Advertisement

Effect of High Pressure on Paracoccus denitrificans Growth and Polyhydroxyalkanoates Production from Glycerol

  • Maria J. Mota
  • Rita P. Lopes
  • Mário M. Q. Simões
  • Ivonne Delgadillo
  • Jorge A. SaraivaEmail author
Article
  • 25 Downloads

Abstract

The performance of fermentation under non-conventional conditions, such as high pressure (HP), is a strategy currently tested for different fermentation processes. In the present work, the purpose was to apply HP (10–50 MPa) to fermentation by Paracoccus denitrificans, a microorganism able to produce polyhydroxyalkanoates (PHA) from glycerol. In general, cell growth and glycerol consumption were both reduced by HP application, more extensively at higher pressure levels, such as 35 or 50 MPa. PHA production and composition was highly dependent on the pressure applied. HP was found to decrease polymer titers, but increase the PHA content in cell dry mass (%), indicating higher ability to accumulate these polymers in the cells. In addition, some levels of HP affected PHA monomeric composition, with the polymer produced at 10 and 35 MPa showing considerable differences relative to the ones obtained at atmospheric pressure. Therefore, it is possible to foresee that the changes in polymer composition may also affect its physical and mechanical properties. Overall, the results of this study demonstrated that HP technology (at specific levels) can be applied to P. denitrificans fermentations without compromising the ability to produce PHA, with potentially interesting effects on polymer composition.

