Exogenous Trehalose Improves Growth, Glycogen and Poly-3-Hydroxybutyrate (PHB) Contents in Photoautotrophically Grown Arthrospira platensis under Nitrogen Deprivation
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Bacterial Strain and Culture Conditions
2.2. Transcriptional Expression Study
2.3. Glycogen Synthase Activity Assay
2.4. PHA Synthase Activity Assay
2.5. Glycogen Extraction and Quantitative Analysis
2.6. PHB Extraction and Quantitative Analysis
2.7. Fourier Transform Infrared (FTIR) Spectroscopy
2.8. 1H- NMR and 13C-NMR Analysis
2.9. Statistical Analysis
3. Results
3.1. Effects of Exogenous Trehalose (Tre) on Biomass and Chlorophyll-a Contents under Nitrogen Deprivation
3.2. Effects of Exogenous Trehalose (Tre) on Glycogen and PHB Contents under Nitrogen Deprivation
3.3. Effects of Exogenous Trehalose (Tre) on the Expression of glgA and phaC Genes under Nitrogen Deprivation
3.4. Effects of Exogenous Trehalose (Tre) on Glycogen Synthase and PHA Synthase under Nitrogen Deprivation
3.5. Fourier Transform Infrared Spectroscopy Analysis
3.6. NMR Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Elbein, A.D.; Pan, Y.T.; Pastuszak, I.; Carroll, D. New insights on trehalose: A multifunctional molecule. Glycobiology 2003, 13, 17R–27R. [Google Scholar] [CrossRef]
- Paul, M.J.; Primavesi, L.F.; Jhurreea, D.; Zhang, Y. Trehalose metabolism and signaling. Annu. Rev. Plant Biol. 2008, 59, 417–441. [Google Scholar] [CrossRef]
- Lin, Y.; Zhang, J.; Gao, W.; Chen, Y.; Li, H.; Lawlor, D.W.; Paul, M.J.; Pan, W. Exogenous trehalose improves growth under limiting nitrogen through upregulation of nitrogen metabolism. BMC Plant Biol. 2017, 17, 247. [Google Scholar] [CrossRef] [PubMed]
- Wu, S.; He, L.; Shen, R.; Zhang, X.; Wang, Q. Molecular cloning of maltooligosyltrehalose trehalohydrolase gene from Nostoc flagelliforme and trehalose-related response to stresses. J. Microbiol. Biotechnol. 2011, 21, 830–837. [Google Scholar] [CrossRef] [PubMed]
- Sakamoto, T.; Yoshida, T.; Arima, H.; Hatanaka, Y.; Takani, Y.; Tamaru, Y. Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc commune. Phycol. Res. 2009, 57, 66–73. [Google Scholar] [CrossRef]
- Hershkovitz, N.; Oren, A.; Cohen, Y. Accumulation of trehalose and sucrose in cyanobacteria exposed to matric water stress. Appl. Environ. Microbiol. 1991, 57, 645–648. [Google Scholar] [CrossRef] [PubMed]
- Higo, A.; Katoh, H.; Ohmori, K.; Ikeuchi, M.; Ohmori, M. The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 2006, 152, 979–987. [Google Scholar] [CrossRef]
- Hagemann, M. Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol. Rev. 2011, 35, 87–123. [Google Scholar] [CrossRef]
- Ohmori, K.; Ehira, S.; Kimura, S.; Ohmori, M. Changes in the amount of cellular trehalose, the activity of maltooligosyl trehalose hydrolase, and the expression of its gene in response to salt stress in the cyanobacterium Spirulina platensis. Microbes Environ. 2009, 24, 52–56. [Google Scholar] [CrossRef]
- Duangsri, C.; Mudtham, N.-A.; Incharoensakdi, A.; Raksajit, W. Enhanced polyhydroxybutyrate (PHB) accumulation in heterotrophically grown Arthrospira platensis under nitrogen deprivation. J. Appl. Phycol. 2020, 32, 3645–3654. [Google Scholar] [CrossRef]
- Kaewbai-ngam, A.; Incharoensakdi, A.; Monshupanee, T. Increased accumulation of polyhydroxybutyrate in divergent cyanobacteria under nutrient-deprived photoautotrophy: An efficient conversion of solar energy and carbon dioxide to polyhydroxybutyrate by Calothrix scytonemicola TISTR 8095. Bioresour. Technol. 2016, 212, 342–347. [Google Scholar] [CrossRef]
