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mixotrophy in cyanobacteria: a dual nutritional strategy
- 1. CCS Haryana Agricultural University Agriculture is Mixotrophy in Cyanobacteria Mansi Ph.D. Scholar 2022BS23D Credit seminar 692
- 2. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 2 1. Cyanobacteria and their types 2. Cell structure and reproductive mode 3. Photoautotrophy vs heterotrophy 4. Mixotrophy: a dual mode of nutrition 5. Mechanism of mixotrophy 6. Factors affecting mixotrophy in cyanobacteria 7. Biotechnological applications of mixotrophic cyanobacteria 8. Current understanding and future directions 9. Conclusion Flow of content
- 3. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Cyanobacteria? 3 Nostoc sp. Oscillotoria sp. Spirulina sp. Gleotrichia sp. Anaebina sp. • Cyanobacteria are Gram negative, aerobic, photoautotrophic prokaryotes having size ranges from 1-10µm • Originated over 2.5 billion years ago and are believed to be one of the first organisms to perform oxygenic photosynthesis • Ubiquitous in existence and often found in all types of environment- freshwater, marine water, moist rock, etc. • Capable of nitrogen-fixation and carbon sequestration • Uses chlorophyll- based light harvesting complex • Chlorophyll a, phycocyanin and phycoerythrin are the photosynthetic pigments present in cyanobacteria • Keep ‘Cyanophycean starch’ as reserves food material • Known to releases oxygen and uses water as electron-donor i.e. splits water molecule to release oxygen
- 4. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 4 Single-celled, having mucilaginous sheath Examples: Chroococcus sp. Single cell colonizes and form multicellular colonies Examples: Gleocapsa sp. Form chain covered with mucilaginous sheath. It consists of: Heterocyst and Akinetes Examples: Nostoc sp., Oscillatoria sp. etc. Filamentous Colonial Unicellular Types of cyanobacteria
- 5. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 5 Norena-Caro & Benton (2018) Fig 1. Cell structure of cyanobacteria
- 6. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 6 6 Vegetative reproduction Asexual reproduction Binary fission Fragmentation Hormogones Formation of separator disc Exospores Endospores Akinetes Hormocyst Hormospores Vegetative cell Constriction Cell enlargement and formation of “constriction” Two identical individuals Hormogonia Mucilaginous sheath Gelatinous material occupies between the cell Thick wall Hormospores Heterocyst covered by thick wall Germination Growth of new individual Akinete Endospores Exospores Fig 2. Reproductive modes in cyanobacteria
- 7. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 7 O2 + 2NADPH + 3ATP Light-dependent reactions 2H2O + 2NADP+ + 3ADP + 3Pi O2 + 2NADPH + 3ATP Light-independent reactions (Calvin cycle) 3CO2 + 9ATP + 6NADPH + 6H+ G3P + 9ADP + 8Pi + 6NADP+ + 3H2O Romanowska & Dębowska (2022) Fig 3. Photoautotrophy vs heterotrophy
- 8. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 8 Fig 4. Photosynthesis in cyanobacteria Selão et al. (2020)
- 9. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Mixotrophy: A dual mode of nutrition 9 • Mixotrophy refers to the ability of cyanobacteria to obtain energy and nutrients through both photosynthesis and heterotrophic means, e.g. absorbing organic compounds from environment in the presence of light • Also includes the acquisition of molecules containing nitrogen, phosphorus, trace elements, vitamins and high-energy compounds • Provides competitive advantage, enhancing their adaptability and survival in dynamic ecosystems • Mixotrophic cyanobacteria play crucial roles in aquatic and terrestrial ecosystems by contributing to primary production, nutrient cycling and ecosystem stability
- 10. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Mechanism of mixotrophy 10 There are several strategies that make phototrophs adapt various environmental conditions, such as, • Morphological adaptations that provide long term viability during low light periods including precipitation of calcium carbonate crystals in cell membrane, glycans, UV-absorbing pigments and water stress proteins in extracellular matrix. e.g., Scytonema sp. • Modifications in photosynthetic apparatus • Changes in the quantity of pigments and associated pigment forming proteins to increase proton capture efficiency in low light • Physiological adaptations and the entire set of enzymes involved in the Oxidative Pentose Phosphate pathway (OPP), glycolysis and Calvin cycle • Presence of membrane transporters of simple organic compounds • glcH: encodes for high affinity glucose transporter • proX: encodes for glucine-betaine transporter • pmgA: encoding a putative regulatory protein (controls carbon partitioning between the Calvin cycle and OPP pathway)
