Biotransformation of aquaculture wastewater into aquatic feed protein source: Chlorella sorokiniana nutritional value and safety risk assessment

Cui Liu; Luohai Hua; Haokun Liu; Lan Wang; Xiaoming Zhu; Céline Rebours; Kevin Graham Harding; Lu Tan; Qiang Hu; Shouqi Xie

doi:10.1016/j.jenvman.2024.122510

Biotransformation of aquaculture wastewater into aquatic feed protein source: Chlorella sorokiniana nutritional value and safety risk assessment

J Environ Manage. 2024 Sep 17:370:122510. doi: 10.1016/j.jenvman.2024.122510. Online ahead of print.

Authors

Cui Liu¹, Luohai Hua², Haokun Liu³, Lan Wang⁴, Xiaoming Zhu⁵, Céline Rebours⁶, Kevin Graham Harding⁷, Lu Tan⁸, Qiang Hu⁹, Shouqi Xie¹⁰

Affiliations

¹ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China; Xianghu Laboratory, Hangzhou, 311231, China.
² State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China; University of Chinese Academy of Sciences, Beijing, 100049, China.
³ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China. Electronic address: liuhaokun@ihb.ac.cn.
⁴ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China; Key Laboratory for Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China.
⁵ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China; Hubei Engineering Research Center for Aquatic Animal Nutrition and Feed, Wuhan, 430072, China.
⁶ Møreforsking AS, Ålesund, Norway.
⁷ School of Chemical & Metallurgical Engineering, University of the Witwatersrand (WITS), Johannesburg, South Africa.
⁸ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China.
⁹ Faculty of Synthetic Biology, CAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.
¹⁰ State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China; University of Chinese Academy of Sciences, Beijing, 100049, China; The Innovative Academy of Seed Design, Chinese Academy of Sciences, 430072, Wuhan, China.

PMID: 39293110
DOI: 10.1016/j.jenvman.2024.122510

Abstract

Aquaculture wastewater contains high concentrations of nitrogen and phosphorus compounds, which can be used as nutrients for microalgal growth. In this study, the ability of Chlorella sorokiniana (C. sorokiniana) to purify aquaculture wastewater from an intensive recirculating aquaculture system (RAS) carp sp. farm was evaluated. We then assessed the safety risk of C. sorokiniana cultured from aquaculture wastewater and conducted an 8-week fish feeding trial to evaluate its nutritional value as a feed protein source. The three diets were supplemented with 0 (FM, control), 5% (MM5) or 15% (MM15) C. sorokiniana to replace the fish meal. A total of 180 healthy gibel carp (Carassius gibelio) of similar size were randomly selected into 9 tanks (20 fish/tank, 3 tanks/group). At the end of C. sorokiniana purifying aquaculture wastewater, DIC and DTC gradually decreased by 80.6% and 16.5%, respectively, whereas DOC increased by 52.2%. The change curve of COD_Mn was similar to that of DOC, and the removal rates of NH₄-N, DTN, DIP and DTP were 93.5%, 86.8%, 36.0% and 26.6%, respectively. The heavy metals and antibiotics contents of C. sorokiniana were low or not detected and conformed to the requirements of the aquatic feed ingredient standards. The ARA, EPA and total polyunsaturated fatty acids contents of C. sorokiniana were 13.67, 33.82 and 76.81% of the total fatty acids content, respectively. At the end of the fish feeding trial, we found that the replacement of fishmeal with C. sorokiniana did not affect the growth of the fish or the amino acids contents of the muscle but promoted the body colour values of the fish and the relative content of n-3 polyunsaturated fatty acids in the muscle. In addition, 5% dietary C. sorokiniana can upregulate the relative expression of cat and increase the activity of CAT in the liver; upregulate the relative expression of the proinflammatory factor inf-γ and the anti-inflammatory factors il-4 and tgf-β; and reduce the relative abundance of pathogenic bacteria, such as Citrobacter, Staphylococcus and Pseudomonas, in the gut of gibel carp. However, 15% dietary C. sorokiniana significantly increased the relative expression of inf-γ and hsp70 in the liver and only reduced the relative abundance of Citrobacter. Overall, C. sorokiniana has the ability to remove nutrients from aquaculture wastewater and can be an alternative protein source for fish. On the basis of growth performance, antioxidant capacity, fatty acid contents of muscle, and the gut microbiota, 5% dietary C. sorokiniana is recommended.

Keywords: Aquaculture wastewater; Chlorella sorokiniana; Fatty acids; Intestinal flora; Removal rates of nutrients.