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The Feasibility of Thermophilic Caldimonas manganoxidans as a Platform for Efficient PHB Production

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Abstract

Recently, poly(3-hydroxybutyrate) (PHB) has been found in a few thermophilic strains where several advantages can be gained from running fermentation at high temperatures. Caldimonas manganoxidans, a thermophilic gram-negative bacterium, was investigated for the feasibility as a PHB-producing strain. It is suggested that the best fermentation strategy for achieving the highest PHB concentration of 5.4 ± 1.1 g/L (from 20 g/L glucose) in 24 h is to use the fermentation conditions that are favored for the bacterial growth, yet temperature and pH should be chosen at conditions that are favored for the PHB content. Besides, the above fermentation conditions produce PHB that has a high molecular weight of 1274 kDa with a low polydispersity index (PDI) of 1.45, where the highest Mw of PHB of 1399 kDa (PDI of 1.32) is obtained in this study. To the best knowledge of authors, C. manganoxidans has the best PHB productivity among the thermophiles and is comparable to those common PHB-producing mesophiles.

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References

  1. Akar, A., Akkaya, E. U., Yesiladali, S. K., Çelikyilmaz, G., Çokgor, E. U., Tamerler, C., Orhon, D., & Çakar, Z. P. (2006). Accumulation of polyhydroxyalkanoates by Microlunatus phosphovorus under various growth conditions. Journal of Industrial Microbiology and Biotechnology, 33, 215–220.

    Article  CAS  Google Scholar 

  2. Aoyagi, Y., Doi, Y., & Iwata, T. (2003). Mechanical properties and highly ordered structure of ultra-high-molecular-weight poly[(R)-3-hydroxybutyrate] films: effects of annealing and two-step drawing. Polymer Degradation and Stability, 79, 209–216.

    Article  CAS  Google Scholar 

  3. Ashby, R. D., Solaiman, D. K., & Foglia, T. A. (2004). Bacterial poly (hydroxyalkanoate) polymer production from the biodiesel co-product stream. Journal of Polymer and the Environment, 12, 105–112.

    Article  CAS  Google Scholar 

  4. Belal, E. B. (2013) Production of poly-βhydroxybutyric acid (PHB) by Rhizobium elti and Pseudomonas stutzeri. Current Research Journal of Biological Sciences, 5, 273–284.

  5. Bertrand, J.-L., Ramsay, B., Ramsay, J., & Chavarie, C. (1990). Biosynthesis of poly-β-hydroxyalkanoates from pentoses by Pseudomonas pseudoflava. Applied and Environmental Microbiology, 56, 3133–3138.

    CAS  Google Scholar 

  6. Bonartsev, A., Myshkina, V., Nikolaeva, D., Furina, E., Makhina, T., Livshits, V., Boskhomdzhiev, A., Ivanov, E., Iordanskii, A., & Bonartseva, G. (2007). Biosynthesis, biodegradation, and application of poly (3-hydroxybutyrate) and its copolymers-natural polyesters produced by diazotrophic bacteria. Communicating Current Research and Educational Topics and Trends in Applied Microbiology, 1, 295–307.

    Google Scholar 

  7. Brigham, C. J., & Sinskey, A. J. (2012). Applications of polyhydroxyalkanoates in the medical industry. International Journal of Biotechnology for Wellness Industries, 1, 52–60.

    Google Scholar 

  8. Chen, S.-K., Chin, W.-C., Tsuge, K., Huang, C.-C., & Li, S.-Y. (2013). Fermentation approach for enhancing 1-butanol production using engineered butanologenic Escherichia coli. Bioresource Technology, 145, 204–209.

    Article  CAS  Google Scholar 

  9. Chen, Y., Tsai, Y.-H., Chou, I., Tseng, S.-H. and Wu, H.-S. (2014) Application of biodegradable polyhydroxyalkanoates as surgical films for ventral hernia repair in mice. International Journal of Polymer Science, 11. doi:10.1155/2014/789681.

