Effect of Lignocellulose Related Compounds on Microalgae Growth and Product Biosynthesis: A Review
Abstract
:1. Microalgae: A Source of Valuable Compounds
Taxonomy | Microalgae | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Domain | Eucaryota | ||||||||||
Division | Chlorophyta | ||||||||||
Class | Chlorophyceae | Trebouxiophyceae | |||||||||
Order | Sphaeropleales | Volvocaes 1 | Chlamydomonadales | Chlorellales | |||||||
Family | Scenedesmaceae | Haematococcaceae | Dunaliellaceae | Chlamydomonadaceae | Chlorellaceae | ||||||
Genus | Acutodesmus | Haematococcus | Dunaliella | Chlamydomonas | Chlorella | ||||||
Species | Scenedesmus obliquus | Haematococcus pluvialis | Dunaliella salina | Chlamydomonas reinhardtii | Chlorella prothotecoides | Chlorella zoofingiensis | Chlorella vulgaris | ||||
Content | Proteins 51% | Pigments 1.5% | Pigments 11% | Lipids 65% | Lipids 62% | Lipids 54% | Proteins 46% | ||||
Reference | [19] | [20] | [21] | [22] | [23] | [24] | [25] | ||||
Domain | Eucaryota | ||||||||||
Division | Heterokontophyta | Dinophyta 2 | Euglenophyta | Heterokontophyta | Chlorophyta | ||||||
Class | Bacillarophyceae | Dinophyceae | Euglenophyceae | Eustigmatophyceae | Chlorophyceae | Chlorophyceae 3 | |||||
Order | Naviculales | Dinotrichales 2 | Euglenales | Eustigmatales | Sphaeropleales | Chlorococcales | Chlorococcales 3 | ||||
Family | Phaeodactylaceae | Crypthecodiniaceae | Euglenaceae | Monodopsidaceae | Selenastraceae | Chlorococcaceae | Dictyosphaeriaceae 3 | ||||
Genus | Phaeodactylum | Crypthecodinium | Euglena | Nannochloropsis | Monoraphidium | Neochloris | Botryococcus | ||||
Species | Phaeodyctylum tricornutum | Crypthecodinium cohnii | Euglena gracilis | Nannochloropsis oculata | Monoraphidium contortum | Neochloris oleoabundans | Botryococcus braunii | ||||
Content | Lipids 20% | Lipids 20% | Lipids 29% | Lipids 32% | Lipids 30% | Lipids 52% | Lipids 65% | ||||
Reference | [26] | [27] | [28] | [29] | [30] | [31] | [32] | ||||
Domain | Procaryota | ||||||||||
Division | Cyanobacteria | ||||||||||
Class | Cyanophyceae | ||||||||||
Order | Nostocales 3 | Chroococcales 4 | Chroococcales | Chroococcales 5 | Oscillatoriales 6 | ||||||
Family | Nostocaceae 3 | Spirulinaceae 4 | Microcystaceae | – | Oscillatoriaceae | ||||||
Genus | Anabaena | Spirulina | Microcystis | Thermosynechococcus | Oscillatoria | ||||||
Species | Anabaena azollae | Spirulina platensis | Microcystis aeruginosa | Thermosynechococcus elongates | Oscillatoria acuminata | ||||||
Content | Proteins 40% | Proteins 67% | Lipids 28% | Lipids 20% | Lipids 25% | ||||||
Reference | [33] | [34] | [35] | [36] | [35] |
2. Composition and Treatment of Lignocellulose Materials
Component * | Triticum Aestivum Bran | Corn Stover | Cynodon Dactylon Grass | Hordeum Vulgare Brewer’s Spent Grain | Oryza Sativa Straw | Picea Abies Softwood | Saccharum Officinarum Bagasse | Salix Hardwood |
---|---|---|---|---|---|---|---|---|
Glucan 1 | 10.5 | 36.1 | 30.4 | 16.7 | 35.9 | 40.9 | 35.8 | 43.0 |
Xylan | 18.3 | 21.4 | 22.6 | 19.9 | 19.0 | 5.1 | 21.2 | 14.9 |
Mannan | – | 1.8 | 0.0 | – | – | 10.1 | 0.79 | 3.2 |
