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Strategies for PHA production by mixed cultures and renewable waste materials

Abstract

Production of polyhydroxyalkanoates (PHA) by mixed cultures has been widely studied in the last decade. Storage of PHA by mixed microbial cultures occurs under transient conditions of carbon or oxygen availability, known respectively as aerobic dynamic feeding and anaerobic/aerobic process. In these processes, PHA-accumulating organisms, which are quite diverse in terms of phenotype, are selected by the dynamic operating conditions imposed to the reactor. The stability of these processes during long-time operation and the similarity of the polymer physical/chemical properties to the one produced by pure cultures were demonstrated. This process could be implemented at industrial scale, providing that some technological aspects are solved. This review summarizes the relevant research carried out with mixed cultures for PHA production, with main focus on the use of wastes or industrial surplus as feedstocks. Basic concepts, regarding the metabolism and microbiology, and technological approaches, with emphasis on the kind of feedstock and reactor operating conditions for culture selection and PHA accumulation, are described. Challenges for the process optimization are also discussed.

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References

  1. Albuquerque MGE, Eiroa M, Torres C, Nunes BR, Reis MAM (2007) Strategies for the development of a side stream process for polyhydroxyalkanoate (PHA) production from sugar cane molasses. J Biotechnol 130:411–421

  2. Albuquerque MGE, Torres C, Bengtsson S, Werker A, Reis MAM (2008) Strategies for culture selection in a three-stage PHA production process from sugar cane molasses. Proceedings II of 4th IWA Specialised Conference on Sequencing Batch Reactor Technology (SBR4), 7–10 April, Rome, Italy, 2–4

  3. Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microb Rev 54:450–472

  4. Beccari M, Majone M, Massanisso P, Ramadori R (1998) A bulking sludge with high storage response selected under intermittent feeding. Water Res 32:3403–3413

  5. Bengtsson S, Werker A, Christensson M, Welander T (2008a) Production of polyhydroxyalkanoates by activated sludge treating a paper mill wastewater. Biores Technol 99:519–526

  6. Bengtsson S, Werker A, Welander T (2008b) Production of polyhydroxyalkanoates by glycogen accumulating organisms treating a paper mill wastewater. Proceedings of 4th IWA Specialised Conference on Sequencing Batch Reactor Technology (SBR4), 7–10 April, Rome, Italy, 67–74

  7. Bengtsson S, Pisco AR, Werker A, Reis MAM, Lemos PC (2008c) Polyhydroxyalkanoates production from molasses by glycogen accumulating organisms. Proceedings of 4th IWA Specialised Conference on Sequencing Batch Reactor Technology (SBR4), 7–10 April, Rome, Italy, 5–8

  8. Beun JJ, Dirks K, Van Loosdrecht MCM, Heijnen JJ (2002) Poly-(hydroxybutyrate) metabolism in dynamically fed mixed microbial cultures. Water Res 36:1167–1180

  9. Braunegg G, Lefebvre G, Genser KF (1998) Polyhydroxyalkanoates, biopolyesters from renewable resources: physiological and engineering aspects. J Biotechnol 65:127–161

  10. Carta F, Beun JJ, Van Loosdrecht MCM, Heijnen JJ (2001) Simultaneous storage and degradation of PHB and glycogen in activated sludge cultures. Water Res 35:2693–2702

  11. Choi J, Lee SY (1997) Process analysis and economic evaluation for poly (3-hydroxybutyrate) production by fermentation. Bioprocess Eng 17:335–342

  12. Chua H, Yu PHF (1999) Production of biodegradable plastics from chemical wastewater—a novel method to reduce excess activated sludge generated from industrial wastewater treatment. Water Sci Technol 39:273–280

  13. Chua ASM, Takabatake H, Satoh H, Mino T (2003) Production of polyhydroxyalkanoates (PHA) by activated sludge treating municipal wastewater: effect of pH, sludge retention time (SRT), and acetate concentration in influent. Water Res 37:3602–3611