- 11. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 11 Fig 5. Changes in enzymes involved in glucose metabolism in Synechococcus sp. strain WH8102 under light and dark conditions. The strategies utilized by cyanobacteria to metabolize organic compound such as glucose, shows unexpected links to other pathways. (Moreno-Cabezuelo et al. 2023) Metabolic flow upon glucose addition
- 12. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Table 1: Examples of mixotrophic cyanobacteria 12 Cyanobacteria General characteristics Gloeobacter violaceus Performs both photosynthesis and utilize organic carbon sources when available Synechococcus elongatus Capable of utilizing organic carbon sources such as glucose in addition to photosynthesis Anabaena variabilis Ability to fix atmospheric nitrogen and utilize organic carbon sources also Cyanothece spp. Utilizes organic carbon sources in addition to photosynthesis, particularly in low light conditions Chlorogloea fritschii Utilizes organic carbon sources in addition to photosynthesis Spirulina subsalsa Primarily relies on photosynthesis, under certain conditions it has been observed to exhibit mixotrophic behavior, utilizing organic carbon sources for growth Aulosira fertilissima Utilizes both organic carbon sources and photosynthesis for growth
- 13. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 13 Carbon Dioxide Concentration pH Temperature Nutrient Availability (Nitrogen, Phosphorus and Organic Carbon Sources) Light Availability (Light Intensity and Light Quality) Environmental factors affecting mixotrophic cyanobacteria
- 14. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Applications of mixotrophic cyanobacteria 14 Fig 6. Potential applications of cyanobacterial biomass Vu et al. (2020)
- 15. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 15 Waste water Bioremediation Low cost inputs, limited maintenance & eco- friendly Mixotrophic nature Nitrogen fixation, plant growth promotion, soil stability & highly efficient By products Easy biomass separation Cyanobacteria Liquid fuel & bio-methane High value products High cost inputs, regular maintenance & cause toxicity Heterotrophic nature Release toxic gases, causes anaerobic conditions & less efficient By products Typical biomass separation Other microbes Singh et al. (2019) Fig 7. Advantages of cyanobacteria over other microbes in wastewater treatment
- 16. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 16 Fig 8. Conceptual model for cyanobacterial mediated remediation of heavy metals (a) Adsorption by extracellular cell associated materials (b) Absorption and accumulation inside the cell Singh et al. (2019)
- 17. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Table 2: Cyanoremediation of heavy metals 17 Heavy metal Cyanobacteria References Cd Nostoc linckia, Nostoc rivularis, Tolypothrix tenuis El-Enany and Issa (2000) Co Nostoc muscorum, Anabaena subcylindrica EI-Sheekh et al. (2012) Cr Nostoc calcicole, Chroococus sp. Anjana et al. (2007) Cu Nostoc muscorum, Anabaena subcylindrica EI-Sheekh et al. (2012) Mn Nostoc muscorum, Anabaena subcylindrica EI-Sheekh et al. (2012) Pb Nostoc muscorum, Anabaena subcylindrica, Gloeocapsa sp. EI-Sheekh et al. (2012) Zn Nostoc linckia, Nostoc rivularis El-Enany and Issa (2000) Ni Nostoc sp. EI-Sheekh et al. (2012) Singh et al. (2019)
- 18. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Elham Ghorbani, Bahareh Nowruzi, Masoumeh Nezhadali and Azadeh Hekmat 18 BMC Microbiology, 2022 Highlights: 1.Comparing Nostoc sp. N27P72 and Nostoc sp. FB71, maltose supplementation significantly boosts EPS production and cell dry weight, with Nostoc sp. N27P72 showing notably high levels 2.The cultures, assessed for Cu (II), Cr (III) and Ni (II) removal, demonstrate enhanced metal absorption with maltose as a carbon source, potentially due to increased EPS, protein and carbohydrate production 3.Gas Chromatography-Mass Spectrometry (GC–MS) analysis of Nostoc sp. N27P72 reveals a strong Ni (II) removal capacity Metal removal capability of two cyanobacterial species in autotrophic and mixotrophic mode of nutrition