Galactan | 1.1 | 2.5 | 1.8 | – | – | 1.9 | 0.74 | 2.0 |
Arabinan | 10.1 | 3.5 | 4.9 | 8.4 | 3.1 | 1.0 | 1.94 | 1.2 |
Klason lignin | 5.0 | 17.2 3 | 18.8 | 22.9 | 13.6 | 27.7 3 | 16.6 | 24.2 |
AS lignin 2 | – | 4.4 | 4.8 | 3.3 | 1.6 | 2.4 | ||
Reference | [41] | [56] | [57] | [58] | [59] | [60] | [61] | [62] |
3. Effect of Lignocellulose Components on Microalgae Cultures
3.1. Sugars
3.2. Acetates
3.3. Methanol
3.4. Sugar Acids
3.5. Phenolics
Phenolic Compound | Concentration in Hydrolysate (mg/L) | Treatment Method | Material | References |
---|---|---|---|---|
Vanillin | 36, 430 | Dilute acid treatment | Spruce | [68,98] |
Steam explotion + SO2 impregnation | Willow | |||
Vanilic acid | 3, 33 | Alkaline hydrolysis Dilute acid treatment | Brewer’s spent grain Spruce | [68,99] |
Catechol | 440 | Steam explotion + SO2 impregnation | Willow | [98] |
Ferulic acid | 145 | Alkaline hydrolysis | Brewer’s spent grain | [99] |
p-Hydroxybenzoic acid | 27, 81 | Alkaline hydrolysis Dilute acid treatment | Brewer’s spent grain Spruce | [68,99] |
p-Coumaric acid | 139 | Alkaline hydrolysis | Brewer’s spent grain | [99] |
Syringic acid | 8 | Alkaline hydrolysis | Brewer’s spent grain | [99] |
3.6. Furans
3.7. Levulinic Acid
3.8. Fatty Acids
3.9. Terpenoids
Name | Group | Source | Extraction Solvent | Content | Ref. |
---|---|---|---|---|---|
α–Pinene (1) | Monoterpenoids | Abies alba wood | Water | 0.2% A | [46] |
Abies alba knots | 26.4% A | ||||
β-Pinene | Monoterpenoids | Abies balsamea knots | Water | 0.4% A | [46] |
Abies alba knots | 2.3% A | ||||
Limonene | Monoterpenoids | Abies alba knots | Water | 2.1% A | [46] |
Abietic acid | Diterpenoids | Pinus sylvestris wood | Acetone | 0.65%–1.43% A | [47] |
Pinus sylvestris knots | 2.1%–3.9% A | ||||
Picea abies wood | 0.017% A | ||||
Picea abies knots | 0% A | ||||
Palustric acid | Diterpenoids | Pinus sylvestris wood | Acetone | 0.25%–0.67% A | [47] |
Pinus sylvestris knots | 0.43%–1.7% A | ||||
Picea abies wood | 0.045% A | ||||
Picea abies knots | 0.014% A | ||||
Betulin | Triterpenoids | Betula papyrifera bark | EtOAC— Ethanol-Water | 15.4% A | [48] |
Gallic acid (2) | Gallotannins | Terminalia paniculata bark | Water-Chloroform | 0.068% B | [112] |
Ellagic acid (3) | Ellagitannins | Terminalia paniculata bark | Water-Chloroform | 0.061% B | [112] |
Catechin (4) | Proanthocyanidins | Acacia catechu wood | Water | 4.5% A | [113] |
Quercetin (5) | Flavonoids | Terminalia paniculata bark | Water-Chloroform | 0.019% B | [112] |
Rutin (6) | Flavonoids | Terminalia paniculata bark | Water-Chloroform | 0.049% B | [112] |
Pinosylvin | Stilbenes | Pinus sylvestris wood | Acetone | 0.12%–0.98% A | [47] |
Pinus sylvestris knots | 0.91%–3.5% A | ||||
Resveratrol | Stilbenes | Picea mariana bark | Water | 0.01% A | [114] |
Pterostilbene (7) | Stilbenes | Pterocarpus marsupium wood | EtOAc | No data | [115] |
Secoisolariciresinol | Lignans | Araucaria araucana wood | Methanol | 32.99% C | [116] |
Lariciresinol | Lignans | Araucaria araucana wood | Methanol | 10.09% C | [116] |
Pinoresinol | Lignans | Araucaria araucana wood | Methanol | 7.32% C | [116] |