Keywords

Fermentation Cell growth Glycerol Stress High pressure 

Notes

Funding Information

This work was supported by the FCT/MEC (QOPNA research Unit, FCT UID/QUI/00062/2019), through national funds and, where applicable, co-financed by the FEDER, within the PT2020 Partnership Agreement. The authors Maria J. Mota and Rita P. Lopes were supported by FCT (Fundação para a Ciência e a Tecnologia), with the grants SFRH/BD/97061/2013 and SFRH/BD/97062/2013, respectively.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    da Silva, G. P., Mack, M., & Contiero, J. (2009). Glycerol: a promising and abundant carbon source for industrial microbiology. Biotechnology Advances, 27(1), 30–39.CrossRefGoogle Scholar
  2. 2.
    Kolesárová, N., Hutnan, M., Bodík, I., & Špalková, V. (2011). Utilization of biodiesel by-products for biogas production. BioMed Research International, 2011, 126798.Google Scholar
  3. 3.
    Mattam, A. J., Clomburg, J. M., Gonzalez, R., & Yazdani, S. S. (2013). Fermentation of glycerol and production of valuable chemical and biofuel molecules. Biotechnology Letters, 35(6), 831–842.CrossRefGoogle Scholar
  4. 4.
    Yamane, T., Chen, X.-F., & Ueda, S. (1996). Polyhydroxyalkanoate synthesis from alcohols during the growth of Paracoccus denitrificans. FEMS Microbiology Letters, 135(2–3), 207–211.CrossRefGoogle Scholar
  5. 5.
    Yamane, T., Chen, X., & Ueda, S. (1996). Growth-associated production of poly(3-hydroxyvalerate) from n-pentanol by a methylotrophic bacterium, Paracoccus denitrificans. Applied and Environmental Microbiology, 62(2), 380–384.Google Scholar
  6. 6.
    Ueda, S., Matsumoto, S., Takagi, A., & Yamane, T. (1992). Synthesis of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) from methanol and n-amyl alcohol by the methylotrophic bacteria Paracoccus denitrificans and Methylobacterium extorquens. Applied and Environmental Microbiology, 58(11), 3574–3579.Google Scholar
  7. 7.
    Ashby, R. D., Solaiman, D. K. Y., & Foglia, T. A. (2004). Bacterial poly (hydroxyalkanoate) polymer production from the biodiesel co-product stream. Journal of Polymers and the Environment, 12(3), 105–112.CrossRefGoogle Scholar
  8. 8.
    Mothes, G., Schnorpfeil, C., & Ackermann, J.-U. (2007). Production of PHB from crude glycerol. Engineering in Life Sciences, 7(5), 475–479.CrossRefGoogle Scholar
  9. 9.
    Kalaiyezhini, D., & Ramachandran, K. B. (2015). Biosynthesis of poly-3-hydroxybutyrate (PHB) from glycerol by Paracoccus denitrificans in a batch bioreactor: Effect of process variables. Preparative Biochemistry and Biotechnology, 45(1), 69–83.CrossRefGoogle Scholar
  10. 10.
    Mota, M. J., Lopes, R. P., Koubaa, M., Roohinejad, S., Barba, F. J., Delgadillo, I., & Saraiva, J. A. (2018). Fermentation at non-conventional conditions in food-and bio-sciences by the application of advanced processing technologies. Critical Reviews in Biotechnology, 38(1), 122–140.CrossRefGoogle Scholar
  11. 11.
    Mota, M. J., Lopes, R. P., Delgadillo, I., & Saraiva, J. A. (2013). Microorganisms under high pressure—adaptation, growth and biotechnological potential. Biotechnology Advances, 31(8), 1426–1434.CrossRefGoogle Scholar
  12. 12.
    Picard, A., Daniel, I., Montagnac, G., & Oger, P. (2007). In situ monitoring by quantitative Raman spectroscopy of alcoholic fermentation by Saccharomyces cerevisiae under high pressure. Extremophiles, 11(3), 445–452.CrossRefGoogle Scholar
  13. 13.
    Bothun, G. D., Knutson, B. L., Berberich, J. A., Strobel, H. J., & Nokes, S. E. (2004). Metabolic selectivity and growth of Clostridium thermocellum in continuous culture under elevated hydrostatic pressure. Applied Microbiology and Biotechnology, 65(2), 149–157.CrossRefGoogle Scholar
  14. 14.
    Kato, N., Sato, T., Kato, C., Yajima, M., Sugiyama, J., Kanda, T., Mizuno, M., Nozaki, K., Yamanaka, S., & Amano, Y. (2007). Viability and cellulose synthesizing ability of Gluconacetobacter xylinus cells under high-hydrostatic pressure. Extremophiles, 11(5), 693–698.CrossRefGoogle Scholar
  15. 15.
    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. Biotechnology and Bioengineering, 109(2), 451–461.CrossRefGoogle Scholar
  16. 16.
    Mota, M. J., Lopes, R. P., Delgadillo, I., & Saraiva, J. A. (2015). Probiotic yogurt production under high pressure and the possible use of pressure as an on/off switch to stop/start fermentation. Process Biochemistry, 50(6), 906–911.CrossRefGoogle Scholar
  17. 17.
    Neto, R., Mota, M. J., Lopes, R. P., Delgadillo, I., & Saraiva, J. A. (2016). Growth and metabolism of Oenococcus oeni for malolactic fermentation under pressure. Letters in Applied Microbiology, 63(6), 426–433.CrossRefGoogle Scholar
  18. 18.
    Oger, P. M., & Jebbar, M. (2010). The many ways of coping with pressure. Research in Microbiology, 161(10), 799–809.CrossRefGoogle Scholar
  19. 19.
    Kato, C., & Qureshi, M. H. (1999). Pressure response in deep-sea piezophilic bacteria. Journal of Molecular Microbiology and Biotechnology, 1(1), 87–92.Google Scholar
  20. 20.
    Chilukuri, L. N., & Bartlett, D. H. (1997). Isolation and characterization of the gene encoding single-stranded-DNA-binding protein (SSB) from four marine Shewanella strains that differ in their temperature and pressure optima for growth. Microbiology, 143(4), 1163–1174.CrossRefGoogle Scholar
  21. 21.
