The potency of oleaginous yeast Lipomyces starkeyi in organic waste valorization to biodiesel

Abstract

Oleaginous yeast-derived biodiesel production utilizing zero-value organic waste biomasses has been prioritized to curb environmental pollution, global warming, and rising bioenergy demands. Lipomyces starkeyi is a promising lipid accumulator among various oleaginous yeasts due to its potency for lipogenesis utilizing a diverse variety of substrates and tolerating various fermentation inhibitors produced during biomass pretreatment. The prevalence of saturated and monounsaturated longer-chain fatty acids (C16–C18) in triglyceride of L. starkeyi improves the quality of the produced biodiesel. Nevertheless, variations in substrate types, fermentation conditions, and modes of fermentation influence the growth of L. starkeyi and its lipid productivity and profile. This review will comprehensively discuss the lipid production potency of oleaginous L. starkeyi during variations in substrate composition and fermentation conditions and their impact on lipid production and its quality to facilitate industrial production of L. starkeyi-derived biodiesel utilizing zero-value organic waste.

Graphical Abstract

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Keywords

Oleaginous yeast organic waste biodiesel valorization waste-to-biofuel

Introduction

Biodiesel, an alternative fuel to fossil fuels, reduces the environmental carbon footprint to combat global warming and rising energy demands globally.¹ International Energy Agency or IEA projected a rise of 44% (21 billion liters) in global biofuel utilization for transportation till 2027, where nearly 13% of the biodiesel will be derived from waste cooking oils and animal fats as it decreases greenhouse gas emissions and satisfy the feedstock management policy of the United States and Europe.^2,3 India launched and led the Global Biofuel Alliance at the G20 summit in September 2023 to serve as a catalytic platform to foster global collaboration for the advancement and widespread adoption of biofuels.^4,5 Envisioning as the third largest economy in the world, India advocates for the rapid transformation of its fuel economy to self-reliant sustainable renewable energy, especially by adopting biodiesel for the world's second-longest transport network to achieve a market share of US$643 million by 2028.^6,7 Therefore, biodiesel production from zero-value feedstocks has been prioritized recently as a sustainable process worldwide.^3,8,9

Oleaginous microorganisms such as microalgae, yeasts, fungi, and bacteria exhibited the potency to produce intracellular lipids by more than half of their cellular biomass (w/w_dry), which makes them suitable candidates to produce microbial biodiesel.^3,10 Nevertheless, oleaginous yeasts arise superior feedstock among others for biodiesel production considering their high productivity of endotoxin-free biomass with greater C16 and C18 fatty acids-enriched intracellular triglyceride content (Table 1) under a short growth time, ability to grow in a variety of substrates and to tolerate various inhibitors, less susceptible to other microbial contaminations, and easy scale-up of the process.^11–13 Rhodosporidium toruloides produced 51% lipid in their biomass during fed-batch fermentation of glycerol and sunflower meal hydrolysate.¹⁴ Rhodosporidium toruloides yielded intracellular oil of 78% (w/w_biomass) during glycerol fermentation in the presence of 0.7% Tween 20.¹⁰ Pichia kudriavzevii, a rotten fruit isolate produced 19% oil (w/w_biomass) with 42% of oleic, 29% of palmitic, and 9% each of stearic and linoleic acids as major fatty acids during fed-batch fermentation.¹⁵ Trichosporon cutaneum accumulated around 23% oil of their dry cell weight during the fermentation of corn stover hydrolysates.¹³ Fed-batch cultivation of Cryptococcus curvatus and Rhodosporidium toruloides in a mixture of crude glycerol and other nutrient-rich hydrolysates yielded 48% (oleic acid 48%, palmitic acid 32%, linoleic acid 9%, and stearic acid 8%) and 51% (palmitic acid 33% and stearic acid 42%) intracellular oil, respectively, in their biomass.¹⁴

Table 1.

Biomass and lipid production capacity of various oleaginous yeasts and their lipid profiles.

Sl. no.	Oleaginous yeasts	Biomass (g/L)	Lipid production (g/L)	Fatty acid profile (%)	Reference
1.	Rhodosporidium spp.	16–18	11–13	Saturated fatty acid: 18–35 Unsaturated fatty acid: 65–82	Singh et al.¹⁶
2.	Trichosporon spp.	17.4–43.82	5.6–21.87	Saturated fatty acid: 37–38 Unsaturated fatty acid: 59–61	Chen et al.¹⁷ and Liu et al.¹⁸
3.	Cryptococcus spp.	32.9–104	17.40–86.09	Saturated fatty acid: 39.7–50.7 Unsaturated fatty acid: 48.8–56.3	Liang et al.¹⁹ and Zhang et al.²⁰
4.	Pichia spp.	33	6.27	Saturated fatty acid: 38.19 Unsaturated fatty acid: 52.14	Sankh et al.¹⁵
5.	Yarrowia spp.	42.23–59.67	19.47–31.44	Saturated fatty acid: 9.32–43.2 Unsaturated fatty acid: 53.8–68.9	Kumar et al.^21,22
6.	Lipomyces starkeyi	60.4–296.6	36–178	Saturated fatty acid: 71.6–74.9 Unsaturated fatty acid: 28–57.6	Sutanto et al.¹²