- Drosg, B.; Fritz, I.; Gattermayr, F.; Silvestrini, L. Photo-autotrophic production of poly(hydroxyalkanoates) in cyanobacteria. Chem. Biochem. Eng. Q. 2015, 29, 145–156. [Google Scholar] [CrossRef]
- Monshupanee, T.; Incharoensakdi, A. Enhanced accumulation of glycogen, lipids and polyhydroxybutyrate under optimal nutrients and light intensities in the cyanobacterium Synechocystis sp. PCC 6803. J. Appl. Microbiol. 2014, 116, 830–838. [Google Scholar] [CrossRef]
- Delrue, F.; Alaux, E.; Moudjaoui, L.; Gaignard, C.; Fleury, G.; Perilhou, A.; Richaud, P.; Petitjean, M.; Sassi, J.-F. Optimization of Arthrospira platensis (Spirulina) growth: From laboratory scale to pilot scale. Fermentation 2017, 3, 59. [Google Scholar] [CrossRef]
- Shimamatsu, H. Mass production of Spirulina, an edible microalga. Hydrobiologia 2004, 512, 39–44. [Google Scholar] [CrossRef]
- de Morais, M.G.; Stillings, C.; Dersch, R.; Rudisile, M.; Pranke, P.; Costa, J.A.V.; Wendorff, J. Biofunctionalized nanofibers using Arthrospira (Spirulina) biomass and biopolymer. BioMed Res. Int. 2015, 2015, 967814. [Google Scholar] [CrossRef] [PubMed]
- Aikawa, S.; Izumi, Y.; Matsuda, F.; Hasunuma, T.; Chang, J.-S.; Kondo, A. Synergistic enhancement of glycogen production in Arthrospira platensis by optimization of light intensity and nitrate supply. Bioresour. Technol. 2012, 108, 211–215. [Google Scholar] [CrossRef]
- Sirohi, R.; Prakash Pandey, J.; Kumar Gaur, V.; Gnansounou, E.; Sindhu, R. Critical overview of biomass feedstocks as sustainable substrates for the production of polyhydroxybutyrate (PHB). Bioresour. Technol. 2020, 311, 123536. [Google Scholar] [CrossRef] [PubMed]
- Novo, M.T.; Beltran, G.; Rozès, N.; Guillamón, J.M.; Mas, A. Effect of nitrogen limitation and surplus upon trehalose metabolism in wine yeast. Appl. Microbiol. Biotechnol. 2005, 66, 560–566. [Google Scholar] [CrossRef] [PubMed]
- Meeks, J.C.; Castenholz, R.W. Growth and photosynthesis in an extreme thermophile, Synechococcus lividus (Cyanophyta). Archiv. Mikrobiol. 1971, 78, 25–41. [Google Scholar] [CrossRef] [PubMed]
- Díaz-Lobo, M.; Garcia-Amorós, J.; Fita, I.; Velasco, D.; Guinovart, J.J.; Ferrer, J.C. Selective photoregulation of the activity of glycogen synthase and glycogen phosphorylase, two key enzymes in glycogen metabolism. Org. Biomol. Chem. 2015, 13, 7282–7288. [Google Scholar] [CrossRef]
- Chek, M.F.; Kim, S.-Y.; Mori, T.; Tan, H.T.; Sudesh, K.; Hakoshima, T. Asymmetric open-closed dimer mechanism of polyhydroxyalkanoate synthase PhaC. Iscience 2020, 23, 101084. [Google Scholar] [CrossRef]
- Hasunuma, T.; Kikuyama, F.; Matsuda, M.; Aikawa, S.; Izumi, Y.; Kondo, A. Dynamic metabolic profiling of cyanobacterial glycogen biosynthesis under conditions of nitrate depletion. J. Exp. Bot. 2013, 64, 2943–2954. [Google Scholar] [CrossRef]
- Keshari, N.; Gugger, M.; Zhu, T.; Lu, X. Compatible solutes profiling and carbohydrate feedstock from diversified cyanobacteria. Algal Res. 2019, 43, 101637. [Google Scholar] [CrossRef]
- Pade, N.; Compaoré, J.; Klähn, S.; Stal, L.J.; Hagemann, M. The marine cyanobacterium Crocosphaera watsonii WH8501 synthesizes the compatible solute trehalose by a laterally acquired OtsAB fusion protein. Environ. Microbiol. 2012, 14, 1261–1271. [Google Scholar] [CrossRef]