- 19. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Methodology 19 Collection of Nostoc sp. (N27P72 and FB71) Growth of culture on BG11 medium + maltose, lactose, sucrose, glucose (10g/L) separately Determination of cell biomass after 6, 12, 24, 36 and 48 h Isolation of exopolysaccharides Heavy metal removal (Cu (II), Cr (III) and Ni (II)), total EPS, total soluble proteins, carbohydrate content, chemical composition of solution were analyzed
- 20. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 20 Fig 9. EPS production and cell dry weight of Nostoc sp. N27P72 cultivated in media culture (A) without additional sugars as a control (B) media culture containing (10 g/L) maltose (C) lactose (D) sucrose (E) Glucose Results Symbols indicate ● Cell dry weight (g/L) ■ Total EPS concentration (μg/mL) ▲ Sugar concentration (g/L) in the media
- 21. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 21 Fig 10. EPS production and cell dry weight of Nostoc sp. FB71 cultivated in media culture without additional sugars as (A) control (B) media culture containing (10 g/L) maltose (C) lactose (D) sucrose (E) Glucose Symbols indicate ● Cell dry weight (g/L) ■ Total EPS concentration (μg/mL) ▲ Sugar concentration (g/L) in the media
- 22. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 22 Fig 11. Time course of specific metal removal (q) by (A) Nostoc sp. N27P72 (B) Nostoc sp. FB71 cultivated in media culture containing (10 g/L) maltose, with copper, chromium and nickel (10 mg/L) in single-metal solutions
- 23. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 23 Fig 12. Comparison of the total produced (a) EPSs (μg/mL), (b) Protein (mg/mL) and (c) Carbohydrates (μg/mL) of Nostoc sp. N27P72 and Nostoc sp. FB71 in lyophilized EPSs containing maltose and metal solution of Cu (II), Cr (III) and Ni (II)
- 24. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Table 3: Chemical composition of Nostoc sp. N27P72 (control) extracts as revealed by Gas Chromatography Mass Spectrophotometry (GC–MS) 24 Name of Compound Molecular Formula Molecular weight Nature of the compound RT (Mins) Area % 2-Ethoxyethanol C4H10O2 90.12 Hydroxy ether 8.77 83% Phenol, 2,4-bis-(1,1- dimethylethyl) C17H30OSi 278.5 Phenolic ester 26.29 96% Dodecane, 2,6,10-trimethyl C15H32 212.41 Alkane 26.41 64% 3,3-dimethylhexane C8H18 114.23 Alkane 27.15 40% Undecane C11H24 156.31 Alkane 28 78% Hydroxylamine, O-decyl C10H23 173.2957 Alkane 29.75 78% Tetradecane C14H30 198.39 Alkane 29.95 59% Nonadecane C19H40 268.5 Alkane hydrocarbon 30.20 83% Propionic acid CH3CH2CO2H 74.08 Organic acid 30.66 35% Dotriacontane C32H66 450.8664 Alkane 30.68 64% Eicosane C20H42 282.5 Alkane 31.69 83% 2-Methyldecane C11H24 156.31 Alkane 31.99 53%
- 25. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Table 4: Chemical composition of Nostoc sp. N27P72 (Ni(II)) extracts as revealed by Gas Chromatography Mass Spectrophotometry (GC–MS) 25 Name of Compound Molecular Formula Molecular weight Nature of the compound RT Area % Pyran C5H6O 82.1 Six-membered heterocyclic 11.55 49% Cyclotrisiloxane H6O3Si3 138.3 Heterocyclic compound 12.02 90% Cyclotrisiloxane H6O3Si3 138.3 Heterocyclic compound 15.97 91% Cyclotrisiloxane H6O3Si3 138.3 Heterocyclic compound 19.62 91% Cyclotrisiloxane H6O3Si3 138.3 Heterocyclic compound 23.22 91% 1,2-Benzenedicarboxylic acid C8H6O4 166.1308 Quinoline Ester 23.51 90% 1,2-Benzenedicarboxylic acid C8H6O4 166.1308 Quinoline Ester 24.01 91% 1,2-Benzenedicarboxylic acid C8H6O4 166.1308 Quinoline Ester 24.13 91% 1,2-Benzenedicarboxylic acid C8H6O4 166.1308 Quinoline Ester 24.35 91% 1,2-Benzenedicarboxylic acid C8H6O4 166.1308 Quinoline Ester 24.55 91% 1,2-Benzenedicarboxylic acid C8H6O4 166.1308 Quinoline Ester 24.63 91%
- 26. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Enhancing biodiesel production in Anabaena sphaerica MBDU 105: exploring photo-, hetero- and mixotrophic cultivation for biomass, lipid and fuel properties Antonyraj Matharasi Perianaika Anahas, Nainangu Prasannabalaji and Gangatharan Muralitharan Highlights: • High lipid-yielding strain Anabaena sphaerica MBDU 105 evidenced appropriateness for biodiesel production was selected to uplift biomass and lipid production under three different modes • Biomass production, lipid yield, pigment, biomolecules and fuel quality were studied • Exogenous addition of glucose in media significantly increased biomass productivity