A MULTISTAGE GRADUAL NITROGENREDUCTION STRATEGY FOR INCREASED LIPID PRODUCTIVITY AND NITROGEN REMOVAL IN WASTEWATER USING <i>Chlorella vulgaris  </i>   AND <i>Scenedesmus obliquus</i>

Robles-Heredia, J. C.; Sacramento-Rivero, J. C.; Canedo-López, Y.; Ruiz-Marín, A.; Vilchiz-Bravo, L. E.

doi:10.1590/0104-6632.20150322s00003304

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BIOPROCESS ENGINEERING • Braz. J. Chem. Eng. 32 (2) • Apr-Jun 2015 • https://doi.org/10.1590/0104-6632.20150322s00003304 copy

A MULTISTAGE GRADUAL NITROGENREDUCTION STRATEGY FOR INCREASED LIPID PRODUCTIVITY AND NITROGEN REMOVAL IN WASTEWATER USING Chlorella vulgaris AND Scenedesmus obliquus

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Chlorella vulgaris and Scenedesmus obliquuswere grown in artificial-wastewater using a new nitrogen-limitation strategy aimed at increasing lipid productivity. This strategy consisted in a multi-stage process with sequential reduction of N-NH₄ concentration (from 90 to 60, 40, and 20 mg.L^-1) to promote a balance between cell growth and lipid accumulation. Lipid productivity was compared against a reference process consisting of nitrogen reduction in two stages, where the nitrogen concentration was suddenly reduced from 90 mg.L^-1 to three different concentrations (10, 20, and 30 mg.L^-1). In the multi-stage mode, only C. vulgaris exhibited a net lipid-productivity increase. Lipid content of S. obliquus did not present a significant increase, thus decreasing lipid productivity. The highest lipid productivities were observed in the two-stage mode for both S. obliquus and C. vulgaris (194.9 and 133.5 mg.L^-1.d^-1, respectively), and these values are among the highest reported in the literature to date.

Keywords
Nitrogen limitation; Lipid productivity; Multistage; Microalgae; Biodiesel

Species	P_L (mg L^-1d^-1)	Culture conditions and reference
C. vulgaris	180.0	Nitrogen limitation (Gouveia and Oliveira, 2009Gouveia, L., Oliveira, A. C., Microalgae as a raw material for biofuels production. Journal of Industrial Microbiology & Biotechnology, 36, 269-74 (2009).)
	147.0	Semi-continuous cultivation in bubble column photobioreactors (*Feng et al.,* 2011**Feng, Y., Li, C., Zhang, D., Lipid production ofChlorella vulgaris cultured in artificial wastewater medium. Bioresource Technology, 102, 101-105 (2011).)
	77.1	Nitrogen limitation (*Mujtaba et al.,* 2012**Mujtaba, G., Choi, W., Lee, C., Lee, K., Lipid production byChlorella vulgaris after a shift from nutrient-rich to nitrogen starvation conditions. Bioresource Technology, 123, 279-283 (2012).)
	67.0	Nitrogen limitation (*Griffiths et al.,* 2011**Griffiths, M. J., Hille, R. P., Harrison, S. T. L., Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. Journal of Applied Phycology (2011).)
	54.0	Nitrogen starvation of Chlorella sp. BUM11008 (*Praveenkumar et al.,2012*Praveenkumar, Shameera, R., K., Mahalakshmi, G., Akbarsha, M. A., Thajuddin, N., Influence of nutrient deprivations on lipid accumulation in a dominant indigenous microalgaChlorella sp., BUM11008: Evaluation for biodiesel production. Biomass Bioenergy, 37, 60-66 (2012).).
	40.0	Optimized productivity limiting nitrogen source, adding CO₂ and varying the light intensity (*Lv et al.,2010*Lv, J., Cheng, L., Xu, X., Zhang, L., Chen, H., Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions. Bioresource Technology, 101, 6797-6804 (2010).)
	16.9	Nitrogen starvation (*Widjaja et al.,* 2009**Widjaja, A., Chien, C., Ju, Y., Study of increasing lipid production from fresh water microalgaeChlorella vulgaris. Journal of the Taiwan Institute of Chemical Engineer, 40, 13-20 (2009).)
	20.4	Reduced nitrate culture (*Converti et al.,2009*Converti, A., Casazza, A. A., Ortiz, E. Y., Perego, P., Del Borghi, M., Effect of temperature and nitrogen concentration on the growth and lipid content ofNannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chemical Engineering and Processing: Process Intensification, 48, 1146-1151 (2009).)
S. obliquus	140.4	Five-day nitrogen starvation in S. obliquus CNW-N (*Ho et al.,* 2012**Ho, S., Chen, C., Chang, J., Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/ carbohydrate production of an indigenous microalgaScenedesmus obliquus CNW-N. Bioresource Technology, 113, 244-252 (2012).)
	106.0	Nitrogen limitation (*Griffiths et al.,* 2011**Griffiths, M. J., Hille, R. P., Harrison, S. T. L., Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. Journal of Applied Phycology (2011).)
	90.0	Nitrogen limitation (Gouveia and Oliveira, 2009Gouveia, L., Oliveira, A. C., Microalgae as a raw material for biofuels production. Journal of Industrial Microbiology & Biotechnology, 36, 269-74 (2009).)
	78.73	Nine-day nitrogen starvation in S. obliquus CNW-N (*Ho et al.,* 2010**Ho, S., Chen, W., Chang, J.,Scenedesmus obliquus CNW-N as a potential candidate for CO2 mitigation and biodiesel production. Bioresource Technology, 101, 8725-8730 (2010).)