- Yoshida, T.; Sakamoto, T. Water-stress induced trehalose accumulation and control of trehalase in the cyanobacterium Nostoc punctiforme IAM M-15. J. Gen. Appl. Microbiol. 2009, 55, 135–145. [Google Scholar] [CrossRef]
- Li, L.; Chen, X.; Huang, Y.; Shen, Y.; Liu, S.; Lu, J.; Hu, J.; You, W. The salt tolerance of the freshwater cyanobacterium Microcystis depends on nitrogen availability. Sci. Total Environ. 2021, 777, 146186. [Google Scholar] [CrossRef]
- Hickman, J.W.; Kotovic, K.M.; Miller, C.; Warrener, P.; Kaiser, B.; Jurista, T.; Budde, M.; Cross, F.; Roberts, J.M.; Carleton, M. Glycogen synthesis is a required component of the nitrogen stress response in Synechococcus elongatus PCC 7942. Algal Res. 2013, 2, 98–106. [Google Scholar] [CrossRef]
- Phélippé, M.; Gonçalves, O.; Thouand, G.; Cogne, G.; Laroche, C. Characterization of the polysaccharides chemical diversity of the cyanobacteria Arthrospira platensis. Algal Res. 2019, 38, 101426. [Google Scholar] [CrossRef]
- Chentir, I.; Doumandji, A.; Ammar, J.; Zili, F.; Jridi, M.; Markou, G.; Ben Ouada, H. Induced change in Arthrospira sp. (Spirulina) intracellular and extracellular metabolites using multifactor stress combination approach. J. Appl. Phycol. 2018, 30, 1563–1574. [Google Scholar] [CrossRef]
- Sharma, L.; Mallick, N. Accumulation of poly-β-hydroxybutyrate in Nostoc muscorum: Regulation by pH, light-dark cycles, N and P status and carbon sources. Bioresour. Technol. 2005, 96, 1304–1310. [Google Scholar] [CrossRef]
- Satchasataporn, K.; Duangsri, C.; Charunchaipipat, W.; Laloknam, S.; Burut-Archanai, S.; Powtongsook, S.; Akrimajirachoote, N.; Raksajit, W. Enhanced production of poly-3-hydroxybutyrate and carotenoids by Arthrospira platensis under combined glycerol and phosphorus supplementation. ScienceAsia 2022, 48, 509–517. [Google Scholar] [CrossRef]
- Kettner, A.; Noll, M.; Griehl, C. Leptolyngbya sp. NIVA-CYA 255, a promising candidate for poly(3-hydroxybutyrate) production under mixotrophic deficiency conditions. Biomolecules 2022, 12, 504. [Google Scholar] [CrossRef]
- de Morais, E.G.; Druzian, J.I.; Nunes, I.L.; de Morais, M.G.; Costa, J.A.V. Glycerol increases growth, protein production and alters the fatty acids profile of Spirulina (Arthrospira) sp. LEB 18. Process Biochem. 2019, 76, 40–45. [Google Scholar] [CrossRef]
- Joseph, A.; Aikawa, S.; Sasaki, K.; Teramura, H.; Hasunuma, T.; Matsuda, F.; Osanai, T.; Hirai, M.Y.; Kondo, A. Rre37 stimulates accumulation of 2-oxoglutarate and glycogen under nitrogen starvation in Synechocystis sp. PCC 6803. FEBS Lett. 2014, 588, 466–471. [Google Scholar] [CrossRef]
- Gordon, G.C.; Pfleger, B.F. Regulatory tools for controlling gene expression in cyanobacteria. In Synthetic Biology of Cyanobacteria; Zhang, W., Song, X., Eds.; Advances in Experimental Medicine and Biology; Springer: Singapore, 2018; Volume 1080, pp. 281–315. [Google Scholar]
- Hauf, W.; Schlebusch, M.; Hüge, J.; Kopka, J.; Hagemann, M.; Forchhammer, K. Metabolic changes in Synechocystis PCC 6803 upon nitrogen-starvation: Excess NADPH sustains polyhydroxybutyrate accumulation. Metabolites 2013, 3, 101–118. [Google Scholar] [CrossRef]
- Duangsri, C.; Salminen, T.A.; Alix, M.; Kaewmongkol, S.; Akrimajirachoote, N.; Khetkorn, W.; Jittapalapong, S.; Mäenpää, P.; Incharoensakdi, A.; Raksajit, W. Characterization and homology modeling of catalytically active recombinant PhaCAp Protein from Arthrospira platensis. Biology 2023, 12, 751. [Google Scholar] [CrossRef]