  10. Chien, C.-C., Chen, C.-C., Choi, M.-H., Kung, S.-S., & Wei, Y.-H. (2007). Production of poly-β-hydroxybutyrate (PHB) by Vibrio spp. isolated from marine environment. Journal of Biotechnology, 132, 259–263.

    Article  CAS  Google Scholar 

  11. Chien, C.-C., Hong, C.-C., Soo, P.-C., Wei, Y.-H., Chen, S.-Y., Cheng, M.-L., & Sun, Y.-M. (2010). Functional expression of phaCAB genes from Cupriavidus taiwanensis strain 184 in Escherichia coli for polyhydroxybutyrate production. Applied Biochemistry and Biotechnology, 162, 2355–2364.

    Article  CAS  Google Scholar 

  12. Ciou, C.-Y., Li, S.-Y., & Wu, T.-M. (2014). Morphology and degradation behavior of poly(3-hydroxybutyrate-co-3-hydroxyvalerate)/layered double hydroxides composites. European Polymer Journal, 59, 136–143.

    Article  CAS  Google Scholar 

  13. Grothe, E., Moo-Young, M., & Chisti, Y. (1999). Fermentation optimization for the production of poly (β-hydroxybutyric acid) microbial thermoplastic. Enzyme and Microbial Technology, 25, 132–141.

    Article  CAS  Google Scholar 

  14. Hamieh, A., Olama, Z., & Holail, H. (2013). Microbial production of polyhydroxybutyrate, a biodegradable plastic using agro-industrial waste products. Global Advanced Research Journal of Microbiology, 2, 54–64.

    Google Scholar 

  15. Harding, K., Dennis, J., Von Blottnitz, H., & Harrison, S. (2007). Environmental analysis of plastic production processes: comparing petroleum-based polypropylene and polyethylene with biologically-based poly-β-hydroxybutyric acid using life cycle analysis. Journal of Biotechnology, 130, 57–66.

    Article  CAS  Google Scholar 

  16. Ho, M.-H., Li, S.-Y., Ciou, C.-Y. and Wu, T.-M. (2014) The morphology and degradation behavior of electrospun poly(3-hydroxybutyrate)/Magnetite and poly(3-hydroxybutyrate-co-3-hydroxyvalerate)/Magnetite composites. Journal of Applied Polymer Science, 131, 41070.

  17. Holst, O., Manelius, Å., Krahe, M., Märkl, H., Raven, N., & Sharp, R. (1997). Thermophiles and fermentation technology. Comparative Biochemistry and Physiology. Part A, Physiology, 118, 415–422.

    Article  Google Scholar 

  18. Hoshino, A., & Isono, Y. (2002). Degradation of aliphatic polyester films by commercially available lipases with special reference to rapid and complete degradation of poly (L-lactide) film by lipase PL derived from Alcaligenes sp. Biodegradation, 13, 141–147.

    Article  CAS  Google Scholar 

  19. Ibrahim, M., Willems, A., & Steinbüchel, A. (2010). Isolation and characterization of new poly (3HB)‐accumulating star‐shaped cell‐aggregates‐forming thermophilic bacteria. Journal of Applied Microbiology, 109, 1579–1590.

    CAS  Google Scholar 

  20. Jackson, F. A., & Dawes, E. A. (1976). Regulation of the tricarboxylic acid cycle and poly-β-hydroxybutyrate metabolism in Azotobacter beijerinckii grown under nitrogen or oxygen limitation. Journal of General Microbiology, 97, 303–312.

    Article  CAS  Google Scholar 

  21. Kadouri, D., Jurkevitch, E., & Okon, Y. (2003). Involvement of the reserve material poly-β-hydroxybutyrate in Azospirillum brasilense stress endurance and root colonization. Applied and Environmental Microbiology, 69, 3244–3250.

