Polyhydroxybutyrate Production from the Macroalga Rugulopteryx okamurae: Effect of Hydrothermal Acid Pretreatment
Abstract
:1. Introduction
2. Material and Methods
2.1. Sampling and Conditioning of Seaweed Biomass
2.2. Thermochemical Pretreatment Process
2.3. Enzymatic Saccharification
2.4. Fermentation of Sugar Hydrolysates for PHB Production
2.4.1. Micro-Organism and Culture Media
2.4.2. PHB Production by C. necator on Synthetic Media
2.4.3. PHB Production by C. necator on Algal Hydrolysate
2.5. Analytical Techniques
3. Results and Discussion
3.1. Fermentation for PHB Production with Synthetic Media
3.2. Fermentation of Algal Hydrolysate
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Al-Battashi, H.S.; Annamalai, N.; Sivakumar, N.; Al-Bahry, S.; Tripathi, B.N.; Nguyen, Q.D.; Gupta, V.K. Lignocellulosic Biomass (LCB): A Potential Alternative Biorefinery Feedstock for Polyhydroxyalkanoates Production. Rev. Environ. Sci. Bio/Technol. 2019, 18, 183–205. [Google Scholar] [CrossRef]
- Ilyas, R.A.; Sapuan, S.M.; Kadier, A.; Kalil, M.S.; Ibrahim, R.; Atikah, M.S.N.; Nurazzi, N.M.; Nazrin, A.; Lee, C.H.; Faiz Norrrahim, M.N.; et al. Properties and Characterization of PLA, PHA, and Other Types of Biopolymer Composites. In Advanced Processing, Properties, and Applications of Starch and Other Bio-Based Polymers; Elsevier: Amsterdam, The Netherlands, 2020; pp. 111–138. [Google Scholar]
- Saratale, R.G.; Saratale, G.D.; Cho, S.K.; Kim, D.S.; Ghodake, G.S.; Kadam, A.; Kumar, G.; Bharagava, R.N.; Banu, R.; Shin, H.S. Pretreatment of Kenaf (Hibiscus Cannabinus L.) Biomass Feedstock for Polyhydroxybutyrate (PHB) Production and Characterization. Bioresour. Technol. 2019, 282, 75–80. [Google Scholar] [CrossRef] [PubMed]
- Raza, Z.A.; Abid, S.; Banat, I.M. Polyhydroxyalkanoates: Characteristics, Production, Recent Developments and Applications. Int. Biodeterior. Biodegrad. 2018, 126, 45–56. [Google Scholar] [CrossRef]
- Sohn, Y.J.; Son, J.; Jo, S.Y.; Park, S.Y.; Yoo, J.I.; Baritugo, K.A.; Na, J.G.; Choi, J.-i.; Kim, H.T.; Joo, J.C.; et al. Chemoautotroph Cupriavidus necator as a Potential Game-Changer for Global Warming and Plastic Waste Problem: A Review. Bioresour. Technol. 2021, 340, 125693. [Google Scholar] [CrossRef] [PubMed]
- Gholami, A.; Mohkam, M.; Rasoul-Amini, S.; Ghasemi, Y. Industrial Production of Polyhydroxyalkanoates by Bacteria: Opportunities and Challenges. Minerva Biotecnol. 2016, 28, 59–74. [Google Scholar]
- Choi, J.; Lee, S.Y. Process Analysis and Economic Evaluation for Poly(3-Hydroxybutyrate) Production by Fermentation. Bioprocess Eng. 1997, 17, 335. [Google Scholar] [CrossRef]
- Du, C.; Sabirova, J.; Soetaert, W.; Ki Carol Lin, S. Polyhydroxyalkanoates Production from Low-Cost Sustainable Raw Materials. Curr. Chem. Biol. 2012, 6, 14–25. [Google Scholar] [CrossRef]
- Cesário, M.T.; Raposo, R.S.; de Almeida, M.C.M.; van Keulen, F.; Ferreira, B.S.; Telo, J.P.; da Fonseca, M.M.R. Production of Poly(3-Hydroxybutyrate-Co-4-Hydroxybutyrate) by Burkholderia sacchari Using Wheat Straw Hydrolysates and Gamma-Butyrolactone. Int. J. Biol. Macromol. 2014, 71, 59–67. [Google Scholar] [CrossRef] [PubMed]
- Davis, R.; Kataria, R.; Cerrone, F.; Woods, T.; Kenny, S.; O’Donovan, A.; Guzik, M.; Shaikh, H.; Duane, G.; Gupta, V.K.; et al. Conversion of Grass Biomass into Fermentable Sugars and Its Utilization for Medium Chain Length Polyhydroxyalkanoate (Mcl-PHA) Production by Pseudomonas Strains. Bioresour. Technol. 2013, 150, 202–209. [Google Scholar] [CrossRef]
