Treatment of oil-produced water using a fungus–microalga consortium

Francine Pimentel de Andrade1, Andreza Heloiza da Silva Gonçalves2, Carlos Eduardo De Farias Silva1, Larissa Rodrigues Macário1, João Victor Oliveira Nascimento da Silva1, Brígida Maria Villar da Gama1, Renata Maria Rosas Garcia Almeida1, Josealdo Tonholo2
1Technology Center, Federal University of Alagoas, Maceió, Brazil
2Institute of Chemistry and Biotechnology, Federal University of Alagoas, Maceió, Brazil

Tóm tắt

The consortium between microalga and fungus can be used in wastewater treatment due the combination of their metabolisms, but this application in petroleum-produced water has not been verified in the literature. This study investigated the microalga-fungus consortium for the treatment of oil-produced water by varying the initial TPH (total petroleum hydrocarbons) concentrations in the effluent between 312 and 2500 mg L−1, the salinity between 5 and 50 g L−1, and at different concentrations of nitrogen (25, 50, and 100 mg L−1) and phosphorus (approximately 30 mg L−1). A synthetic effluent (modified BG-11 medium) with crude oil as a carbon source was used. The microalga Tetradesmus obliquus LCE-01 and the filamentous fungi Aspergillus niger, Penicillium oxalicum, and Cunninghamella echinulata were the species chosen. The experiments were performed in an aerated bubble column reactor at a rate of 1.5 vvm, using illumination of 100 µmol m−2 s−1 (for microalgal experiments) and room temperature between 30 and 35 °C. By cultivating all fungi and microalga separately and in co-culture, it was found that the highest contribution to TPH removal was made by the filamentous fungi, with C. echinulata achieving removal efficiencies between 90 and 95%. With respect to salinity, it was observed that T. obliquus was able to survive up to concentrations of 25 g L−1, and C. echinulata not only grew in all saline concentrations tested but also significantly removed TPH at rates between 80 and 95%. The co-cultivation of the fungus with the microalga removed higher percentages of nitrogen (as nitrate), of 63.4, 44.4, and 31.7%, considering initial concentrations of 25, 50, and 100 mg L–1, respectively. A similar average of 36.58 ± 4.82% of phosphorus removal percentage was found for all experiments (initial phosphorus concentration of 30 mg L–1). When the real effluent was tested, TPH, nitrogen, and phosphorus were removed efficiently by the microalga–fungus consortium presenting higher efficiency than the monocultures.