Optimization of fermentative parameters such as carbon/nitrogen (C/N) ratio, substrate concentration, pH, and aeration during fed-batch fermentation improved oil content to 61% in oleaginous Rhodotorula glutinis biomass.²³ A variety of oleaginous Lipomyces starkeyi strains exhibited oleic and palmitic acids-rich cellular lipid production capacity (> 70%) during variations in substrate and fermentation conditions.^12,24 This robustness and quality of intracellular oil make oleaginous yeasts industrially significant feedstock for the production of microbial oil-based biodiesel.²⁵ In this review, the heterogenicity of organic waste as potent substrates for oleaginous L. starkeyi-derived biodiesel production has been comprehensively discussed. The impact of substrate variations and fermentation conditions on the biodiesel production potency of L. starkeyi and its lipid profile and productivity were critically evaluated to produce high-quality biodiesel.

Organic wastes as potent substrates for oleaginous yeast fermentation

Globalization led to the disposal of large quantities of heterogeneous organic waste such as various lignocellulosic biomasses; industrial wastewater and sludge; food, fruit, and vegetable wastes; de-oiled biomasses; microalgal biomasses; etc. (Table 2) in the environment. India is expected to generate nearly 165 metric tons of municipal solid waste yearly by 2030, where 50% of that consists of organic waste.²⁶ Global production of lignocellulosic biomasses reached 8.15 × 10⁷ tons annually.²⁷ Annual generation of food waste could exceed 1.3 billion tons globally due to a nearly 28% increase in the human population by 2057.^8,28 Industrial fruit and vegetable processing generates solid organic waste of ∼ 20%–75% of raw biomass.²⁹ Extraction of oil produces a large amount of de-oiled biomass, which accounts for around 65% of grain weight.³⁰ Over 4–5 million tons of spent algal biomass is generated during the production of a billion gallons of algal biodiesel.³¹ Heterogeneity in the composition of organic waste and the richness of carbohydrates, proteins, and moisture make them inappropriate for transesterification to produce biodiesel (Table 2).³² In contrast, the generation of waste glycerol (1/10th of produced biodiesel) during transesterification of lipids/oil to biodiesel led to the accumulation of crude glycerol and annual production of impure glycerol could reach around 6.3 million tons globally by 2025.^3,33 Therefore, fermentative valorization of these organic waste into various biofuels such as biodiesel (i.e. oleaginous yeast oil), bioethanol, biohydrogen, biomethane, and higher alcohols (C3–C5) appears to be promising to reducing the environmental pollution due to improper disposal and to minimizing the process cost.^25,34–37

Table 2.

Physicochemical profile of various organic waste as a potential substrate for oleaginous yeast fermentation.

Sl. no.	Types	Total Solid (%)	Volatile Solid (%)	Carbohydrate content (%)	Protein content (%)	Lipid content (%)	Reference
1.	Rice straw	90.6–96.3	60.55–83.2	60–63	0.19–2.67	NA	Van Hung et al.³⁸ and Basak et al.³⁹
2.	Rice husk	90	81.06	49.53	7.36	NA	Gonzales et al.⁴⁰ and Haider et al.⁴¹
3.	Wheat straw	92.84–93.75	86.49–93.40	53–65	3.24–4.89	NA	Ali et al.⁴² and Tsapekos et al.⁴³
4.	Corn straw	95.91	89.59	55	8.59	NA	Ali et al.⁴² and Tsapekos et al.⁴³
5.	Barley straw	91.4	62.10	55.7	7.38	NA	Sedmihradská et al.⁴⁴ and Aqsha et al.⁴⁵
6.	Switchgrass	91.3	96.9	50.5	3.8	NA	Sheets et al.⁴⁶
7.	Yard trimmings	40	92	39–42	1.5–3.2	NA	Bary et al.⁴⁷
8.	Garden waste	91.4	92.66	32.3	NA	NA	Abreu et al.⁴⁸
9.	Sugarcane Bagasse	95	79.27	58.74	3.98	NA	Vats et al.⁴⁹
10.	Waste paper	95.5	89	65.3–87	0.9	NA	Xu et al.⁵⁰ and Di Fidio et al.⁵¹
11.	Olive mill effluent	5.2	85	NA	3.83	NA	Mekki et al.⁵²
12.	Palm oil mill effluent	6.45	79	59.5	NA	NA	Mamimin et al.⁵³
13.	Mixed wastewater sludge	3.8–4.9	68–79	14–15	16–35	2.1–4.5	Patil et al.⁵⁴ and Kurade et al.⁵⁵
14.	Cheese whey	6.9–7.6	83.91–93	76–77.68	7.79–14	1.28–2.35	Asunis et al.⁵⁶ and Sakarika et al.⁵⁷
15.	Food waste	6.17–25	82–94	19–32	26–36	24–26	Patil et al.⁵⁴ and Saha et al.⁵⁸
16.	De-oiled food waste	7.69	82	69	11	2.2	Yang et al.⁵⁹ and Jiang et al.⁶⁰
17.	De-oiled mustard	88.82	74.49	24.86	32.76	NA	Banerjee et al.⁶¹
18.	De-oiled rice-bran	87.79	75.3	25.85	17	NA	Banerjee et al.⁶¹
19.	De-oiled Jatropha	92.6	85.4	72	5.46	NA	Kanchi et al.⁶²
20.	De-oiled palm kernel	96.55	76.6	66	15.58	6.8	Jimoh and Babatola⁶³
21.	Fruit wastes	38	93	76	6	NA	Saha et al.⁶⁴
22.	Fruit and vegetable waste	34	94	68	2.7	NA	Basak et al.⁶⁵
23.	Potato (peel, mesh), tomato, carrot wastes	NA	NA	14–65	3–22	NA	Singh et al.⁶⁶
24.	Molasses	78–85	NA	48–58	1.28–17.86	NA	Han et al.⁶⁷
25.	Microalgae: Chlamydomonas spp., Porphyridium spp., Chlorella spp., Nannochloropsis spp., Neochloris spp., Acutodesmus spp., Tetraselmis spp.	3.93–28.74	19.55–80.60	13–50	18–46	12–48	Kim et al.²⁵ and Tibbetts et al.⁶⁸