by 8.6 times and 5.6 times in mixotrophic compared to photoautotrophic and heterotrophic modes, respectively • Mixotrophic cultivation of Anabaena 105 resulted in the highest lipid productivity of 31.64 mg/L/day and lipid content of 39.21% dwt, with a maximum palmitic acid concentration of 59.88–76.25% suitable for biodiesel production • Study demonstrates that mixotrophic cultivation, utilizing glucose, can enhance lipid content, fuel quality and economic viability of biodiesel, including high cetane numbers, low unsaturation and excellent lubricity, contributing to efficient engine performance and reduced emissions 26 Biomass Conversion and Bioenergy, 2024
- 27. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Methodology 27 Anabaena sphaerica MBDU 105 was cultivated @5% with BG-11 medium under three different modes Measurement of growth rate and biomass productivity Effect of glucose on pigments under different modes were analyzed Biochemical analysis of total protein, total lipid content and fatty acid analysis Biodiesel quality was estimated
- 28. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 28 Fig 13. Specific growth rate of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions Results
- 29. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 29 Fig 14. Chlorophyll a synthesis of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions 3.383 mg/g 0.713 mg/g 0.658 mg/g
- 30. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 30 Fig 15. Carotenoid productivity of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions 0.0012 mg/g 0.00026 mg/g
- 31. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 31 Fig 16. Phycocyanin production of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions 0.022 mg/g 0.015 mg/g
- 32. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 32 Fig 17. Total protein content of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions 0.039 mg/g 0.045 mg/g
- 33. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 33 Fig 18. Effect of organic carbon source on saturated fatty acids (SFA), monounsaturated fatty acids (MUFA) and polyunsaturated fatty acids (PUFA) concentration in Anabaena 105
- 34. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Table 5: Effect of glucose on the relative percentage of FAME (% w/w) of the total FAME composition of Anabaena 105 grown under the photoautotrophic and mixotrophic mode 34 Fatty acids Fatty acid composition (% w/w) Mixotrophic mode Photoautotrophic mode BG-11 Glucose (1 g/L) Glucose (2 g/L) Glucose (3 g/L) Glucose (4 g/L) Glucose (5 g/L) Glucose (6 g/L) (Control) Palmitic acid 59.886 62.532 64.311 66.048 73.027 76.252 25.23 Palmitoleic acid 0.463 0.553 0.308 0.493 0.305 0.640 0.72 Stearic acid 0.132 0.112 0.952 1.538 2.894 0.707 0.89 Oleic acid 0.300 0.314 0.175 0.166 1.232 0.203 0.79
- 35. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 35 Cyanobacterial strains+BG-11 Cetane Number Iodine Value (g /biodiesel 100g ) Cold Filter Plugging Point (°C) Cloud Point (°C) Viscosity (mm2/s) Density (g m-3) Oxidation stability Biodiesel Standard IS 15607 ≥ 51 ≤120 ≤5/-20 3.0-12 3.5–5.0 0.86–0.90 ≥ 6 Photoautotrophic mode 62.85 32.51 5.76 8.28 2.89 0.88 5.69 Mixotrophic mode Glucose (1 g/L) 59.35 54.97 5.82 27.89 4.06 0.88 5.98 Glucose (2 g/L) 61.93 44.6 15.86 28.8a3 3.44 0.88 6.75 Glucose (3 g/L) 62.06 37.81 22.08 29.74 3.44 0.87 6.85 Glucose (4 g/L) 62.93 38.52 50.86 33.42 4.49 0.88 7.27 Glucose (5 g/L) 66.33 20.93 42.55 35.11 4.06 0.86 6.73 Glucose (6 g/L) 66.18 25.48 5.75 8.27 3.63 0.88 6.58 Table 6: Biodiesel properties of Anabaena 105 grown under the photoautotrophic and mixotrophic mode of cultivation
- 36. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth 36 Current understanding and future directions
- 39. CCS Haryana Agricultural University Agriculture is supreme wealth Everything else can wait, agriculture can’t. -Norman Borlaug Thank you CCSHAU is a member of the ICAR