  14. Ciesielski S, Cydzik-Kwiatkowska A, Pokoj T, Klimiuk E (2006) Molecular detection and diversity of medium-chain-length polyhydroxyalkanoates-producing bacteria enriched from activated sludge. J Appl Microbiol 101:190–199

  15. Ciesielski S, Pokoj T, Klimiuk E (2008) Molecular insight into activated sludge producing polyhydroxyalkanoates under aerobic–anaerobic conditions.. J Ind Microbiol Biotechnol 35(8):805–814. doi:https://doi.org/10.1007/s10295-008-0352-7

  16. Coats ER, Loge FJ, Wolcott MP, Englund K, McDonald AG (2007) Synthesis of polyhydroxyalkanoates in municipal wastewater treatment. Water Environ Res 79:2396–2403

  17. Dai Y, Yuan Z, Jack K, Keller J (2007) Production of targeted poly(3-hydroxyalkanoates) copolymers by glycogen accumulating organisms using acetate as sole carbon source. J Biotechnol 129:489–497

  18. Daiger GT, Grady PL (1982) The dynamics of microbial growth on soluble substrates: a unifying theory. Water Res 16:365–382

  19. Dias JML, Serafim LS, Lemos PC, Reis MAM, Oliveira R (2005) Mathematical modelling of a mixed culture cultivation process for the production of polyhydroxybutyrate. Biotechnol Bioeng 92:209–222

  20. Dias JML, Lemos PC, Serafim LS, Oliveira C, Eiroa M, Albuquerque MGE, Ramos AM, Oliveira R, Reis MAM (2006) Recent advances in polyhydroxyalkanoate production by mixed aerobic cultures: from the substrate to the final product. Macromol Biosci 6:885–906

  21. Dias JML, Oehmen A, Serafim LS, Lemos PC, Reis MAM, Oliveira R (2008) Metabolic modelling of polyhydroxyalkanoate copolymers production by mixed microbial cultures. BMC Syst Biol 2:59

  22. Din MF Md, Ujang Z, van Loosdrecht MCM, Ahmad A, Sairan MF (2006) Optimization of nitrogen and phosphorus limitation for better biodegradable plastic production and organic removal using single fed-batch mixed cultures and renewable resources. Water Sci Technol 53:15–20

  23. Dionisi D, Majone M, Tandoi V, Beccari M (2001) Sequencing batch reactor: influence of periodic operation on performance of activated sludge in biological wastewater treatment. Ind Eng Chem Res 40:5110–5119

  24. Dionisi D, Majone M, Papa V, Beccari M (2004) Biodegradable polymers from organic acids by using activated sludge enriched by aerobic periodic feeding. Biotechnol Bioeng 85:569–579

  25. Dionisi D, Beccari M, Di Gregorio S, Majone M, Petrangeli Papini M, Vallini G (2005a) Storage of biodegradable polymers by an enriched microbial community in a sequencing batch reactor operated at high organic load rate. J Chem Tech Biotech 80:1306–1318

  26. Dionisi D, Carucci G, Papinia MP, Riccardi C, Majone M, Carrasco F (2005b) Olive oil mill effluents as a feedstock for production of biodegradable polymers. Water Res 39:2076–2084

  27. Dionisi D, Majone M, Levantesi C, Bellani A, Fuoco A (2006a) Effect of feed length on settleability, substrate uptake and storage in a sequencing batch reactor treating an industrial wastewater. Environ Technol 27:901–908

  28. Dionisi D, Majone M, Vallini G, Di Gregorio S, Beccari M (2006b) Effect of applied organic load rate on biodegradable polymer production by mixed microbial cultures in a sequencing batch reactor. Biotechnol Bioeng 93:76–88

  29. Dionisi D, Majone M, Vallini G, Di Gregorio S, Beccari M (2007) Effect of the length of the cycle on biodegradable polymer production and microbial community selection in a sequencing batch reactor. Biotechnol Prog 23:1064–1073

  30. Fukui T, Doi Y (1997) Cloning and Analysis of the Poly(3-Hydroxybutyrate-co-3-Hydroxyhexanoate) Biosynthesis Genes of Aeromonas caviae. J Bacteriol 179:4821–4830