NA: not available.

Being zero-value substrates and able to stabilize the fermentation process by balancing nutrients, organic waste could decrease the process cost by around 70%–75%.^11,69 Nevertheless, fermentative utilization of these complex organic wastes requires solubilization of their organic matter to make them bioavailable to the oleaginous yeast. Various pretreatment processes such as enzymatic hydrolysis; acid/alkali hydrolysis; microwave irradiation, hydrothermal, deep eutectic solvents, ultrasound, ionic liquids, and supercritical carbon dioxide treatments; etc. have been employed to hydrolyze and solubilize the organic matters.^70,71 Microwave irradiation of microalgal biomass extracted 33%–57% of organic constituents as soluble fractions and increased the bioaccessibility by lysing the rigid cell wall.⁷² Ultrasound pretreatment of wastewater sludge increased the soluble COD by 23 times of untreated sludge.⁷³ Hydrothermal treatment of lignocellulosic rice straw achieved solubilization of 96% of hemicellulosic fraction in the biomass.⁷⁴ Humic acid-assisted alkaline pretreatment of lignocellulosic Kentucky bluegrass followed by enzymatic hydrolysis solubilized around 71% cellulose in the hydrolysate.⁷⁵ Therefore, pretreatment of these complex zero-value biomasses could be the primary step to solubilize organic matter for their fermentative utilization using oleaginous yeast.

Lipomyces starkeyi in biodiesel production

Oleaginous yeasts produce triglyceride (TAG) as the major form of lipid (∼ 90%) and accumulate them as lipid droplets due to the inadequacy of TAG to be used for phospholipid bilayer production.^12,76 L. starkeyi is immersed as a promising lipid droplet accumulator among oleaginous yeasts using a large variety of substrates and tolerating diverse fermentation inhibitors produced during biomass pretreatment (Table 3).^77,78 Comparatively high content of oleic acid (48%–55%) and palmitic acid (28%–58%) in TAG of L. starkeyi make it industrially suitable for the production of high-quality biodiesel.^12,79,80 The presence of saturated and longer-chain fatty acids (C16–C18) in TAG of L. starkeyi improves the cetane number of produced biodiesel to ∼ 61, which is much higher than the standard values (40–51) for biodiesel in Europe and the USA (Table 4).⁸¹ Biodiesel with a high cetane number enables smooth engine ignition and improves cold start behavior for complete fuel combustion, minimizing carbon monoxide, and particulate matter emissions.¹¹ Saturated fatty acids in biodiesel provide sufficient lubricity and decrease NO_X emissions.⁸² Relatively large monounsaturated fatty acid content (i.e. oleic acid) in oleaginous TAG increases its specific gravity, heating value, and iodine number in produced biodiesel (Table 4).^10,83 L. starkeyi-derived biodiesel exhibited an excellent degree of unsaturation (105.5), oxidative stability (5.12), and cold filter plugging point (−4.13 °C) among other oleaginous yeast due to its high oleic acid content.³ The monounsaturated and saturated fatty acids ratio in L. starkeyi biodiesel provides good oxidative stability to meet international standards.^12,82

Table 3.

Growth of various L. starkeyi strains and their fatty acid profiles under variations in substrates and fermentation modes.

