteria. PLoS One 11(8):e0160981Google Scholar
  135. 135.
    Jeon JM, Kim HJ, Bhatia SK, Sung C, Seo HM, Kim JH, Park HY, Lee D, Brigham CJ, Yang YH (2017) Application of acetyl-CoA acetyltransferase (AtoAD) in Escherichia coli to increase 3-hydroxyvalerate fraction in poly(3-hydroxybutyrate-co-3-hydroxyvalerate). Bioprocess Biosyst Eng 40(5):781–789Google Scholar
  136. 136.
    Koller M, Dias MMS, Rodríguez-Contreras A, Kunaver M, Žagar E, Kržan A, Braunegg G (2015) Liquefied wood as inexpensive precursor-feedstock for bio-mediated incorporation of (.)-3-Hydroxyvalerate into polyhydroxyalkanoates. Materials 8:6543–6557Google Scholar
  137. 137.
    Koutinas AA, Xu Y, Wang R, Webb C (2007) Polyhydroxybutyrate production from a novel feedstock derived from a wheat-based biorefinery. Enzym Microb Technol 40(5):1035–1044Google Scholar
  138. 138.
    Kushwah BS, Kushwah AV, Singh V (2016) Towards understanding polyhydroxyalkanoates and their use. J Polym Res 23:1–14Google Scholar
  139. 139.
    Lee GN, Na J (2013) Future of microbial polyesters. Microb Cell Factories 12:54Google Scholar
  140. 140.
    Li P, Chakraborty S, Stubbe J (2009) Detection of covalent and noncovalent intermediates in the polymerization reaction catalyzed by a C149S class III polyhydroxybutyrate synthase. Biochemistry 48(39):9202–9211Google Scholar
  141. 141.
    Liu XJ, Zhang J, Hong PH, Li ZJ (2016) Microbial production and characterization of poly-3-hydroxybutyrate by Neptunomonas antarctica. PeerJ 4:e2291Google Scholar
  142. 142.
    Lütke-Eversloh T, Bergander K, Luftmann H, Steinbüchel A (2001) Identification of a new class of biopolymer: bacterial synthesis of a sulfur-containing polymer with thioester linkages. Microbiology 147(Pt 1):11–19Google Scholar
  143. 143.
    Madden LA, Anderson AJ, Asrar J, Berger P, Garrett P (2000) Production and characterization of poly(3-hydroxybutyrate-co-3-hydroxyvalerate-co-4-hydroxybutyrate) synthesized by Ralstonia eutropha in fed-batch cultures. Polymer 41:3499–3505Google Scholar
  144. 144.
    Meng DC, Shi ZY, Wu LP, Zhou Q, Wu Q, Chen JC, Chen G-Q (2012) Production and characterization of poly(3-hydroxypropionate-co-4-hydroxybutyrate) with fully controllable structures by recombinant Escherichia coli containing an engineered pathway. Metab Eng 14:317–324Google Scholar
  145. 145.
    Muhammadi S, Afzal M, Hameed S (2015) Bacterial polyhydroxyalkanoates eco-friendly next generation plastic: production, biocompatibility, biodegradation, physical properties and applications. Green Chem Lett Rev 8:56–77Google Scholar
  146. 146.
    Myung J, Galega WM, Van Nostrand JD, Yuan T, Zhou J, Criddle CS (2015) Long-term cultivation of a stable Methylocystis-dominated methanotrophic enrichment enabling tailored production of poly(3-hydroxybutyrate-co-3-hydroxyvalerate). Bioresour Technol 198:811–818Google Scholar
  147. 147.
    Myung J, Flanagan JCA, Waymouth RM, Criddle CS (2017) Expanding the range of polyhydroxyalkanoates synthesized by methanotrophic bacteria through the utilization of omega-hydroxyalkanoate co-substrates. AMB Express 7(1):118Google Scholar
  148. 148.
    Ostle AG, Holt JG (1982) Nile blue A as a fluorescent stain for poly ß-hydroxybutyrate. Appl Environ Microbiol 44:238–241Google Scholar
  149. 149.
    Pagliano G, Ventorino V, Panico A, Pepe O (2017) Integrated systems for biopolymers and bioenergy production from organic waste and by-products: a review of microbial processes. Biotechnol Biofuels 10:113Google Scholar
  150. 150.
    Pandey A, Negi S, Soccol CR (eds) (2017) Current developments in biotechnology and bioengineering. Production, isolation and purification of industrial products. Elsevier, Amsterdam, The NetherlandsGoogle Scholar
  151. 151.
    Poblete-Castro I, Binger D, Rodrigues A, Becker J, Martins Dos Santos VA, Wittmann C (2013) In-silico-driven metabolic engineering of Pseudomonas putida for enhanced production of polyhydroxyalkanoates. Metab Eng 15:113–123Google Scholar
  152. 152.