- Getachew, A.; Woldesenbet, F. Production of Biodegradable Plastic by Polyhydroxybutyrate (PHB) Accumulating Bacteria Using Low Cost Agricultural Waste Material. BMC Res. Notes 2016, 9, 509. [Google Scholar] [CrossRef]
- Adeleye, A.T.; Odoh, C.K.; Enudi, O.C.; Banjoko, O.O.; Osiboye, O.O.; Toluwalope Odediran, E.; Louis, H. Sustainable Synthesis and Applications of Polyhydroxyalkanoates (PHAs) from Biomass. Process Biochem. 2020, 96, 174–193. [Google Scholar] [CrossRef]
- Yun, E.J.; Kim, H.T.; Cho, K.M.; Yu, S.; Kim, S.; Choi, I.G.; Kim, K.H. Pretreatment and Saccharification of Red Macroalgae to Produce Fermentable Sugars. Bioresour. Technol. 2016, 199, 311–318. [Google Scholar] [CrossRef]
- Öhgren, K.; Bura, R.; Saddler, J.; Zacchi, G. Effect of Hemicellulose and Lignin Removal on Enzymatic Hydrolysis of Steam Pretreated Corn Stover. Bioresour. Technol. 2007, 98, 2503–2510. [Google Scholar] [CrossRef] [PubMed]
- Fernand, F.; Israel, A.; Skjermo, J.; Wichard, T.; Timmermans, K.R.; Golberg, A. Offshore Macroalgae Biomass for Bioenergy Production: Environmental Aspects, Technological Achievements and Challenges. Renew. Sustain. Energy Rev. 2017, 75, 35–45. [Google Scholar] [CrossRef]
- Jiang, R.; Ingle, K.N.; Golberg, A. Macroalgae (Seaweed) for Liquid Transportation Biofuel Production: What Is Next? Algal Res. 2016, 14, 48–57. [Google Scholar] [CrossRef]
- Greiserman, S.; Epstein, M.; Chemodanov, A.; Steinbruch, E.; Prabhu, M.; Guttman, L.; Jinjikhashvily, G.; Shamis, O.; Gozin, M.; Kribus, A.; et al. Co-Production of Monosaccharides and Hydrochar from Green Macroalgae Ulva (Chlorophyta) sp. with Subcritical Hydrolysis and Carbonization. BioEnergy Res. 2019, 12, 1090–1103. [Google Scholar] [CrossRef]
- Harb, T.B.; Chow, F. An Overview of Beach-Cast Seaweeds: Potential and Opportunities for the Valorization of Underused Waste Biomass. Algal Res. 2022, 62, 102643. [Google Scholar] [CrossRef]
- Lymperatou, A.; Engelsen, T.K.; Skiadas, I.V.; Gavala, H.N. Different Pretreatments of Beach-Cast Seaweed for Biogas Production. J. Clean. Prod. 2022, 362, 132277. [Google Scholar] [CrossRef]
- Carrillo, J.A.; Ocaña, Ó.; Ballesteros, E. Massive Proliferation of a Dictyotalean Species (Phaeophyceae, Ochrophyta) through the Strait of Gibraltar (Research Note). Rev. Acad. Canar. Cienc. 2016, 28, 165–170. [Google Scholar]
- García-Gómez, J.C.; Sempere-Valverde, J.; González, A.R.; Martínez-Chacón, M.; Olaya-Ponzone, L.; Sánchez-Moyano, E.; Ostalé-Valriberas, E.; Megina, C. From Exotic to Invasive in Record Time: The Extreme Impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in the Strait of Gibraltar. Sci. Total Environ. 2020, 704, 135408. [Google Scholar] [CrossRef]
- Wang, D.; Kim, D.H.; Kim, K.H. Effective Production of Fermentable Sugars from Brown Macroalgae Biomass. Appl. Microbiol. Biotechnol. 2016, 100, 9439–9450. [Google Scholar] [CrossRef] [PubMed]
- Ko, J.K.; Um, Y.; Park, Y.-C.; Seo, J.-H.; Kim, K.H. Compounds Inhibiting the Bioconversion of Hydrothermally Pretreated Lignocellulose. Appl. Microbiol. Biotechnol. 2015, 99, 4201–4212. [Google Scholar] [CrossRef] [PubMed]
- Ding, L.; Cheng, J.; Lin, R.; Deng, C.; Zhou, J.; Murphy, J.D. Improving Biohydrogen and Biomethane Co-Production via Two-Stage Dark Fermentation and Anaerobic Digestion of the Pretreated Seaweed Laminaria digitata. J. Clean. Prod. 2020, 251, 119666. [Google Scholar] [CrossRef]