- Naknean, P.; Meenune, M. Factors affecting retention and release of flavour compounds in food carbohydrates. Int. Food Res. J. 2010, 17, 23–34. [Google Scholar]
- Wiercigroch, E.; Szafraniec, E.; Czamara, K.; Pacia, M.Z.; Majzner, K.; Kochan, K.; Kaczor, A.; Baranska, M.; Malek, K. Raman and infrared spectroscopy of carbohydrates: A review. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2017, 185, 317–335. [Google Scholar] [CrossRef]
- Nikonenko, N.A.; Buslov, D.K.; Sushko, N.I.; Zhbankov, R.G. Investigation of stretching vibrations of glycosidic linkages in disaccharides and polysaccharides with use of IR spectra deconvolution. Biopolymers 2000, 57, 257–262. [Google Scholar] [CrossRef]
- Nur, M.M.A.; Achmad, Z.; Jaya, D.; Setyoningrum, T.M.; Widayati, T.W.; Kholisoh, S.D.; Djarot, I.N. Screening and optimization of cyanobacteria cultivated on palm oil mill effluent (POME) to produce polyhydroxybutyrate. J. Appl. Phycol. 2023, 35, 1213–1221. [Google Scholar] [CrossRef]
- Ansari, S.; Fatma, T. Cyanobacterial polyhydroxybutyrate (PHB): Screening, optimization and characterization. PLoS ONE 2016, 11, e0158168. [Google Scholar] [CrossRef] [PubMed]
- Bhati, R.; Samantaray, S.; Sharma, L.; Mallick, N. Poly-β-hydroxybutyrate accumulation in cyanobacteria under photoautotrophy. Biotechnol. J. 2010, 5, 1181–1185. [Google Scholar] [CrossRef] [PubMed]
- Simonazzi, M.; Pezzolesi, L.; Galletti, P.; Gualandi, C.; Pistocchi, R.; De Marco, N.; Paganelli, Z.; Samorì, C. Production of polyhydroxybutyrate by the cyanobacterium cf. Anabaena sp. Int. J. Biol. Macromol. 2021, 191, 92–99. [Google Scholar] [CrossRef]
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Mudtham, N.-A.; Promariya, A.; Duangsri, C.; Maneeruttanarungroj, C.; Ngamkala, S.; Akrimajirachoote, N.; Powtongsook, S.; Salminen, T.A.; Raksajit, W. Exogenous Trehalose Improves Growth, Glycogen and Poly-3-Hydroxybutyrate (PHB) Contents in Photoautotrophically Grown Arthrospira platensis under Nitrogen Deprivation. Biology 2024, 13, 127. https://doi.org/10.3390/biology13020127
Mudtham N-A, Promariya A, Duangsri C, Maneeruttanarungroj C, Ngamkala S, Akrimajirachoote N, Powtongsook S, Salminen TA, Raksajit W. Exogenous Trehalose Improves Growth, Glycogen and Poly-3-Hydroxybutyrate (PHB) Contents in Photoautotrophically Grown Arthrospira platensis under Nitrogen Deprivation. Biology. 2024; 13(2):127. https://doi.org/10.3390/biology13020127
Chicago/Turabian StyleMudtham, Nat-Anong, Authen Promariya, Chanchanok Duangsri, Cherdsak Maneeruttanarungroj, Suchanit Ngamkala, Nattaphong Akrimajirachoote, Sorawit Powtongsook, Tiina A. Salminen, and Wuttinun Raksajit. 2024. "Exogenous Trehalose Improves Growth, Glycogen and Poly-3-Hydroxybutyrate (PHB) Contents in Photoautotrophically Grown Arthrospira platensis under Nitrogen Deprivation" Biology 13, no. 2: 127. https://doi.org/10.3390/biology13020127
APA StyleMudtham, N. -A., Promariya, A., Duangsri, C., Maneeruttanarungroj, C., Ngamkala, S., Akrimajirachoote, N., Powtongsook, S., Salminen, T. A., & Raksajit, W. (2024). Exogenous Trehalose Improves Growth, Glycogen and Poly-3-Hydroxybutyrate (PHB) Contents in Photoautotrophically Grown Arthrospira platensis under Nitrogen Deprivation. Biology, 13(2), 127. https://doi.org/10.3390/biology13020127