  31. Grothe E, Moo-Young M, Chisti Y (1999) Fermentation optimization for the production of poly(β-hydroxybutyric acid) microbial thermoplastic. Enzyme Microb Technol 25:132–141

  32. Gujer W, Henze M, Mino T, Van Loosdrecht MCM (1999) Activated sludge model no. 3. Water Sci Technol 39:183–193

  33. Gurieff NB (2007) Production of biodegradable polyhydroxyalkanoate polymers using advanced biological wastewater treatment process technology. Doctoral thesis (University of Queensland)

  34. Kim BS (2000) Production of poly (3-hydroxybutyrate) from inexpensive substrates. Enzyme Microb Technol 27:774–777

  35. Krishna C, van Loosdrecht MCM (1999) Effect of temperature on storage polymers and settleability of activated sludge. Water Res 33:2374–2382

  36. Lee SY (1996) Plastic bacteria? Progress and prospects for polyhydroxyalkanoate production in bacteria. Trends Biotechnol 14:431–438

  37. Lee SY, Choi J (1998) Effect of fermentation performance on the economics of poly-(3-hydroxybutyrate) production by Alcaligenes latus. Polym Degrad Stab 59:387–393

  38. Lee SY, Choi J, Wong HH (1999) Recent advances in polyhydroxyalkanoate production by bacterial fermentation: mini-review. Int J Biol Macromol 25:31–36

  39. Lemos PC, Serafim LS, Santos MM, Reis MAM, Santos H (2003) Metabolic pathway for propionate utilization by phosphorus accumulating organisms in activated sludge: 13C labelling and in vivo NMR. Appl Env Microbiol 69:241–251

  40. Lemos PC, Serafim LS, Reis MAM (2006) Synthesis of polyhydroxyalkanoates from different short-chain fatty acids by mixed cultures submitted to aerobic dynamic feeding. J Biotech 122:226–238

  41. Lemos PC, Dai Y, Yuan Z, Santos H, Keller J, Reis MAM (2007) Metabolism of glycogen-accumulating organisms (GAO) revealed by in vivo 13C nuclear magnetic resonance. Environ Microbiol 9:2694–2706

  42. Lemos PC, Levantesi C, Serafim LS, Rossetti S, Reis MAM, Tandoi V (2008) Microbial characterisation of polyhydroxyalkanoates storing populations selected under different operating conditions using a cell-sorting RT-PCR approach. Appl Microbiol Biotechnol 78:351–360

  43. Levantesi C, Serafim LS, Crocetti GR, Lemos PC, Rossetti S, Blackall LL, Reis MAM, Tandoi V (2002) Analysis of the microbial community structure and function of a laboratory scale enhanced biological phosphate removal reactor. Environ Microbiol 4:559–569

  44. Liu H-Y, Hall PV, Darby JL, Coats ER, Green PG, Thompson DE, Loge FJ (2008) Production of polyhydroxyalkanoate during treatment of tomato cannery wastewater. Water Environ Res 80:367–372

  45. Madison LL, Huisman GW (1999) Metabolic engineering of poly-(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63:21–53

  46. Majone M, Masanisso P, Carucci A, Lindrea K, Tandoi V (1996) Influence of storage on kinetic selection to control aerobic filamentous bulking. Water Sci Technol 34:223–232

  47. Majone M, Dionisi D, Villano M, Beccari M (2008) Proceedings of 4th IWA Specialised Conference on Sequencing Batch Reactor Technology (SBR4), 7–10 April, Rome, Italy, 43–50

  48. Mato T, Ben M, Kennes C, Veiga MC (2008) PHA production using brewery wastewater. Proceedings of 4th IWA Specialised Conference on Sequencing Batch Reactor Technology (SBR4), 7–10 April, Rome, Italy, 59–66

  49. Oehmen A, Lemos PC, Carvalho G, Yuan Z, Keller J, Blackall LL, Reis MAM (2007) Advances in enhanced biological phosphorus removal: from micro to macro scale. Water Res 41:2271–2300