		C. vulgaris		S. obliquus
ID	Initial N-NH₄ concentration (mg L^-1)	Max. cell density (cells×10⁶mL^-1)	µ (d^-1)	Max. cell density (cells×10⁶mL^-1)	µ (d^-1)
C₉₀	90	17.73 ± 0.05^a	0.694 ± 0.007^a	19.90 ± 0.05^a	0.638 ± 0.014^a
C₃₀	30	13.82 ± 0.14^b	0.455 ± 0.008^b	14.50 ± 0.05^b	0.600^† † Calculated using only two measurements (0 and 12 h). After 12 h the culture reached stationary or death phase. ± 0.035^a
C₂₀	20	12.22 ± 0.25^c	0.321 ± 0.018^c	9.17 ± 0.06^c	0.247^† † Calculated using only two measurements (0 and 12 h). After 12 h the culture reached stationary or death phase. ± 0.024^b
C₁₀	10	13.29 ± 0.07^d	0.397 ± 0.008^d	11.93 ± 0.22^bc	0.192^† † Calculated using only two measurements (0 and 12 h). After 12 h the culture reached stationary or death phase. ± 0.015^b

Species	Treatment ID	N-NH₄ removal (%)	w (%w/w)	P_L (mg L^-1 d^-1)	P_L increment^† † Increment with respect to C90 (%)
C. vulgaris	C₉₀	92.96	42.8 ± 6.1^a	67.24
	C₃₀	49.96	52.0 ± 5.7^b	96.17	43.0
	C₂₀	52.84	67.8 ± 1.2^c	194.92	189.9
	C₁₀	53.31	23.9 ± 2.8^d	3.00	-95.5
S. obliquus	C₉₀	85.33	37.4 ± 3.2^a	79.67
	C₃₀	62.90	60.0 ± 1.4^b	133.48	67.5
	C₂₀	70.24	63.4 ± 3.3^b	106.92	34.2
	C₁₀	74.21	24.4 ± 4.6^c	6.82	-91.4

		C. vulgaris		S. obliquus
Treatment ID	Initial N-NH₄ concentration (mg L^-1)	Max. cell density (cells×10⁶mL^-1)^* * Different letters in the same column represent significant differences according to Tukey's test (p ≥ 0.05); (± Standard deviation)	µ (d^-1)	Max. cell density (cells×10⁶ml^-1)^* * Different letters in the same column represent significant differences according to Tukey's test (p ≥ 0.05); (± Standard deviation)	µ (d^-1)
C₉₀	90	22.48 ± 0.53^a	0.551 ± 0.010^a	17.27 ± 0.75^a	0.837 ± 0.027^a
C₃₀	60	32.75 ± 0.55^b	0.270 ± 0.004^b	18.97 ± 0.15^b	0.360 ± 0.062^b
C₂₀	40	21.63 ± 0.31^a	0.134 ± 0.044^c	15.68 ± 1.83^ab	0.377 ± 0.127^b
C₁₀	20	12.17 ± 0.15^c	0.124 ± 0.013^c	14.76 ± 1.65^ab	0.324 ± 0.223^b

Species	Treatment ID	N-NH₄ removal (%)	w (%w/w)	P_L (mg L^-1 d^-1)	P_L increment^† † Increment with respect to C90 (%)
C. vulgaris	C₉₀	86.31	53.2 ± 3.0^a	79.19
	C₆₀	80.40	51.1 ± 2.9^a	53.46	-32.5
	C₄₀	86.00	54.3 ± 2.8^a	62.77	-20.7
	C₂₀	74.83	62.9 ± 3.0^b	108.01	36.4
S. obliquus	C₉₀	87.63	37.6 ± 1.1^a	60.20
	C₆₀	82.43	40.1 ± 3.5^a	77.74	29.1
	C₄₀	73.63	32.4 ± 2.8^ab	40.06	-33.5
	C₂₀	56.12	28.4 ± 5.9^b	-19.71	-132.7