    Article  CAS  Google Scholar 

  22. Khanna, S., & Srivastava, A. K. (2005). Statistical media optimization studies for growth and PHB production by Ralstonia eutropha. Process Biochemistry, 40, 2173–2182.

    Article  CAS  Google Scholar 

  23. Lawrence, A., Schoenheit, J., He, A., Tian, J., Liu, P., Stubbe, J., & Sinskey, A. (2005). Transcriptional analysis of Ralstonia eutropha genes related to poly-(R)-3-hydroxybutyrate homeostasis during batch fermentation. Applied Microbiology and Biotechnology, 68, 663–672.

    Article  CAS  Google Scholar 

  24. Li, S.-Y., Srivastava, R., Suib, S. L., Li, Y., & Parnas, R. S. (2011). Performance of batch, fed-batch, and continuous A–B–E fermentation with pH-control. Bioresource Technology, 102, 4241–4250.

    Article  CAS  Google Scholar 

  25. Liu, Y., Huang, S., Zhang, Y., & Xu, F. (2014). Isolation and characterization of a thermophilic Bacillus shackletonii K5 from a biotrickling filter for the production of polyhydroxybutyrate. Journal of Environmental Sciences, 26, 1453–1462.

    Article  CAS  Google Scholar 

  26. Loh, X. J., Goh, S. H., & Li, J. (2007). Hydrolytic degradation and protein release studies of thermogelling polyurethane copolymers consisting of poly[(R)-3-hydroxybutyrate], poly(ethylene glycol), and poly(propylene glycol). Biomaterials, 28, 4113–4123.

    Article  CAS  Google Scholar 

  27. Maehara, A., Ueda, S., Nakano, H., & Yamane, T. (1999). Analyses of a polyhydroxyalkanoic acid granule-associated 16-Kilodalton Protein and its putative regulator in the pha Locus of Paracoccus denitrificans. Journal of Bacteriology, 181, 2914–2921.

    CAS  Google Scholar 

  28. Miller, G. (1959). Use of DNS reagent for the measurement of reducing sugar. Analytical Chemistry, 31, 426–428.

    Article  CAS  Google Scholar 

  29. Mona, K. G., Azza, E. S., & Sanaa, H. O. (2001). Production of PHB by a Bacillus megaterium strain using sugarcane molasses and corn steep liquor as sole carbon and nitrogen source. Microbiological Research, 156, 201–207.

    Article  Google Scholar 

  30. Nishioka, M., Nakai, K., Miyake, M., Asada, Y., & Taya, M. (2001). Production of poly-β-hydroxybutyrate by thermophilic cyanobacterium, Synechococcus sp. MA19, under phosphate-limited conditions. Biotechnology Letters, 23, 1095–1099.

    Article  CAS  Google Scholar 

  31. Oehmen, A., Keller-Lehmann, B., Zeng, R. J., Yuan, Z., & Keller, J. (2005). Optimisation of poly-β-hydroxyalkanoate analysis using gas chromatography for enhanced biological phosphorus removal systems. Journal of Chromatography A, 1070, 131–136.

    Article  CAS  Google Scholar 

  32. Philip, S., Sengupta, S., Keshavarz, T., & Roy, I. (2009). Effect of impeller speed and pH on the production of poly (3-hydroxybutyrate) using Bacillus cereus SPV. Biomacromolecules, 10, 691–699.

    Article  CAS  Google Scholar 

  33. Quagliano, J., & Miyazaki, S. S. (1997). Effect of aeration and carbon/nitrogen ratio on the molecular mass of the biodegradable polymer poly-β-hydroxybutyrate obtained from Azotobacter chroococcum 6B. Applied Microbiology and Biotechnology, 48, 662–664.

    Article  CAS  Google Scholar 

  34. Quillaguamán, J., Doan-Van, T., Guzmán, H., Guzmán, D., Martín, J., Everest, A., & Hatti-Kaul, R. (2008). Poly (3-hydroxybutyrate) production by Halomonas boliviensis in fed-batch culture. Applied Microbiology and Biotechnology, 78, 227–232.