  50. Pereira H, Lemos PC, Carrondo MJT, Crespo JPSG, Reis MAM, Santos H (1996) Model for carbon metabolism in biological phosphorus removal processes based on in vivo 13C-NMR labelling experiments. Water Res 30:2128–2138

  51. Pisco AR, Bengtsson S, Werker A, Reis MAM, Lemos P C (2008) Use of industrial By-products for polyhydroxyalkanoates production by glycogen-accumulating organisms. Proceedings of the 5th IWA Leading-Edge Conference on Water and Wastewater Technologies, 1–4 June, Zurich, Switzerland

  52. Reddy CSK, Ghai R, Kalia RVC (2003) Polyhydroxyalkanoates: an overview. Bioresour Technol 87:137–146

  53. Rehm BHA (2003) Polyester synthases: natural catalysts for plastics. Biochem J 376:15–33

  54. Rhu DH, Lee WH, Kim JY, Choi E (2003) Polyhydroxyalkanoate (PHA) production from waste. Water Sci Technol 48:221–228

  55. Salmiati, Ujang Z, Salim MR, Din MF Md, Ahmad MA (2007) Intracellular biopolymer productions using mixed microbial cultures from fermented POME. Water Sci Technol 56:179–185

  56. Satoh H, Ramey WD, Koch FA, Oldham WK, Mino T, Matsuo T (1996) Anaerobic substrate uptake by the enhanced biological phosphorus removal activated sludge treating real sewage. Water Sci Technol 34:9–16

  57. Satoh H, Iwamoto Y, Mino T, Matsuo T (1998) Activated sludge as a possible source of biodegradable plastic. Water Sci Technol 38:103–109

  58. Serafim LS, Lemos PC, Oliveira RF, Reis MAM (2004) Optimisation of polyhydroxybutyrate production by mixed cultures submitted to aerobic dynamic feeding conditions. Biotech Bioeng 87:145–160

  59. Serafim LS, Lemos PC, Rossetti S, Levantesi C, Tandoi V, Reis MAM (2006) Microbial community analysis with a high PHA storage capacity. Water Sci Technol 54:183–188

  60. Serafim LS, Lemos PC, Torres C, Reis MAM, Ramos AM (2008) The Influence of process parameters on the characteristics of polyhydroxyalkanoates produced by mixed cultures. Macromol Biosci 8:355–366

  61. Takabatake H, Satoh H, Mino T, Matsuo T (2000) Recovery of biodegradable plastics from activated sludge process. Water Sci Technol 42:351–356

  62. Takabatake H, Satoh H, Mino T, Matsuo T (2002) PHA production potential of activated sludge treating wastewater. Water Sci Technol 45:119–126

  63. Van Loosdrecht MCM, Pot MA, Heijnen JJ (1997) Importance of bacterial storage polymers in bioprocess. Water Sci Technol 35:41–47

  64. Wallen LL, Rohwedder WK (1974) Poly-β-hydroxyalkanoate from activated sludge. Environ Sci Technol 8:576–579

  65. Yu J (2001) Production of PHA from starchy wastewater via organic acids. Biotechnology 36:105

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Acknowledgements

The authors acknowledge the financial support of the Fundação para a Ciência e Tecnologia (FCT) through the project POCI/BIO/55789/2004 and EU Integrated Project Contract n° 026515. Luísa S. Serafim and Maria G.E. Albuquerque acknowledge Fundação para a Ciência e Tecnologia for grants SFRH/BPD/41227/2007 and SFRH/BD/17141/2004, respectively. The authors also acknowledge Cristiana Torres for Fig. 2 and Ana Rita Pisco for the experimental results.

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Correspondence to Maria A. M. Reis.

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Serafim, L.S., Lemos, P.C., Albuquerque, M.G.E. et al. Strategies for PHA production by mixed cultures and renewable waste materials. Appl Microbiol Biotechnol 81, 615–628 (2008). https://doi.org/10.1007/s00253-008-1757-y

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Keywords

  • PHA
  • Mixed cultures
  • Aerobic dynamic feeding (ADF)
  • Anaerobic/aerobic (AN/AE)
  • Renewable waste resources