Eudesmin (8) | Lignans | Araucaria araucana wood | Methanol | 18.24% C | [116] |
Gramine (9) | Alkaloids | Hordeum vulgare shoots Phalaris arundinacea samples | No data Chloroform | 0.7% A 0.011% A | [117] [52] |
Berberine (10) | Alkaloids | Phellodendron bark | Water or Methanol | No data | [118] |
Flindersine (11) | Alkaloids | Flindersia australis wood Hortia colombiana wood | No data Ethanol | No data 0.009% A | [119] [120] |
3.10. Polyphenols
3.11. Alkaloids
3.12. Impurities
3.12.1. Heavy Metal Ions
3.12.2. Ionic Liquids
4. Effect of Lignocellulose Hydrolysates on Microalgae
Compound | Concentration | Microalgae | Light | Cultivation Time | Effect on Microalgae | Ref. |
---|---|---|---|---|---|---|
Glucose Mannose Galactose | 50 g/L a | Chlorella zofingiensis | No | Not mentioned | Growth confirmed Astaxanthin synthesis confirmed | [74] |
Glucose | 10 g/L | Chlorella vulgaris | No | 6 days | Increased growth 1 Decreased lipid content 1 | [75] |
Glucose Cellobiose | 10 g/L a | Neochloris oleoabundans | No | 5 days | Growth confirmed | [31] |
Xylose Arabinose | 10 g/L a | Neochloris oleoabundans | No | 5 days | No effect on growth | [31] |
Glucose | 8 g/L 8 g/L | Chlorella sorokiniana | Yes No | 6 days 6 days | Growth acceleration 1 Increased total fatty acid content 1 Growth acceleration 1 Increased total fatty acid content 1 | [76] |
Glucose | 18 g/L | Chlorella sorokiniana | Yes | 10 days | Increased biomass density 1 Decreased lutein content 1 | [77] |
Glucose | 0.5–1 g/L | Phaeodactylum tricornutum | Yes | 10 days | Increased growth 1 Increased lipid content 1 | [78] |
Xylose | 0.15 g/L | Chlorella | Yes | 2 weeks | Increased growth 2 | [79] |
Glucose Rhamnose Xylose | 1.8 g/L a 1.64 g/L a 1.5 g/L a | Chlorella vulgaris | No | 15 days | Growth confirmed | [80] |
Acetate | 2.46 g/L over 4.1 g/L | Haematococcus pluvialis | Yes | 8 days | Growth confirmed Decreased growth 3 | [81] |
Acetate | 2.5 g/L 10–20 g/L | Haematococcus pluvialis | Yes | 10 days | Increased growth 1 Increased carotenoid content 1 Decreased growth 1 Increased carotenoid content 1 | [82] |
Acetate | up to 3.28 g/L 4.1–4.9 g/L | Chlorella sorokiniana | Yes | 10 days | Increased biomass concentration 1 Increased lutein content 1 Increased biomass concentration 1 Decreased lutein content 1 | [77] |
Acetate | 1 g/L | Chlamydomonas reinhardtii | Yes | 2 days | Increased growth 1 Chlorophyll content increased 1 Cell size increased 1 Oxygen production increased 1 Increased growth 4 Chlorophyll content decreased 4 Cell size unchanged 4 Oxygen production decreased 4 | [84] |
Methanol | 7.9 g/L + 5% CO2 7.9 g/L without 5% CO2 | Chlorella sp. | Yes Yes | 45 days 45 days | Increased biomass growth 4 Increased lipid content 4 Decreased biomass growth 4 Decreased lipid content 4 | [85] |
Methanol | 3.9 g/L | Scenedesmus obliquus | Yes No | 40 h 24 h | Biomass growth enhancement 1 No growth enhancement 1 | [86] |
Glucuronic acid | 2.5 g/L b | Ochromonas danica | Yes | 6 h | No increase in ascorbic acid synthesis 5 | [89] |
Glucuronic acid | 2.5 g/L | Euglena gracilis | Yes | 4 h | Enhanced ascorbic acid synthesis 6 | [90] |
