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CCS Haryana Agricultural
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Agriculture is
Mixotrophy in Cyanobacteria
Mansi
Ph.D. Scholar
2022BS23D
Credit seminar 692
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
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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
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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
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Norena-Caro & Benton (2018)
Fig 1. Cell structure of cyanobacteria
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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
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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
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Fig 4. Photosynthesis in cyanobacteria
Selão et al. (2020)
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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
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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)
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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
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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
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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
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14
Fig 6. Potential applications of cyanobacterial biomass Vu et al. (2020)
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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
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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)
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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)
CCS
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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
CCS
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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
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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
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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
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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
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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)
CCS
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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%
CCS
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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%
CCS
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Agricultural
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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
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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
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Fig 13. Specific growth rate of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions
Results
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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
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Fig 15. Carotenoid productivity of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions
0.0012 mg/g
0.00026 mg/g
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Fig 16. Phycocyanin production of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions
0.022 mg/g 0.015 mg/g
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Fig 17. Total protein content of Anabaena 105 grown under (a) mixotrophic (b) heterotrophic conditions
0.039 mg/g
0.045 mg/g
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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
CCS
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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
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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
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Current understanding and future directions
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CCS
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Agricultural
University,
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Agriculture
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Conclusion
38
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
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

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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
  • 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
  • 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
  • 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
  • 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

  1. 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
  2. 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.
  3. (heavy metal stress induces the production of extracellular metabolites like polysaccharides, metallothioneins or siderophores).
  4. expressed as mg of metal removed per g of biomass dry weight
  5. The study delves into various aspects including biomass production, lipid yield, pigment, biomolecules and fuel quality