Sl. no.	Substrates	Yeast strain	Fermentation modes	Biomass yields (g/L)	Lipid content (%)	Lipid yields (g/L)	Lipid yields (g/g)	Fatty acid profile (%)	Reference
1.	Glucose	AS 2.1560	Fed-batch cultivation	104.6	64.9	67.9	NA	C14:0, 0.5; C16:0, 36.5; C16:1, 3.6; C18:0, 5.4; C18:1, 52.8; C18:2, 1.2	Lin et al.⁸⁴
2.	Xylose	DSM 70296	Batch cultivation	12.32	35.02	4.13	0.14	C16:0, 36.2; C16:1, 2.27; C18:0, 12.09; C18:1, 45.67; C18:2, 3.5	Tapia et al.⁸⁵
3.	Xylose	ATCC 56304	Fed-batch cultivation	27	51.7	13.96	0.16	C16:0, 18.9; C16:1, 4.0; C18:0, 5.0; C18:1, 67.9; C18:2, 2.9	Probst and Vadlani⁸⁶
4.	Glucose and mannose	AS 2.1560	Fed-batch cultivation	22.0	58.3	12.8	0.18	C16:0, 35.5; C16:1, 3.9; C18:0, 5.4; C18:1, 53.9; C18:2, 0.6	Yang et al.⁸⁷
5.	Glucose-xylose mixture	NBRC 10381	Biphasic fed-batch cultivation	58.26	43.75	25.5	0.1	C16:0, 24.5; C16:1, 10.4; C18:0, 7.9; C18:1, 42.9; C18:2, 10.2	Amza et al.⁷⁹
6.	Crude glycerol	DSM 70296	Batch cultivation	34.4	35.9	12.34	0.11	C16:0, 33.1; C18:0, 8.0; C18:1, 53.1; C18:2, 4.4	Tchakouteu et al.⁸⁸
7.	Crude glycerol	DSM 70295	Fed-batch cultivation	32.7	55.9	18.27	0.187	C14:0, 3.0; C16:0, 32.2; C16:1, 4.2; C18:0, 10.9; C18:1, 40.9; C18:2, 7.2; C18:3, 0.6	Signori et al.⁸⁹
8.	Crude glycerol	CBS 1870	Batch cultivation	NA	NA	19.5	0.39	NA	Maruyama et al.⁹⁰
9.	Furfural, 5-hydroxymethylfurfural (HMF), acetic acid, formic acid, levulinic acid, vanillin, and syringaldehyde	NBRC 10381	Batch cultivation	28.52	68.24	19.46	0.19	C16:0, 39.27; C16:1, 5.57; C18:0, 9.23; C18:1, 40.56; C18:2, 2.05; C24:0, 0.22	Juanssilfero et al.⁹¹
10.	Furfural, HMF, vanillin, para-hydroxy benzaldehyde (PHB), and syringaldehyde	ATCC 58680	Batch cultivation	7.60–10.00	27.3–56.5	2.07–5.65	0.162–0.18	C16:0, 40.71–54.93; C16:1, 1.01–3.80; C18:0, 6.10–14.03; C18:1, 26.40–47.70	Rahman et al.⁹²
11.	Hemicellulosic (Sugarcane bagasse) hydrolysate	DSM 70296	Batch cultivation	9.6	26.1	2.51	0.14	C16:0, 27.8; C16:1, 3.7; C18:0, 6.0; C18:1, 48.2; C18:2, 10.1	Xavier et al.⁸⁰
12.	Hemicellulosic (Sugarcane bagasse) hydrolysate	DSM 70296	Continuous cultivation	11.5	27.3	3.14	0.18	C16:0, 30.3; C16:1, 1.3; C18:0, 12.6; C18:1, 46.7; C18:2, 7.0
13.	Oil palm empty fruit bunch hydrolysate	DSM 70295	Batch cultivation	9.4	41.4	3.9	0.15	NA	Thanapimmetha et al.⁹³
14.	Corn stover hydrolysate	ATCC 58680	Batch cultivation	18.28	54.85	10.03	0.17	C16:0, 36.9; C16:1, 2.4; C18:0, 15.1; C18:1, 42.9; C18:2, 1.2; C24:1, 0.5	Calvey et al.⁹⁴
15.	Paper mill wastepaper enzymatic hydrolysate	DSM 70296	Batch cultivation	11	20.2	3.7	0.20	C16:0, 36.7; C16:1, 4.5; C18:0, 6.1; C18:1, 47.5; C18:2, 5.2	Di Fidio et al.⁵¹
16.	Sugarcane bagasse hydrolysate	DSM 70296	Continuous cultivation	13.9	26.7	3.7	0.22	C16:0, 30.3; C16:1, 0.7; C18:0, 12.6; C18:1, 46.7; C18:2, 7.0	Anschau et al.⁸¹
17.	Rice straw hydrolysate	NA	Batch cultivation	12.76	35.65	4.5	0.15	C16:0, 5.42; C18:0, 3.86; C18:1, 28.26; C18:2, 9.14; C24:0, 41.56	Azad et al.⁹⁵
18.	Rice bran hydrolysate	BCRC 23408	Batch cultivation	23.1	56.11	12.96	0.21	C16:0, 36.14; C16:1, 4.46; C18:0, 5.10; C18:1, 51.95	Sutanto et al.⁹⁶