Galacturonic acid | 2.5 g/L b | Ochromonas danica | Yes | 6 h | Enhanced ascorbic acid synthesis 5 | [89] |
Galacturonic acid | 2.5 g/L | Euglena gracilis | Yes | 4 h | Enhanced ascorbic acid synthesis 6 | [90] |
Catechol | 0.05 μg c | Chlorella zofingiensis Coelastrum microporum Mesotaenium caldarorium | Yes | Not mentioned | Growth inhibition 7a | [92] |
Catechol | 0.05 μg c | Chlorella saccharophila Scenedesmus quadricauda | Yes | Not mentioned | No effect on growth 7b | [92] |
Catechol P-hydroxybenzoic acid P-coumaric acid Caffeic acid Ferulic acid | 0.4 g/L a | Scenedesmus quadricauda | Yes | 5 or 10 days | Removal of compounds from growth medium | [92] |
O-hydroxybenzoic acid P-hydroxybenzoic acid | 13.8 mg/L a | Chlorella vulgaris | Yes | 6–9 days | Growth stimulation 8 Increased pigment content 8 Increased protein content 8 Increased RNA and DNA content 8 | [93] |
M-hydroxybenzoic acid | 13.8 mg/L | Chlorella vulgaris | Yes | 6–9 days | Growth inhibition 8 | [93] |
P-hydroxybenzoic acid | 13.8–55 mg/L | Chlorella pyrenoidosa | Yes | 16 days | Growth stimulation 8 | [94] |
Vanillic acid | 16.8–67 mg/L | Chlorella pyrenoidosa | Yes | 16 days | Growth stimulation 8 | [94] |
Syringic acid | 19.8–79 mg/L 99 mg/L | Chlorella pyrenoidosa | Yes | 16 days | Growth stimulation 8 Culture death | [94] |
P-hydroxybenzoic acid | 13.8–138 mg/L 1.36 g/L | Pseudokirchneriella subcapitata+ | Yes | 72 h | Growth stimulation 8 Growth inhibition 8 | [95] |
O-hydroxybenzoic acid | 13.8–138 mg/L | Pseudokirchneriella subcapitata+ | Yes | 72 h | Growth inhibition 8 | [95] |
2-Furfural | 0.67 g/L | Spirulina maxima | Yes | 144 h | Growth inhibition 8 Photosynthesis inhibition 8 | [102] |
2-Furfural | 0.6 g/L + acetate | Chlamydomonas reinhardtii | Yes | Not mentioned | Growth inhibition 9 | [103] |
5-HMF | 1.13 g/L | Spirulina maxima | Yes | 144 h | Growth inhibition 8 Photosynthesis inhibition 8 | [102] |
Levulinic acid | 1.16–11.6 g/L | Sceletonema costatum | Yes | 96 h | Growth inhibition 8 Aminolevulinic acid accumulation 8 Chlorophyll synthesis inhibited 8 | [105] |
Levulinic acid | 1.16–5.8 g/L | Chlorella vulgaris | Yes | 24 h | Growth inhibition 8 Aminolevulinic acid accumulation8 Chlorophyll synthesis inhibited 8 | [104] |
Levulinic acid | 6.96 g/L | Agmenellum quadruplicatum | Yes | 14 h | Growth inhibition 8 Aminolevulinic acid accumulation 8 Chlorophyll synthesis inhibited 8 | [106] |
Palmitic acid C16:0 | 3.87 mg/L | Selenastrum capricornutum | Yes | 72 h | Growth inhibition 8 | [108] |
Palmitic acid C16:0 | 59.1 mg/L | Chlorella vulgaris | Yes | 24 h | Growth inhibition 8 K+ leakage from cells | [109] |
Palmitic acid C16:0 | 9.2 mg/L | Monoraphidium contortum | Yes | 24 h | Growth inhibition 8 K+ leakage from cells | [109] |
Oleic acid C18:1 | 0.47 mg/L | Selenastrum capricornutum | Yes | 72 h | Growth inhibition 8 | [108] |
Oleic acid C18:1 | 12.4 mg/L | Chlorella vulgaris | Yes | 24 h | Growth inhibition 8 K+ leakage from cells | [109] |
Oleic acid C18:1 | 12.1 mg/L | Monoraphidium contortum | Yes | 24 h | Growth inhibition 8 K+ leakage from cells | [109] |
