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.
Similar content being viewed by others
References
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.
Kolesárová, N., Hutnan, M., Bodík, I., & Špalková, V. (2011). Utilization of biodiesel by-products for biogas production. BioMed Research International, 2011, 126798.
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.
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.
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.
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.
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.
Mothes, G., Schnorpfeil, C., & Ackermann, J.-U. (2007). Production of PHB from crude glycerol. Engineering in Life Sciences, 7(5), 475–479.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Oger, P. M., & Jebbar, M. (2010). The many ways of coping with pressure. Research in Microbiology, 161(10), 799–809.
Kato, C., & Qureshi, M. H. (1999). Pressure response in deep-sea piezophilic bacteria. Journal of Molecular Microbiology and Biotechnology, 1(1), 87–92.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Możejko-Ciesielska, J., & Kiewisz, R. (2016). Bacterial polyhydroxyalkanoates: Still fabulous? Microbiological Research, 192, 271–282.
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.
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.
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.
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.
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.
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.
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.
Funding
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mota, M.J., Lopes, R.P., Simões, M.M.Q. et al. Effect of High Pressure on Paracoccus denitrificans Growth and Polyhydroxyalkanoates Production from Glycerol. Appl Biochem Biotechnol 188, 810–823 (2019). https://doi.org/10.1007/s12010-018-02949-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-018-02949-0