TS^† † Lipid samples in the C10 treatment were smaller than the detection limits.				MS
FAMES	C₉₀	C₃₀	C₂₀	C₉₀	C₆₀	C₄₀	C₂₀
C4:0	12.53(0.38)	15.04(1.33)	11.80 (0.59)	9.11 (0.30)	11.24 (0.64)	12.05 (3.25)	13.12 (0.94)
C14:0	10.27 (0.31)	11.36 (0.28)	10.84 (0.34)	8.45 (1.22)	5.47 (0.01)	6.10 (0.27)	6.18 (0.1)
C15:1	n.d.	n.d.	n.d.	8.88 (0.11)	8.03 (0.11)	6.24 (0.06)	6.87 (0.17)
C16:0	7.03 (0.11)	n.d.	7.05 (0.32)	5.12 (0.07)	4.77 (1.09)	3.93 (0.00)	4.15 (0.06)
C16:1	9.75 (0.42)	11.36 (0.28)	9.60 (0.27)	7.07 (0.29)	5.86 (0.13)	6.40 (0.11)	6.26 (0.00)
C17:0	n.d.	n.d.	n.d.	9.13 (0.30)	7.86 (0.04)	6.48 (0.01)	6.97 (0.19)
C18:1n9t	n.d.	n.d.	n.d.	3.99 (0.00)	3.60 (0.04)	6.65 (0.87)	4.93 (0.41)
C20:0	9.48 (0.04)	12.32 (0.17)	10.65 (0.07)	6.85 (0.02)	7.18 (0.22)	8.30 (0.38)	8.33 (0.04)
C18:3n6	n.d.	n.d.	n.d.	n.d.	5.48 (0.09)	4.75 (0.15)	4.52 (0.07)
C20:1	20.79 (0.12)	20.75 (0.12)	20.23 (0.15)	15.08 (0.10)	15.29 (0.46)	14.48 (0.58)	13.73 (0.05)
C21:0	7.17 (0.17)	7.04 (1.26)	7.31 (0.46)	5.20 (0.12)	5.23 (0.18)	4.78 (0.03)	4.87 (0.20)
C22:0	22.97 (0.56)	22.12 (0.58)	22.52 (1.10)	15.64 (0.42)	14.46 (0.36)	15.33 (0.86)	15.20 (0.37)
C22:1n9	n.d.	n.d.	n.d.	5.48 (0.28)	5.52 (0.10)	4.51 (0.03)	4.87 (0.24)
SFA	69.46(0.31)^a	67.90(0.40)^a	70.16(0.13)^b	59.50(0.02)^a	56.22(0.94)^a	56.98(1.69)^a	58.82(0.01)^a
MUFA	30.54(0.34)^a	32.11(0.40)^a	29.83(0.12)^b	49.50(0.02)^a	38.30(0.85)^a	38.27(1.54)^a	36.66(0.05)^a
PUFA	n.d.	n.d.	n.d.	n.d.	5.41(0.09)^a	4.75(0.15)^a	4.56(0.07)^a
SFA:MUFA	2.27 ^a	2.11 ^a	2.35 ^b	1.47 ^a	1.47 ^a	1.49 ^a	1.60 ^a

TS^† † Lipid samples in the C10 treatment were smaller than the detection limits.				MS
FAMES	C₉₀	C₃₀	C₂₀	C₉₀	C₆₀	C₄₀	C₂₀
C4:0	12.28 (1.67)	23.85 (1.51)	18.43 (1.55)	11.55 (0.30)	15.50 (0.35)	26.13 (0.54)	21.81 (3.6)
C14:0	11.43 (0.16)	14.74 (1.54)	15.39 (1.62)	9.75 (0.04)	7.72 (0.07)	7.33 (0.06)	7.98 (0.62)
C16:1	10.69 (0.16)	8.54 (0.5)	10.53 (0.26)	9.12 (0.00)	7.61 (0.20)	7.06 (0.01)	6.91 (0.66)
C18:1n9t	n.d.	n.d.	n.d.	4.13 (0.04)	5.10 (0.68)	1.64 (1.08)	5.50 (3.51)
C20:0	14.20 (0.21)	9.19 (0.44)	11.38 (0.31)	12.11 (0.36)	9.59 (0.10)	8.54 (0.04)	8.14 (0.18)
C20:1	20.93 (0.28)	17.71 (2.52)	19.19 (0.90)	17.88 (0.08)	20.73 (0.78)	18.51 (0.07)	17.96 (0.06)
C21:0	n.d.	n.d.	n.d.	7.72 (0.56)	7.39 (0.14)	7.35 (0.01)	6.98 (0.14)
C22:0	20.96 (0.42)	14.09 (0.98)	14.68 (0.42)	17.90 (0.64)	17.32 (0.88)	15.03 (0.05)	16.53 (0.97)
C22:1n9	9.52 (1.64)	11.88 (2.50)	10.40 (1.83)	9.83 (0.90)	9.03 (0.31)	8.42 (0.43)	8.19 (0.47)
SFA	58.87 (1.19)^a	61.87 (0.51)^ab	59.88 (0.67)^b	59.03(0.78)^a	57.52(0.41)^a	64.37(0.59)^b	61.44 (2.32)^ab
MUFA	41.13 (1.20)^a	38.13 (0.50)^b	40.12 (0.66)^ab	40.96(0.80)^a	42.48(0.42)^a	35.62(0.60)^b	39.01(2.30)^ab
SFA:MUFA	1.43^a	1.62^b	1.49^a	1.44^a	1.35^a	1.80^b	1.60^ab

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