Linoleic acid C18:2 | 1.55 mg/L | Selenastrum capricornutum | Yes | 72 h | Growth inhibition 8 | [108] |
Linoleic acid C18:2 | 9.4 mg/L | Chlorella vulgaris | Yes | 24 h | Growth inhibition 8 K+ leakage from cells | [109] |
Linoleic acid C18:2 | 8.0 mg/L | Monoraphidium contortum | Yes | 24 h | Growth inhibition 8 K+ leakage from cells | [109] |
α–Pinene β–Pinene Limonene | 10 g/L d | Chlorella pyrenoidosa | Yes | 2 days | No effect on growth 7b | [110] |
α–Pinene | Analytical grade | Chlorella vulgaris stored as dried paste | – | 7–8 h of extraction | Extraction of lipids from Chlorella | [111] |
Gallic acid | 10 mg/L | Nostoc sp. | Yes | 5 days | Growth inhibition 8 Protein content reduction 8 Chlorophyll content reduction 8 Inhibition of glutamine synthetase activity 8 Inhibition of nitrate reductase activity 8 | [128] |
Gallic acid | 1 mg/L | Microcystis aeruginosa | Yes | 15 days | Growth inhibition 8 | [131] |
Ellagic acid | 5 mg/L | Microcystis aeruginosa | Yes | 15 days | Growth inhibition 8 | [131] |
Quercetin | 6 mg/L | Thalassiosira pseudonana Phaeodactylum tricornutum Thalassiosira weissflogii | Yes | Not mentioned | Photosynthetic mechanism inhibited 8 | [132] |
Quercetin | 12 mg/L | Chlamydomonas sp. Dunaliella tetriolecta | Yes | Not mentioned | No inhibition of photosynthetic mechanism 8 | [132] |
Rutin | 0.4 mg/L | Sceletonema costatum | Yes | 3 days | Growth inhibition 8 | [133] |
Catechin | 25–100 mg/L | Microcystis aeruginosa Pseudokirchneriella subcapitata | Yes No Yes No | 2 h 2 h 2 h 2 h | Formation of ROS~ in cells Formation of ROS~ in cells Formation of ROS~ in cells Formation of ROS~ in cells | [134] |
Pinosylvin | 21.2 mg/L 21.2 mg/L | Selenastrum capricornutum Oscillatoria perornata | Yes Yes | 4 days 4 days | No effect on growth 8 No effect on growth 8 | [135] |
Resveratrol | 22.8 mg/L 22.8 mg/L | Selenastrum capricornutum Oscillatoria perornata | Yes Yes | 4 days 4 days | No effect on growth 8 No effect on growth 8 | [135] |
Pterostilbene | 2.5 mg/L 25.6 mg/L | Selenastrum capricornutum Oscillatoria perornata | Yes Yes | 4 days 4 days | Growth inhibition 8 Growth inhibition 8 | [135] |
Eudesmin | 3.8 mg/L 38.6 mg/L 38.6 mg/L | Oscillatoria perornata Oscillatoria agardhii Selenastrum capricornutum | Yes Yes Yes | 4 days 4 days 4 days | Growth inhibition 8 No effect on growth 8 Growth inhibition 8 | [136] |
Gramine | 2 mg/L 1 mg/L 8 mg/L | Microcystis aeruginosa | Yes | 24–60 h 5 days 1 day or 5 days | Breakage of cell wall structure 8 DNA fragmentation 8 DNA fragmentation 8 | [138] |
Gramine | 65 mg/L | Chlorella vulgaris | Yes | 10 days | Growth inhibition 8 | [139] |
Berberine | 1 mg/L 1 mg/L 0.75 mg/L 0.27 mg/L 0.57 mg/L 0.64 mg/L | Pseudokirchneriella subcapitata+ Chlorella vulgaris Scenedesmus quadricauda Microcystis aeruginosa Synechococcus nidulans Aphanothece clathrata | Yes Yes Yes Yes Yes Yes | 4 days 4 days 4 days 4 days 4 days 4 days | Not stated Not stated Growth inhibition 8 Growth inhibition 8 Growth inhibition 8 Growth inhibition 8 | [140] |
Berberine | 0.2 g/L | Microcystis aeruginosa | Yes | 3 days | Inhibition of SOD activity 8 Increased O2− content in cells 8 | [141] |