- 40. CCS Haryana Agricultural University, Hisar Agriculture is supreme wealth Bibliography • Anahas, A. M. P., Prasannabalaji, N., & Muralitharan, G. (2024). Enhancing biodiesel production in Anabaena sphaerica MBDU 105: exploring photo-, hetero-, and mixotrophic cultivation for biomass, lipid, and fuel properties. Biomass Conversion and Biorefinery, 1-20. • del Carmen Muñoz-Marín, M., López-Lozano, A., Moreno-Cabezuelo, J. Á., Díez, J., & García-Fernández, J. M. (2024). Mixotrophy in cyanobacteria. Current Opinion in Microbiology, 78, 102432. • Ghorbani, E., Nowruzi, B., Nezhadali, M., & Hekmat, A. (2022). Metal removal capability of two cyanobacterial species in autotrophic and mixotrophic mode of nutrition. BMC microbiology, 22(1), 58. • Kim, S. M., Bae, E. H., Kim, J. Y., Kang, J. S., & Choi, Y. E. (2022). Mixotrophic Cultivation of a Native Cyanobacterium, Pseudanabaena mucicola GO0704, to Produce Phycobiliprotein and Biodiesel. Journal of microbiology and biotechnology, 32(10), 1325. • Moreno-Cabezuelo, J. Á., Gómez-Baena, G., Díez, J., & García-Fernández, J. M. (2023). Integrated Proteomic and Metabolomic Analyses Show Differential Effects of Glucose Availability in Marine Synechococcus and Prochlorococcus. Microbiology Spectrum, 11(2), e03275-22. • Norena-Caro, D., & Benton, M. G. (2018). Cyanobacteria as photoautotrophic biofactories of high-value chemicals. Journal of CO2 Utilization, 28, 335-366. • Romanowska, E., & Wasilewska-Dębowska, W. (2022). Light-Dependent Reactions of Photosynthesis in Mesophyll and Bundle Sheath Chloroplasts of C4 Plant Maize. How Our Views Have Changed in Recent Years. Acta Societatis Botanicorum Poloniae, 91. • Selão, T. T., Jebarani, J., Ismail, N. A., Norling, B., & Nixon, P. J. (2020). Enhanced production of D-lactate in cyanobacteria by re-routing photosynthetic cyclic and pseudo-cyclic electron flow. Frontiers in plant science, 10, 498215. • Singh, J. S., Kumar, A., & Singh, M. (2019). Cyanobacteria: a sustainable and commercial bio-resource in production of bio-fertilizer and bio-fuel from waste waters. Environmental and Sustainability Indicators, 3, 100008. • Stebegg, R., Schmetterer, G., & Rompel, A. (2023). Heterotrophy among cyanobacteria. ACS omega, 8(37), 33098-33114. • Vu, H. P., Nguyen, L. N., Zdarta, J., Nga, T. T., & Nghiem, L. D. (2020). Blue-green algae in surface water: problems and opportunities. Current pollution reports, 6, 105-122. 40
Editor's Notes
- Function: protects cells from drying and helps in gliding Sheath is often colored :- Red: acidic; Blue: basic; Yellow /brown: high salt Heterocyst: thick walled cell, hollow, larger than vegetative cell, provides anaerobic environment for N fixation, photosynthetically inactive, formation of heterocyst triggered by molybdenum and low nitrogen
- Binary fission: In this type, a constriction forms between the cells that lead to the cell enlargement and exchange of the chromosomal material. At last, the cell produces two identical daughter cells. Fragmentation: During unfavourable conditions, thallus detaches to form a new thallus in the fragmentation method. By the formation of separator disc: Sometimes gelatinous material occupies between the cell, which acts as a separator disc. This disc then separates the cell, which later produces new vegetative cells. By hormogones: Hormogones are the short fragments (5-10) found within the cell. It separates from the cell during the unfavourable condition, and the latter body glides and eventually develops into a new filamentous form. By hormospores: Hormospores releases into the environment, as a result of cell lysis during the unfavourable conditions. Later, the spores germinate to produce new individuals as the favourable condition returns. By akinetes: Akinetes develop in adverse conditions. Its size is larger than the vegetative cells, and they are surrounded by a thick wall. Akinetes separate from the vegetative cell and lives in a resting stage after the accumulation of enough food material within the cells. When favourable conditions return, it grows into a new individual. By heterocyst: It also forms in adverse conditions. On favourable conditions, these germinate into a new filament from either one or both the ends. By endospore: Endospores are present inside the cell. It releases outside the cell as the cell ruptures during the unfavourable conditions. Later, the spores germinate into a new individual in the favourable conditions. By exospore: Exospores are present outside the cell. In adverse conditions, it releases into the environment and germinates into a new individual on the favourable conditions.
- (heavy metal stress induces the production of extracellular metabolites like polysaccharides, metallothioneins or siderophores).
- expressed as mg of metal removed per g of biomass dry weight
- The study delves into various aspects including biomass production, lipid yield, pigment, biomolecules and fuel quality