19.	Flour-rich waste hydrolysate	DSM 70296	Fed-batch cultivation	109.8	58.7	64.5	0.14	C14:0, 1.2; C16:0, 27.1; C16:1, 0.6; C18:0, 8.7; C18:1, 52.9; C18:2, 8.5	Tsakona et al.⁹⁷
20.	Wheat bran hydrolysate	ATCC 56304	Batch cultivation	17.1	37.3	6.38	0.12	C16:0, 17.1; C16:1, 8.2; C18:0, 5.6; C18:1, 64.2; C18:2, 3.5	Probst and Vadlani⁹⁸
21.	Corn bran hydrolysate	ATCC 56304	Batch cultivation	23.5	33.3	7.83	0.13	C16:0, 16.2; C16:1, 6.8; C18:0, 5.2; C18:1, 67.5; C18:2, 2.1	Probst and Vadlani⁹⁸
22	Birchwood chips hydrolysate	CBS 1807	Batch cultivation	15.63	51.3	8.02	0.1	C16:0, 25; C18:0, 1–3; C18:1, 45	Brandenburg et al.⁹⁹
23.	Xylose-acetate mixture	CBS 1807	Fed-batch cultivation	13.30	60.47	8.04	0.11	C16:0, 36; C18:0, 5–8; C18:1, 52	Brandenburg et al.⁹⁹
24.	Pine needles hydrolysate	MTCC 1400	Batch cultivation	35.89	67.46	19.58	NA	C16:0, 36.3; C16:1, 4.4; C18:0, 6.2; C18:1, 51.4; C18:2, 3.48	Pant and Pant¹⁰⁰
25.	Glucose	AS 2.1560	Batch cultivation	12.4	47.0	5.8	0.18	C16:0, 35.7; C16:1, 5.8; C18:0, 10.2; C18:1, 41.5; C18:2, 2.5	Wang et al.¹⁰¹
26.	Xylose			10.4	36.6	3.8	0.13	C16:0, 38.6; C16:1, 5.5; C18:0, 7.0; C18:1, 43.7; C18:2, 1.8
27.	Glycerol			9.1	46.2	4.2	0.15	C16:0, 35.8; C16:1, 4.0; C18:0, 7.5; C18:1, 43.8; C18:2, 4.1
28.	Willow wood sawdust hydrolysate			8.2	42.7	3.5	0.1	C16:0, 35.4; C16:1, 9.6; C18:0, 6.3; C18:1, 39.4; C18:2, 2.5
29.	Nitrogen-limited glucose medium	DSM 70296	Batch cultivation	NA	90.3	NA	NA	C16:0, 31.6; C16:1, 1.6; C18:0, 10.1; C18:1, 47.8; C18:2, 4.2; C18:3, 0.1	Wei et al.¹⁰²
30.	Spent yeast (Rhodotorula toruloides) cell	AS 2.1560	Batch cultivation	19.7	30.8	6.07	0.12	C16:0, 33.8; C16:1, 4.1; C18:0, 11.5; C18:1, 49.0; C18:2, 2.3	Yang et al.⁸⁷
31.	Spent coffee ground hydrolysate	BCRC 23408	Batch cultivation	4.9	32.6	2.5	0.2	NA	Wang et al.¹⁰³
32.	Olive mill waste hydrolysate	NRRL Y-11557	Batch cultivation	2.7	17.8	0.5	0.07	C16:0, 22.5; C16:1, 3.3; C18:0, 2.7; C18:1, 58.1; C18:2, 11.1	Dourou et al.¹⁰⁴
33.	Olive mill wastewater	NA	Batch cultivation	10.4	22.4	2.33	NA	C16:0, 19.1; C16:1, 0.5; C18:0, 8.5; C18:1, 49.1; C18:2, 18.8	Yousuf et al.¹⁰⁵
34.	Crude glycerol and sunflower meal hydrolysate	DSM 70296	Batch cultivation	16.5	30.3	5.0	0.05	C16:0, 28.95; C16:1, 5.04; C18:0, 6.23; C18:1, 57.01; C18:2, 2.76	Leiva-Candia et al.¹⁴
35.	Sewage sludge	DSM 70295	Batch cultivation	18.8	35.6	6.7	NA	C16:0, 55.93; C16:1, 1.85; C18:0, 13.8; C18:1, 25.89	Angerbauer et al.¹⁰⁶
36.	Waste activated sludge	AS 2.1390	Batch cultivation	2.6	30	0.78	NA	NA	Wen and Li¹⁰⁷
37.	Sweet sorghum juice	CBS 1807	Batch cultivation	21.7	29.5	6.4	0.077	C16:0, 42.9; C16:1, 2.15; C18:0, 4.9; C18:1, 49.85	Matsakas et al.¹⁰⁸
38.	Sugar beet pulp hydrolysate and molasses	DSM 70295	Pulsed fed-batch cultivation	20.5	49.2	9.7	0.178	C16:0, 34.2; C16:1, 4.8; C18:0, 5.0; C18:1, 51.6; C18:2, 1.5	Martani et al.¹⁰⁹
39.	Potato starch	NRRL Y-11557	Batch cultivation	12	40.3	4.84	0.16	C16:0, 39.0; C16:1, 3.0; C18:0, 3.0; C18:1, 55.0	Wild et al.¹¹⁰