    Ramachandran H, Iqbal NM, Sipaut CS, Amirul A-AA (2011) Biosynthesis and characterization of poly(3-hydroxybutyrate-co-3-hydroxyvalerate-co-4-hydroxybutyrate) terpolymer with various monomer compositions by Cupriavidus sp. USMAA2-4. Appl Biochem Biotechnol 164:867–877Google Scholar
  153. 153.
    Ruiz JA, de Almeida A, Godoy MS, Mezzina MP, Bidart GN, Méndez BS, Pettinari MJ, Nikel PI (2013) Escherichia coli redox mutants as microbial cell factories for the synthesis of reduced biochemicals. Comput Struct Biotechnol J 3:e201210019Google Scholar
  154. 154.
    Rydz J, Sikorska W, Kyulavska M, Christova D (2014) Polyester-based (bio)degradable polymers as environmentally friendly materials for sustainable development. Int J Mol Sci 16(1):564–596Google Scholar
  155. 155.
    Scheel RA, Ji L, Lundgren BR, Nomura CT (2016) Enhancing poly(3-hydroxyalkanoate) production in Escherichia coli by the removal of the regulatory gene arcA. AMB Express 6(1):120Google Scholar
  156. 156.
    Simon-Colin C, Raguénès G, Costa B, Guezennec J (2008) Biosynthesis of medium chain length poly-3-hydroxyalkanoates by Pseudomonas guezennei from various carbon sources. React Funct Polym 68:1534–1541Google Scholar
  157. 157.
    Tan G-YA, Chen C-L, Li L, Ge L, Wang L, Razaad IMN, Li Y, Zhao L, Mo Y, Wang J-Y (2014) Start a research on biopolymer polyhydroxyalkanoate (PHA): a review. Polymers 6:706–754Google Scholar
  158. 158.
    Tan D, Yin J, Chen G-Q (2017) Production of polyhydroxyalkanoates. In: Pandey A, Negi S, Soccol CR (eds) Current developments in biotechnology and bioengineering. Production, isolation and purification of industrial products. Elsevier, Amsterdam, pp 655–692Google Scholar
  159. 159.
    Vadlja D, Koller M, Novak M, Braunegg G, Horvat P (2016) Footprint area analysis of binary imaged Cupriavidus necator cells to study PHB production at balanced, transient, and limited growth conditions in a cascade process. Appl Microbiol Biotechnol 100(23):10065–10080Google Scholar
  160. 160.
    Verlinden RA, Hill DJ, Kenward MA, Williams CD, Radecka I (2007) Bacterial synthesis of biodegradable polyhydroxyalkanoates. J Appl Microbiol 102:1437–1449Google Scholar
  161. 161.
    Yang YH, Brigham CJ, Song E, Jeon JM, Rha CK, Sinskey AJ (2012) Biosynthesis of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) containing a predominant amount of 3-hydroxyvalerate by engineered Escherichia coli expressing propionate-CoA transferase. J Appl Microbiol 113(4):815–823Google Scholar
  162. 162.
    Wang Y, Liu S (2014) Production of (R)-3-hydroxybutyric acid by Burkholderia cepacia from wood extract hydrolysates. AMB Express 4:28Google Scholar
  163. 163.
    Kumar P, Patel SKS, Lee JK, Kalia VC (2013) Extending the limits of Bacillus for novel biotechnological applications. Biotechnol Adv 31(8):1543–1561Google Scholar
  164. 164.
    Kumar P, Ray S, Kalia VC (2016) Production of co-polymers of polyhydroxyalkanoates by regulating the hydrolysis of biowastes. Bioresour Technol 200:413–419Google Scholar
  165. 165.
    Patel SKS, Kumar P, Singh M, Lee JK, Kalia VC (2015) Integrative approach to produce hydrogen and polyhydroxybutyrate from biowaste using defined bacterial cultures. Bioresour Technol 176:136–141Google Scholar
  166. 166.
    Oshiki M, Satoh H, Mino T (2011) Rapid quantification of polyhydroxyalkanoates (PHA) concentration in activated sludge with the fluorescent dye Nile blue A. Water Sci Technol 64(3):747–753Google Scholar
  167. 167.
    Spiekermann P, Rehm BHA, Kalscheuer R, Baumeister D, Steinbüchel A (1999) A sensitive, viable-colony staining method using Nile red for direct screening of bacteria that accumulate polyhydroxyalkanoic acids and other lipid storage compounds. 171:73–80Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of Sciences of Food ProductionsNational Research Council, CNR-ISPALecceItaly
  2. 2.Department of Chemical EngineeringChungbuk National UniversityCheongjuRepublic of Korea

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