    Deguchi, S., Shimoshige, H., Tsudome, M., Mukai, S., Corkery, R. W., Ito, S., & Horikoshi, K. (2011). Microbial growth at hyperaccelerations up to 403,627 x g. Proceedings of the National Academy of Sciences, 108(19), 7997–8002.CrossRefGoogle Scholar
  22. 22.
    Hori, K., Soga, K., & Doi, Y. (1994). Effects of culture conditions on molecular weights of poly (3-hydroxyalkanoates) produced by Pseudomonas putida from octanoate. Biotechnology Letters, 16(7), 709–714.CrossRefGoogle Scholar
  23. 23.
    Braunegg, G., Sonnleitner, B. Y., & Lafferty, R. M. (1978). A rapid gas chromatographic method for the determination of poly-β-hydroxybutyric acid in microbial biomass. Applied Microbiology and Biotechnology, 6(1), 29–37.CrossRefGoogle Scholar
  24. 24.
    Tan, G.-Y. A., Chen, C.-L., Li, L., Ge, L., Wang, L., Razaad, I. M. N., et al. (2014). Start a research on biopolymer polyhydroxyalkanoate (PHA): a review. Polymers, 6(3), 706–754.CrossRefGoogle Scholar
  25. 25.
    Kumar, P., Jun, H.-B., & Kim, B. S. (2018). Co-production of polyhydroxyalkanoates and carotenoids through bioconversion of glycerol by Paracoccus sp. strain LL1. International Journal of Biological Macromolecules, 107(Pt B), 2552–2558.CrossRefGoogle Scholar
  26. 26.
    Davis, R., Kataria, R., Cerrone, F., Woods, T., Kenny, S., O’Donovan, A., et al. (2013). Conversion of grass biomass into fermentable sugars and its utilization for medium chain length polyhydroxyalkanoate (mcl-PHA) production by Pseudomonas strains. Bioresource Technology, 150, 202–209.CrossRefGoogle Scholar
  27. 27.
    Kenny, S. T., Runic, J. N., Kaminsky, W., Woods, T., Babu, R. P., Keely, C. M., Blau, W., & O’Connor, K. E. (2008). Up-cycling of PET (polyethylene terephthalate) to the biodegradable plastic PHA (polyhydroxyalkanoate). Environmental Science & Technology, 42(20), 7696–7701.CrossRefGoogle Scholar
  28. 28.
    de Almeida, A., Giordano, A. M., Nikel, P. I., & Pettinari, M. J. (2010). Effects of aeration on the synthesis of poly (3-hydroxybutyrate) from glycerol and glucose in recombinant Escherichia coli. Applied and Environmental Microbiology, 76(6), 2036–2040.CrossRefGoogle Scholar
  29. 29.
    Üçisik-Akkaya, E., Ercan, O., Yesiladali, S. K., Öztürk, T., Ubay-Çokgör, E., Orhon, D., et al. (2009). Enhanced polyhydroxyalkanoate production by Paracoccus pantotrophus from glucose and mixed substrate. Fresenius Environmental Bulletin, 18(11), 2013–2022.Google Scholar
  30. 30.
    Suriyamongkol, P., Weselake, R., Narine, S., Moloney, M., & Shah, S. (2007). Biotechnological approaches for the production of polyhydroxyalkanoates in microorganisms and plants—a review. Biotechnology Advances, 25(2), 148–175.CrossRefGoogle Scholar
  31. 31.
    Huijberts, G. N., Eggink, G., De Waard, P., Huisman, G. W., & Witholt, B. (1992). Pseudomonas putida KT2442 cultivated on glucose accumulates poly(3-hydroxyalkanoates) consisting of saturated and unsaturated monomers. Applied and Environmental Microbiology, 58(2), 536–544.Google Scholar
  32. 32.
    Możejko-Ciesielska, J., & Kiewisz, R. (2016). Bacterial polyhydroxyalkanoates: Still fabulous? Microbiological Research, 192, 271–282.CrossRefGoogle Scholar
  33. 33.
    Abe, H., Doi, Y., Fukushima, T., & Eya, H. (1994). Biosynthesis from gluconate of a random copolyester consisting of 3-hydroxybutyrate and medium-chain-length 3-hydroxyalkanoates by Pseudomonas sp. 61-3. International Journal of Biological Macromolecules, 16(3), 115–119.CrossRefGoogle Scholar
  34. 34.
    Kato, M., Bao, H. J., Kang, C.-K., Fukui, T., & Doi, Y. (1996). Production of a novel copolyester of 3-hydroxybutyric acid and medium-chain-length 3-hydroxyalkanoic acids by Pseudomonas sp. 61-3 from sugars. Applied Microbiology and Biotechnology, 45(3), 363–370.CrossRefGoogle Scholar
  35. 35.
    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. Reactive and Functional Polymers, 68(11), 1534–1541.CrossRefGoogle Scholar
  36. 36.
    Shahid, S., Mosrati, R., Ledauphin, J., Amiel, C., Fontaine, P., Gaillard, J.-L., & Corroler, D. (2013). Impact of carbon source and variable nitrogen conditions on bacterial biosynthesis of polyhydroxyalkanoates: evidence of an atypical metabolism in Bacillus megaterium DSM 509. Journal of Bioscience and Bioengineering, 116(3), 302–308.CrossRefGoogle Scholar
  37. 37.
    Ribeiro, P. L. L., da Silva, A. C. M. S., Menezes Filho, J. A., & Druzian, J. I. (2015). Impact of different by-products from the biodiesel industry and bacterial strains on the production, composition, and properties of novel polyhydroxyalkanoates containing achiral building blocks. Industrial Crops and Products, 69, 212–223.CrossRefGoogle Scholar
  38. 38.
    Laycock, B., Halley, P., Pratt, S., Werker, A., & Lant, P. (2013). The chemomechanical properties of microbial polyhydroxyalkanoates. Progress in Polymer Science, 38(3–4), 536–583.CrossRefGoogle Scholar
  39. 39.
    Ribeiro, P. L. L., Souza Silva, G., & Druzian, J. I. (2016). Evaluation of the effects of crude glycerol on the production and properties of novel polyhydroxyalkanoate copolymers containing high 11-hydroxyoctadecanoate by Cupriavidus necator IPT 029 and Bacillus megaterium IPT 429. Polymers for Advanced Technologies, 27(4), 542–549.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Maria J. Mota
    • 1
  • Rita P. Lopes
    • 1
  • Mário M. Q. Simões
    • 1
  • Ivonne Delgadillo
    • 1
  • Jorge A. Saraiva
    • 1
    Email author
  1. 1.QOPNA, Chemistry DepartmentUniversity of AveiroAveiroPortugal

Personalised recommendations