NA: not available.

Table 4.

Comparative analysis of biodiesel, derived from L. starkeyi and other resources.

Sl. no.	Source of biodiesel	Properties						Reference
Sl. no.	Source of biodiesel	Cetane number	Iodine value	Heating value	Degree of unsaturation	Oxidative stability	Cold filter plugging point	Reference
1.	L. starkeyi	50.21	95	40.1	105.5	5.12	−4.13	Spier et al.¹¹¹
2.		60.79	53	40.64	60.7	17.71	10.76	Signori et al.⁸⁹
3.		68.63	25.60	39.48	29.31	–	12.68	Sartaj et al.¹¹
4.		64.97–65.94	–	–	–	–	4.26–5.1	Leiva-Candia et al.¹⁴
5.	R. kratochvilovae	49.01	120	40.91	122.68	4.51	−7.74	Sartaj et al.¹¹
6.	Y. lipolytica	62.83	64.46	41.68	75	10.32	3.34	Zhao et al.³
7.	R. toruloides	58.48	61.91	40.5	69	11.46	14.53	Zhao et al.³
8.	Metschnikowia spp.	53–68	–	–	0.55–1.06	–	−5.04 to 20.75	Maina et al.¹¹²
9.	Jatropha curcus oil	38	94	38.2	–	2.36	–	Sarker¹¹³ and Kumar and Sharma¹¹⁴
10.	Soybean oil	49–51.77	103–109	39.97–41.43	3.02–4.1	4.1	−5.54 to −2	Leiva-Candia et al.,¹⁴ Sia et al.,⁸² Fassinou,¹¹⁵ Thomas and Soucek¹¹⁶
11.	Waste cooking oil	47.17	–	38.43–40.11	–	3.8–5.8	−9
12.	Microalgal oil	51–70	54–119	39.68–45.63	28.15–112.77	8.83	−12.23 to 4.45	Kumar and Sharma,¹¹⁴ Mostafa and El-Gendy,¹¹⁷ Azad et al.,¹¹⁸ Enwereuzoh et al.,¹¹⁹ Nascimento et al.¹²⁰
13.	Sunflower oil	50–51	–	39.38	–	–	−8.98 to −3	Leiva-Candia et al.¹⁴
14.	Crude salmon oil	49.39	116.79	38.8	–	–	−7.7 to −6.3	Dave et al.¹²¹ and Chiou et al.¹²²
15.	Crude seal oil	44.67	138.67	38.88	–	–	–	Dave et al.¹²¹ and Chiou et al.¹²²

Metabolic modeling of L. starkeyi exhibited its potency for lipogenesis utilizing a diverse variety of substrates and predicted the improved production of long-chain fatty acid-enriched lipid droplets through collective utilization of sugars, glycerol, and hydrolysis products such as acetic acid, furfural, 5-hydroxymethyl furfural (HMF) (Figure 1).^24,78 Nevertheless, variations in substrate types and concentrations; fermentation conditions such as C/N ratio, temperature, pH, and oxygen limitation; and modes of fermentation (i.e. batch, continuous, fed-batch, pulsed fed-batch, and biphasic fed-batch) influence the growth of L. starkeyi and its lipid profile and productivity (Table 3).⁷⁶

Figure 1.

Oleaginous yeast L. starkeyi-mediated triglyceride (TAG) biosynthesis using various carbon sources, derived from organic waste and their pretreated hydrolysate. Growth of L. starkeyi and its lipid production in the presence of arabinose, glucose, xylose, acetic acid, furfural, HMF (a), and glycerol (b) during continuous and batch fermentations, respectively, and biphasic fed-batch (c) fermentation. Acc1: acetyl-CoA carboxylase; Acl1/Acl2: ATP-citrate lyase; Acs: acetyl-CoA synthetase; AKG: α-ketoglutarate; Ale1: acyltransferase for lysophosphatidylethanolamine; Ald: aldehyde dehydrogenase; Cit: citrate synthase; DAG: diacylglycerol; Dga1/Dga2: diacylglycerol acyltransferase; Dgk1: diacylglycerol kinase; DHAP: dihydroxyacetone phosphate; Fas1/Fas2: fatty acid synthase subunit; FBP: fructose-1, 6-biphosphatase; G3P: glyceraldehyde 3-phosphate; G6P: glucose-6phosphate; Gly3P: glycerol-3-phosphate; Gpd1: Gly3P dehydrogenase; Gut2: Gly3P dehydrogenase; HMF: 5-hydroxymethyl furfural; Idh: isocitrate dehydrogenase; LPA: lysophosphatidic acid; Lro1: phospholipid:diacylglycerol acyltransferase; LsElo1/LsElo2: fatty acid elongases; LsFad2/LsFad3: fatty acid desaturases; Mae1: malic enzyme; OAA: oxaloacetate; PA: phosphatidic acid; Pah1: phosphatidate phosphatase; PL: phospholipids; Sct1: glycerol-3-phosphate acyltransferase; Slc1: lyso-phosphatidic acid acyltransferase.^{24,78,81,86,124}