- Sivagurunathan, P.; Kumar, G.; Kobayashi, T.; Xu, K.; Kim, S.-H. Effects of Various Dilute Acid Pretreatments on the Biochemical Hydrogen Production Potential of Marine Macroalgal Biomass. Int. J. Hydrogen Energy 2017, 42, 27600–27606. [Google Scholar] [CrossRef]
- Azizi, N.; Najafpour, G.; Younesi, H. Acid Pretreatment and Enzymatic Saccharification of Brown Seaweed for Polyhydroxybutyrate (PHB) Production Using Cupriavidus necator. Int. J. Biol. Macromol. 2017, 101, 1029–1040. [Google Scholar] [CrossRef] [PubMed]
- Muhammad, M.; Aloui, H.; Khomlaem, C.; Hou, C.T.; Kim, B.S. Production of Polyhydroxyalkanoates and Carotenoids through Cultivation of Different Bacterial Strains Using Brown Algae Hydrolysate as a Carbon Source. Biocatal. Agric. Biotechnol. 2020, 30, 101852. [Google Scholar] [CrossRef]
- Romero-Vargas, A.; Fdez-Güelfo, L.A.; Blandino, A.; Díaz, M.J.; Díaz, A.B. Rugulopteryx okamurae: Effect of Hydrothermal Acid Pretreatment on the Saccharification Process. Bioresour. Technol. 2023, 388, 129721. [Google Scholar] [CrossRef] [PubMed]
- Romero-Vargas, A.; Fdez-Güelfo, L.A.; Blandino, A.; Romero-García, L.I.; Díaz, A.B. Rugulopteryx okamurae: Assessment of Its Potential as a Source of Monosaccharides for Obtaining Bio-Products. Chem. Eng. J. 2023, 468, 143578. [Google Scholar] [CrossRef]
- Gonçalves, C.; Rodriguez-Jasso, R.M.; Gomes, N.; Teixeira, J.A.; Belo, I. Adaptation of Dinitrosalicylic Acid Method to Microtiter Plates. Anal. Methods 2010, 2, 2046–2048. [Google Scholar] [CrossRef]
- Miller, G.L. Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal. Chem. 1959, 31, 426–428. [Google Scholar] [CrossRef]
- Simona, C.; Laura, L.; Francesco, V.; Marianna, V.; Cristina, M.G.; Barbara, T.; Mauro, M.; Simona, R. Effect of the Organic Loading Rate on the PHA-Storing Microbiome in Sequencing Batch Reactors Operated with Uncoupled Carbon and Nitrogen Feeding. Sci. Total Environ. 2022, 825, 153995. [Google Scholar] [CrossRef] [PubMed]
- Braunegg, G.; Sonnleitner, B.; Lafferty, R.M. A Rapid Gas Chromatographic Method for the Determination of Poly-β-Hydroxybutyric Acid in Microbial Biomass. Eur. J. Appl. Microbiol. Biotechnol. 1978, 6, 29–37. [Google Scholar] [CrossRef]
- Marzo, C.; Díaz, A.B.; Caro, I.; Blandino, A. Conversion of Exhausted Sugar Beet Pulp into Fermentable Sugars from a Biorefinery Approach. Foods 2020, 9, 1351. [Google Scholar] [CrossRef] [PubMed]
- Ahn, J.; Jho, E.H.; Nam, K. Effect of C/N Ratio on Polyhydroxyalkanoates (PHA) Accumulation by Cupriavidus necator and Its Implication on the Use of Rice Straw Hydrolysates. Environ. Eng. Res. 2015, 20, 246–253. [Google Scholar] [CrossRef]
- Fereidouni, M.; Younesi, H.; Daneshi, A.; Sharifzadeh, M. The Effect of Carbon Source Supplementation on the Production of Poly(3-Hydroxybutyrate-Co-3-Hydroxyvalerate) by Cupriavidus necator. Biotechnol. Appl. Biochem. 2011, 58, 203–211. [Google Scholar] [CrossRef] [PubMed]
- Morlino, M.S.; Serna García, R.; Savio, F.; Zampieri, G.; Morosinotto, T.; Treu, L.; Campanaro, S. Cupriavidus Necator as a Platform for Polyhydroxyalkanoate Production: An Overview of Strains, Metabolism, and Modeling Approaches. Biotechnol. Adv. 2023, 69, 108264. [Google Scholar] [CrossRef] [PubMed]