    Article  Google Scholar 

  35. Ramsay, B. A., Saracovan, I., Ramsay, J., & Marchessault, R. (1992). Effect of nitrogen limitation on long-side-chain poly-beta-hydroxyalkanoate synthesis by Pseudomonas resinovorans. Applied and Environmental Microbiology, 58, 744–746.

    CAS  Google Scholar 

  36. Santhanam, A., & Sasidharan, S. (2010). Microbial production of polyhydroxy alkanotes (PHA) from Alcaligens spp. and Pseudomonas oleovorans using different carbon sources. African Journal of Biotechnology, 9, 3144–3150.

    CAS  Google Scholar 

  37. Senior, P., Beech, G., Ritchie, G., & Dawes, E. (1972). The role of oxygen limitation in the formation of poly-beta-hydroxybutyrate during batch and continuous culture of Azotobacter beijerinckii. The Biochemical Journal, 128, 1193–1201.

    Article  CAS  Google Scholar 

  38. Shah, A. A., Hasan, F., Hameed, A., & Ahmed, S. (2008). Biological degradation of plastics: a comprehensive review. Biotechnology Advances, 26, 246–265.

    Article  CAS  Google Scholar 

  39. Sheu, D.-S., Chen, W.-M., Yang, J.-Y., & Chang, R.-C. (2009). Thermophilic bacterium Caldimonas taiwanensis produces poly (3-hydroxybutyrate-co-3-hydroxyvalerate) from starch and valerate as carbon sources. Enzyme and Microbial Technology, 44, 289–294.

    Article  CAS  Google Scholar 

  40. Sim, S. J., Snell, K. D., Hogan, S. A., Stubbe, J., Rha, C., & Sinskey, A. J. (1997). PHA synthase activity controls the molecular weight and polydispersity of polyhydroxybutyrate in vivo. Nature Biotechnology, 15, 63–67.

    Article  CAS  Google Scholar 

  41. Sorrentino, A., Gorrasi, G., & Vittoria, V. (2007). Potential perspectives of bio-nanocomposites for food packaging applications. Trends in Food Science and Technology, 18, 84–95.

    Article  CAS  Google Scholar 

  42. Suzuki, T., Deguchi, H., Yamane, T., Shimizu, S., & Gekko, K. (1988). Control of molecular weight of poly-β-hydroxybutyric acid produced in fet-batch culture of Protomonas extorquens. Applied Microbiology and Biotechnology, 27, 487–491.

    Article  CAS  Google Scholar 

  43. Taidi, B., Anderson, A. J., Dawes, E. A., & Byrom, D. (1994). Effect of carbon source and concentration on the molecular mass of poly (3-hydroxybutyrate) produced by Methylobacterium extorquens and Alcaligenes eutrophus. Applied Microbiology and Biotechnology, 40, 786–790.

    Article  CAS  Google Scholar 

  44. Takeda, M., Kamagata, Y., Ghiorse, W. C., Hanada, S., & Koizumi, J.-i. (2002). Caldimonas manganoxidans gen. nov., sp. nov., a poly (3-hydroxybutyrate)-degrading, manganese-oxidizing thermophile. International Journal of Systematic and Evolutionary Microbiology, 52, 895–900.

    CAS  Google Scholar 

  45. Takeda, M., Kitashima, K., Adachi, K., Hanaoka, Y., Suzuki, I., & Koizumi, J.-i. (2000). Cloning and expression of the gene encoding thermostable poly (3-hydroxybutyrate) depolymerase. Journal of Bioscience and Bioengineering, 90, 416–421.

    Article  CAS  Google Scholar 

  46. Takeda, M., Koizumi, J.-I., Yabe, K., & Adachi, K. (1998). Thermostable poly(3-hydroxybutyrate) depolymerase of a thermophilic strain of Leptothrix sp. isolated from a hot spring. Journal of Fermentation and Bioengineering, 85, 375–380.