Flindersine | 3.6 mg/L 22.7 mg/L 4 mg/L | Oscillatoria perornata Oscillatoria agardhii Selenastrum capricornutum | Yes Yes Yes | 4 days 4 days 4 days | Growth inhibition 8 No effect on growth 8 Growth inhibition 8 | [136] |
Lead Pb (added as PbCl2) | 0.5 mg/L | Selenastrum capricornutum Chlorella pyrenoidosa Chlorella ellipsoidea Chlorella vulgaris | Yes | 7 days | Growth inhibition 8 | [144] |
Cadmium Cd (added as CdCl2) | 17 mg/L | Scenedesmus armatus | Yes | 24 h | Growth inhibition 10a Inhibition of photosynthetic mechanism 10a Growth inhibition 10b Inhibition of photosynthetic mechanism 10b | [146] |
Nickel Ni (added as NiCl2) | 10 mg/L | Synechococcus sp. | Yes | 10 days | Growth inhibition 8 | [145] |
Chromium Cr (added as K2CrO4) | 0.97 mg/L | Chlorella vulgaris | Yes | 96 h | Growth inhibition 8 Photosynthetic mechanism inhibited 8 | [147] |
EMIM Cl | 1.46 g/L | Chlorella vulgaris | Yes | 72 h | Growth inhibition 8 | [151] |
EMIM Cl | 1.83 g/L | Oocystis submarina | Yes | 72 h | Growth inhibition 8 | [151] |
EMIM Cl | 14.6 mg/L | Cyclotella meneghiniana | Yes | 72 h | Growth inhibition 8 | [151] |
BMIM Cl | 0.17 g/L | Chlorella vulgaris | Yes | 72 h | Growth inhibition 8 | [151] |
BMIM Cl | 0.26 g/L | Oocystis submarina | Yes | 72 h | Growth inhibition 8 | [151] |
BMIM Cl | 1.74 mg/L | Cyclotella meneghiniana | Yes | 72 h | Growth inhibition 8 | [151] |
Rice straw hydrolysate | 11 g/L sugars e | Chlorella pyrenoidosa | Yes | 60 h | Increased growth 11 Increased lipid content 11 | [152] |
Wheat bran hydrolysate | 0.25%–1.5% f | Chlorella vulgaris | Yes | 6 days | Increased biomass growth 12 Increased protein content 12 Increased pigment content 12 | [19] |
Wheat bran hydrolysate | 0.25%–1.5% f | Chlorella vulgaris | No | 6 days | Increased biomass growth 13 Increased protein content 13 Increased pigment content 13 | [19] |
Wheat bran hydrolysate | 0.25%–1.5% f | Scenedesmus obliquus | Yes | 8 days | Increased biomass growth 12 Increased protein content 12 Decreased pigment content 12 | [19] |
Wheat bran hydrolysate | 0.25%–1.5% f | Scenedesmus obliquus | No | 8 days | Increased biomass growth 13 Increased protein content 13 Decreased pigment content 13 | [19] |
5. Strategies for Implementing Lignocellulose Extracts into Microalgae Cultivation Systems
6. Conclusions
Acknowledgments
Conflict of Interests
References
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Miazek, K.; Remacle, C.; Richel, A.; Goffin, D. Effect of Lignocellulose Related Compounds on Microalgae Growth and Product Biosynthesis: A Review. Energies 2014, 7, 4446-4481. https://doi.org/10.3390/en7074446
Miazek K, Remacle C, Richel A, Goffin D. Effect of Lignocellulose Related Compounds on Microalgae Growth and Product Biosynthesis: A Review. Energies. 2014; 7(7):4446-4481. https://doi.org/10.3390/en7074446
Chicago/Turabian StyleMiazek, Krystian, Claire Remacle, Aurore Richel, and Dorothee Goffin. 2014. "Effect of Lignocellulose Related Compounds on Microalgae Growth and Product Biosynthesis: A Review" Energies 7, no. 7: 4446-4481. https://doi.org/10.3390/en7074446