Changes in C/N ratio during substrate variations

L. starkeyi utilized glucose and mannose simultaneously in a synthetic medium (C/N ratio: 88.3) yielding 58% lipid (0.18 g g_sugar⁻¹) in 22 g L⁻¹ yeast biomass during 5 days of batch cultivation.⁸⁷ L. starkeyi produced 30 g L⁻¹ yeast biomass with around 64% lipid (0.19 g g_sugar⁻¹) in it, when cultivated in oil palm trunk sap extract containing glucose and fructose.¹²³ Cultivation of L. starkeyi in hemicellulose hydrolysate of sugarcane bagasse with C/N of 50 exhibited its capability to utilize acetic acid, furfural, and HMF along with glucose and xylose as carbon sources during continuous fermentation, yielding 27% lipid (0.236 g g⁻¹) rich in oleic acid (47%) and palmitic acid (30%) with high cetane number (63) (Figure 1(a)).⁸¹ Genomic sequence analysis of L. starkeyi confirmed the presence of ACS (acetyl-CoA synthase), hmfD (furoyl-CoA synthetase), hmfE (CoA thioester), hmfH (aldehyde dehydrogenase), and hmfF/G (2,5-furandicarboxylate decarboxylase), which allow the utilization these inhibitors during yeast fermentation.⁸⁰ L. starkeyi utilized crude glycerol as the sole carbon source producing 29 g L⁻¹ yeast biomass with 43% lipid content in 10 days of fermentation under optimized conditions of C/N ratio (60), temperature (30 °C), and pH (6) (Figure 1(b)).¹²⁴ Cultivation of L. starkeyi in glycerol produced 46% lipid (0.15 g g⁻¹) containing biomass rich in oleic acid (44%) and palmitic acid (36%).¹⁰¹ Availability of high titer glycerol (65%–85%) for its utilization in oleaginous fermentation without preprocessing and its moderately higher degree of reduction than other zero-value carbon sources enable greater lipid yields (> 0.328 g g⁻¹) (Table 3).³

An increase of the C/N ratio in the growth medium through nitrogen limitation induced L. starkeyi to produce oleic acid (48%) and palmitic acid (32%) enriched TAG as a major fraction (∼ 90%) of their lipid.¹⁰² The rice hull hydrolysate medium with a C/N ratio of 57 improved lipid accumulation by 64% of the dry fungal biomass utilizing 88% hydrolyzed sugar.¹²⁵ Cultivation of L. starkeyi in C/N ratio of 72 at 200 r/min produced 18 g L⁻¹ dry biomass with 55% lipid, which was dropped by nearly 50%–60% with the increase of agitation (300 r/min) and decrease of C/N ratio (24).⁹⁴ The highest ever lipid content (68 g L⁻¹) and yield (65% of dry_biomass) were achieved in L. starkeyi cultivation under oxygen-limiting conditions because the absence of oxygen limits its use as a terminal electron acceptor to generate enough ATP. This directs carbon utilization toward lipid accumulation under a low level of ATP instead of DNA replication/protein synthesis for cell growth.⁸⁴ Nevertheless, oxygen limiting condition increases the degree of saturation (55% saturated fatty acid in produced lipid) as fatty acid desaturases require oxygen. Dissolved oxygen concentration below 3 mmol L⁻¹ h⁻¹ increased the palmitic acid content to 24% and decreased the contents of oleic acid to 41% and linoleic acid to 3% in the produced lipid of Apiotrichum curvaturn.¹²⁶