    Article  CAS  Google Scholar 

  47. Tanadchangsaeng, N., & Yu, J. (2012). Microbial synthesis of polyhydroxybutyrate from glycerol: gluconeogenesis, molecular weight and material properties of biopolyester. Biotechnology and Bioengineering, 109, 2808–2818.

    Article  CAS  Google Scholar 

  48. Tokiwa, Y., & Calabia, B. (2006). Biodegradability and biodegradation of poly(lactide). Applied Microbiology and Biotechnology, 72, 244–251.

    Article  CAS  Google Scholar 

  49. Trainer, M. A., & Charles, T. C. (2006). The role of PHB metabolism in the symbiosis of rhizobia with legumes. Applied Microbiology and Biotechnology, 71, 377–386.

    Article  CAS  Google Scholar 

  50. Tseng, C.-L., Chen, H.-J., & Shaw, G.-C. (2006). Identification and characterization of the Bacillus thuringiensis phaZ gene, encoding new intracellular poly-3-hydroxybutyrate depolymerase. Journal of Bacteriology, 188, 7592–7599.

    Article  CAS  Google Scholar 

  51. Valappil, S. P., Misra, S. K., Boccaccini, A. R., Keshavarz, T., Bucke, C., & Roy, I. (2007). Large-scale production and efficient recovery of PHB with desirable material properties, from the newly characterised Bacillus cereus SPV. Journal of Biotechnology, 132, 251–258.

    Article  CAS  Google Scholar 

  52. Vishnuvardhan Reddy, S., Thirumala, M., & Mahmood, S. K. (2009). Production of PHB and P (3HB-co-3HV) biopolymers by Bacillus megaterium strain OU303A isolated from municipal sewage sludge. World Journal of Microbiology and Biotechnology, 25, 391–397.

    Article  CAS  Google Scholar 

  53. Wang, F., & Lee, S. Y. (1997). Poly (3-hydroxybutyrate) production with high productivity and high polymer content by a fed-batch culture of alcaligenes latus under nitrogen limitation. Applied and Environmental Microbiology, 63, 3703–3706.

    CAS  Google Scholar 

  54. Wang, J., & Yu, H.-Q. (2007). Biosynthesis of polyhydroxybutyrate (PHB) and extracellular polymeric substances (EPS) by Ralstonia eutropha ATCC 17699 in batch cultures. Applied Microbiology and Biotechnology, 75, 871–878.

    Article  CAS  Google Scholar 

  55. Xin, J., Zhang, Y., Dong, J., Song, H., & Xia, C. (2013). An experimental study on molecular weight of poly-3-hydroxybutyrate (PHB) accumulated in Methylosinus trichosporium IMV 3011. African Journal of Biotechnology, 10, 7078–7087.

    Google Scholar 

  56. Xu, F., Huang, S., Liu, Y., Zhang, Y., & Chen, S. (2014). Comparative study on the production of poly (3-hydroxybutyrate) by thermophilic Chelatococcus daeguensis TAD1: a good candidate for large-scale production. Applied Microbiology and Biotechnology, 98, 3965–3974.

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by the Ministry of Science and Technology Taiwan, MOST-102-2221-E-005-064 and MOST-103-2221-E-005-072-MY3.

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Authors and Affiliations

  1. Department of Chemical Engineering, National Chung Hsing University, Taichung 402, Taiwan

    Li-Jung Hsiao, Ji-Hong Lin, Pantitra Sankatumvong & Si-Yu Li

  2. Department of Materials Science and Engineering, National Chung Hsing University, Taichung 402, Taiwan

    Tzong-Ming Wu

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Correspondence to Si-Yu Li.

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Hsiao, LJ., Lin, JH., Sankatumvong, P. et al. The Feasibility of Thermophilic Caldimonas manganoxidans as a Platform for Efficient PHB Production. Appl Biochem Biotechnol 180, 852–871 (2016). https://doi.org/10.1007/s12010-016-2138-0

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