- Goff, M.; Ward, P.G.; O’Connor, K.E. Improvement of the Conversion of Polystyrene to Polyhydroxyalkanoate through the Manipulation of the Microbial Aspect of the Process: A Nitrogen Feeding Strategy for Bacterial Cells in a Stirred Tank Reactor. J. Biotechnol. 2007, 132, 283–286. [Google Scholar] [CrossRef] [PubMed]
- Arumugam, A.; Senthamizhan, S.G.; Ponnusami, V.; Sudalai, S. Production and Optimization of Polyhydroxyalkanoates from Non-Edible Calophyllum inophyllum Oil Using Cupriavidus necator. Int. J. Biol. Macromol. 2018, 112, 598–607. [Google Scholar] [CrossRef] [PubMed]
- Santolin, L.; Waldburger, S.; Neubauer, P.; Riedel, S.L. Substrate-Flexible Two-Stage Fed-Batch Cultivations for the Production of the PHA Copolymer P(HB-Co-HHx) with Cupriavidus necator Re2058/PCB113. Front. Bioeng. Biotechnol. 2021, 9, 623890. [Google Scholar] [CrossRef]
- González-Rojo, S.; Díez-Antolínez, R. Production of Polyhydroxyalkanoates as a Feasible Alternative for an Integrated Multiproduct Lignocellulosic Biorefinery. Bioresour. Technol. 2023, 386, 129493. [Google Scholar] [CrossRef]
- Sousa, B.V.; Silva, F.; Reis, M.A.M.; Lourenço, N.D. Monitoring Pilot-Scale Polyhydroxyalkanoate Production from Fruit Pulp Waste Using near-Infrared Spectroscopy. Biochem. Eng. J. 2021, 176, 108210. [Google Scholar] [CrossRef]
- Sudhakar, K.; Mamat, R.; Samykano, M.; Azmi, W.H.; Ishak, W.F.W.; Yusaf, T. An Overview of Marine Macroalgae as Bioresource. Renew. Sustain. Energy Rev. 2018, 91, 165–179. [Google Scholar] [CrossRef]
- Ganesh Saratale, R.; Cho, S.K.; Dattatraya Saratale, G.; Kadam, A.A.; Ghodake, G.S.; Kumar, M.; Naresh Bharagava, R.; Kumar, G.; Su Kim, D.; Mulla, S.I.; et al. A Comprehensive Overview and Recent Advances on Polyhydroxyalkanoates (PHA) Production Using Various Organic Waste Streams. Bioresour. Technol. 2021, 325, 124685. [Google Scholar] [CrossRef] [PubMed]
- Mogollón, S.L.; Zilio, M.I.; Buitrago, E.M.; Caraballo, M.Á.; Yñiguez, R. Economic Impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) along the Andalusian Coastline: The Case of Tarifa, Spain. Wetl. Ecol. Manag. 2024, 32, 19–32. [Google Scholar] [CrossRef]
Fermentation Medium | |||||
---|---|---|---|---|---|
C/N ratio | C10 | C20 | C30 | NPM | PM |
Experimental | 21:1 | 42:1 | 61:1 | 17:1 | 21:1 |
Theoretical | 19:1 | 38:1 | 57:1 | n/d | n/d |
CT (g/L) | C10 | C20 | C30 | NPM | PM |
Experimental | 3.75 | 7.65 | 11.13 | 11.07 | 9.50 |
Theoretical | 4.00 | 7.99 | 11.99 | n/d | n/d |
NT (g/L) | C10 | C20 | C30 | NPM | PM |
Experimental | 0.18 | 0.18 | 0.18 | 0.64 | 0.45 |
Theoretical | 0.21 | 0.21 | 0.21 | n/d | n/d |
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Romero-Vargas, A.; Fdez-Güelfo, L.A.; Blandino, A.; Díaz, A.B. Polyhydroxybutyrate Production from the Macroalga Rugulopteryx okamurae: Effect of Hydrothermal Acid Pretreatment. J. Mar. Sci. Eng. 2024, 12, 1228. https://doi.org/10.3390/jmse12071228
Romero-Vargas A, Fdez-Güelfo LA, Blandino A, Díaz AB. Polyhydroxybutyrate Production from the Macroalga Rugulopteryx okamurae: Effect of Hydrothermal Acid Pretreatment. Journal of Marine Science and Engineering. 2024; 12(7):1228. https://doi.org/10.3390/jmse12071228
Chicago/Turabian StyleRomero-Vargas, Agustín, Luis Alberto Fdez-Güelfo, Ana Blandino, and Ana Belén Díaz. 2024. "Polyhydroxybutyrate Production from the Macroalga Rugulopteryx okamurae: Effect of Hydrothermal Acid Pretreatment" Journal of Marine Science and Engineering 12, no. 7: 1228. https://doi.org/10.3390/jmse12071228