Variations in cultivation modes

Modes of cultivation play a crucial role in facilitating lipid productivity in oleaginous yeasts as utilization of high-strength organic waste in batch fermentation could cause substrate inhibition.³ The relatively low yield of L. starkeyi biomass (∼ 14 g L⁻¹) during continuous fermentation compared to fed-batch operation (∼ 80 g L⁻¹) discourages its industrial application for L. starkeyi lipid production.⁸¹ Fed-batch cultivation of oleaginous yeast using high-strength organic waste enables greater lipid production by eliminating substrate inhibition and providing additional substrate to enhance yeast cell growth (Table 3). Fed-batch fermentation of crude glycerol using L. starkeyi produced 33 g L⁻¹ dry biomass (0.26 g g⁻¹) with 60% lipid in it.⁸⁹ A biphasic fed-batch cultivation of L. starkeyi in successive glucose (259.5 g) and xylose (801.2 g) feeding yielded ∼ 60 g L⁻¹ dry biomass (0.28 g g_sugar⁻¹) containing 60% lipid rich in oleic acid (65%) (Figure 1(c)).⁸⁶ Feeding of xylose–acetic acid mixture in fed-batch cultivation of L. starkeyi produced ∼ 61% lipid (0.11 g g⁻¹) containing biomass (13.3 g L⁻¹), where oleic acid (52%) and Palmitic acid (36%) emerged as dominant fatty acids.⁹⁹ Thus, parametric optimization of L. starkeyi fermentation could facilitate the industrial production of high-quality yeast biodiesel utilizing zero-value organic waste.

Current challenges and future perspectives

Structural complexity and rigidity of heterogeneous organic waste hinder the accessibility of the fermentable fractions (i.e. carbohydrates and proteins) during oleaginous yeast fermentation.^71,127 Exploration and optimization of specific, cost-effective, and eco-friendly pretreatment processes considering the variations in structural complexity of agro-industrial organic waste is the need of the hour to solubilize and increase the bioavailability of fermentable organic matter to oleaginous yeast. Artificial intelligence-based smart garbage bins with automatic waste characterization ability could facilitate setting up thresholds for optimized pretreatment and successive oleaginous fermentation of selective organic waste and decrease the upstream process cost.¹²⁸ Nevertheless, variations in substrate types and concentrations; fermentation conditions such as C/N ratio, temperature, pH, and oxygen limitation; and fermentation modes influence the growth of oleaginous yeast and its lipid profile and productivity.⁷⁶ Regulatory genes (LsSPT23) for TAG synthesis and fatty acid elongase genes (LsELo1 and LsELo2) of L. starkeyi play crucial roles in addressing substrate variations and their utilization.^129,130 Employing metabolic engineering in these potential genes would be promising for the growth optimization of L. starkeyi during substrate variation to increase substrate tolerance and enhance TAG production and accumulation of unsaturated long-chain fatty acids in L. starkeyi (Figure 2). These would ensure the economic sustainability of high-quality L. starkeyi-derived biodiesel production by maximizing substrate utilization and decreasing process costs.

Figure 2.

Synergism of metabolic engineering to regulate expression of potent genes (LsELo2 and LsSPT23) and optimization of feedstock (various organic waste) pretreatment and oleaginous fermentation to enhance triglyceride (TAG) biosynthesis in L. starkeyi and C18-rich TAG production for high-quality biodiesel.

Outlook

The availability of large quantities of heterogeneous organic waste paved the way for their sustainable valorization, producing biodiesel to decrease the environmental carbon footprint. Fermentative utilization of organic waste using oleaginous yeast L. starkeyi produces palmitic and oleic acids enriched lipid droplets, suitable for producing high-quality biodiesel to meet international standards. Fed-batch operation emerges as the most reliable operational mode for utilizing diverse substrates in L. starkeyi fermentation to eliminate growth inhibition due to substrates or hemicellulosic hydrolysis products and facilitate greater biomass and lipid yields. Co-fermentation of zero-value organic waste could aid the simultaneous utilization of different substrates in fed-batch (pulsed fed or biphasic) fermentations producing high-density L. starkeyi biomass containing C16–C18 enriched TAG. Therefore, utilizing zero-value agro-industrial organic waste could facilitate L. starkeyi-derived high-quality biodiesel production by decreasing production costs and curtailing environmental pollution due to improper disposal of this organic waste.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

This work was supported by the Korea Institute of Energy Technology Evaluation and Planning (KETEP) and the Ministry of Trade, Industry and Energy (MOTIE) of the Republic of Korea (RS-2023-00255939).

ORCID iDs

Bimal Das

Byong-Hun Jeon

Shouvik Saha is an Assistant Professor of Biotechnology. His area of research is fermentative biofuel production through organic waste valorization, bioremediation of persistent contaminants, and environmental microbiology.

Deep Laha is pursuing a Bachelor's degree in Chemical Engineering. His area of research focuses on the valorization of waste biomass towards value-added product production.

Esha Mandal holds a Bachelor's degree in Biotechnology. Her area of research is biofuel production.

Deepshikha Datta is a Professor of Chemistry. Her area of research focuses on biowaste to value-added product production, fabrication of nanomaterials, and refining of petrochemicals.

Bimal Das is an Assistant Professor of Chemical Engineering. His area of research focuses on waste treatment, remediation of contaminants, bio-nano material synthesis, waste-to-wealth conversion, and advanced battery technologies.

Byong-Hun Jeon, Professor in the Department of Earth Resources and Environmental Engineering at Hanyang University Seoul, South Korea. His area of research includes bioenergy production using various organic waste biomasses and biogeochemistry of metals and (in)organic pollutants in natural and engineered environments.

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