Tài liệu tham khảo

Ai-Jawhari IFH, Mhail NJ, Ali SAA (2015) Efficiency of some filamentous fungi to treatment of effluent petroleum wastewaters from refinery. Int J Curr Microbiol App Sci 4:625–641 Alazaiza MYD, Albahnasawi A, Ahamad Z, Bashir MJK, Al-Wahaibi T, Abujazar MSS, Amr SSA, Nassani DE (2022) Potential use of algae for the bioremediation of different types of wastewater and contaminants: production of bioproducts and biofuel for green circular economy. J Environ Manag. https://doi.org/10.1016/j.jenvman.2022.116415 Al-Hawash AB, Alkooranee JT, Hayder A, Zhang J, Sun J, Zhang X, Ma F (2018) Isolation and characterization of two strains of crude oil-degrading fungi from the Rumaila oil field, Iraq. Biotechnology Reports 17:104–109. https://doi.org/10.1016/j.btre.2017.12.006 Al-Hawash AB, Zhang X, Ma F (2019) Removal and biodegrdation of different petroleum hydrocarbons using the filamentous fungus Aspergillus sp. RFC-1. Microbiologyopen. https://doi.org/10.1002/mbo3.619 Ammar SH, Khadim HJ, Mohamed AI (2018) Cultivation of Nannochloropsis oculata and Isochrysis galbana microalgae in produced water for bioremediation and biomass production. Environ Technol Innov 10:132–142. https://doi.org/10.1016/j.eti.2018.02.002 ANP-Agência Nacional do Petróleo, Gás Natural e Biocombustíveis (2022) Anuário Estatístico Brasileiro do Petróleo, Gás Natural e Biocombustíveis. APHA (2018a)4500-P Phosphorus. Standard methods for the examination of water and wastewater, 23rd edn. American Public Health Association. Washington, DC. https://doi.org/10.2105/SMWW.2882.093 APHA (2018b) 4500-NO3—Nitrogen (Nitrate). Standard methods for the examination of water and wastewater, 23rd edn. American Public Health Association. Washington, DC. https://doi.org/10.2105/SMWW.2882.089 APHA (2018c) 4500-NO2—Nitrogen (Nitrite). Standard methods for the examination of water and wastewater, 18rd edn. American Public Health Association. Washington, DC. https://doi.org/10.2105/SMWW.2882.088 Arriada AA, Abreu PC (2014) Nannochloropsis oculata growth in produced water: an alternative for massive microalgae biomass production. Brazi J Pet Gas 8:119–125. https://doi.org/10.5419/bjpg2014-0011 Atrakpa EO, Zhou H, Jiang L, Ma Y, Liang Y, Li Y, Zhang D, Zhang C (2022) Improved degradation of petroleum hydrocarbons by co-culture of fungi and biosurfactant-producing bacteria. Chemosphere. https://doi.org/10.1016/j.chemosphere.2021 Barbieri P, Galli E (2012) Microbioloia Ambientale ed elementi di ecologia microbica. Casa Editrice Abrosiana, Milano Benguenab A, Chibani A (2021) Biodegradation of petroleum hydrocarbons by filamentous fungi (Aspergillus ustus and Purpureocillium lilacinum) isolated from used engine oil contaminated soil. Acta Ecol Sin 41:416–423. https://doi.org/10.1016/j.chnaes.2020.10.008 Cassini ST, Francisco SA, Antunes PWP, Oss RN, Keller R (2017) Harvesting microalgal biomass grown in anaerobic sewage treatment effluent by the coagulation-flocculation method: effect of ph. Braz Arch Biol Technol. https://doi.org/10.1590/1678-4324-2017160174 Corral P, Amoozegar MA, Ventosa A (2019) Halophiles and their biomolecules: recent advances and future applications in biomedicine. Mar Drugs 18:33. https://doi.org/10.3390/md18010033 Costa TC, Hendges LT, Temochko B, Mazur LP, Marinho BA, Wechenfelder SE, Florido PL, Da Silva A, De Souza AAU (2022) Evaluation of the technical and environmental feasibility of adsorption process to remove water soluble organics from produced water: a review. J Pet Sci Eng. https://doi.org/10.1016/j.petrol.2021.109360 Das P, Abdulquadir M, Thaher M, Khan S, Chaudhary AK, Alghasal G, Al-Jabri HMSJ (2019) Microalgal bioremediation of petroleum-derived low salinity and low pH produced water. J Appl Phycol 31:435–444. https://doi.org/10.1007/s10811-018-1571-6 Das PK, Rani J, Rawat S, Kumar S (2022) Microalgal co-cultivation for biofuel production and bioremediation: current status and benefits. BioEnergy Res 15:1–26. https://doi.org/10.1007/s12155-021-10254-8 De Andrade FP, De Farias Silva CE, Medeiros JA, Vieira RC, De Sá Filho MLF, Santos GKS (2022) Consortium between microalgae and other microbiological groups: a promising approach to emphasise the sustainability of open cultivation systems for wastewater treatment. J Water Process Eng. https://doi.org/10.1016/j.jwpe.2022.103211 De Andrade FP, De Farias Silva CE, Dos Santos J, Ribeiro TRM, Medeiros JA, Do Nascimento MAA, Santos GKS, Dos Santos CW, Almeida RMRG, De Oliveira AMM, Feijó FM, da Silva Costa MM, De Andrade Lima GS, Ribeiro Junior KAL, Tonholo J (2023) Dairy wastewater treatment by Tetradesmus sp. in open system: molecular identification and the effect of light intensity and organic load in the process. Energy, Ecol Environ 8:356–369. https://doi.org/10.1007/s40974-023-00278-5 Dell’Anno F, Rastelli E, Sansone C, Brunet C, Ianora A, Dell’Anno A (2021) Bacteria, fungi and microalgae for the bioremediation of marine sediments contaminated by petroleum hydrocarbons in the omics era. Microorganisms. https://doi.org/10.3390/microorganisms9081695 Dudek M, Vik EA, Aanesen V, Oye G (2020) Colloid chemistry and experimental techniques for understanding fundamental behaviour of produced water in oil and gas production. Adv Coll Interface Sci 276:2020. https://doi.org/10.1016/j.cis.2020.102105 Fontoura JT, Rolim GS, Ferenzena M, Gutterres M (2017) Influence of light intensity and tannery wastewater concentration on biomass production and nutrient removal by microalgae Scenedesmus sp. Process Saf Environ Prot 111:355–362. https://doi.org/10.1016/j.psep.2017.07.024 Gargouri B, Mhiri N, Karray F, Aloui F, Sayadi S (2015) Isolation and characterization of hydrocarbon-degrading yeast strains from petroleum contaminated industrial wastewater. Toxic Environ Contam. https://doi.org/10.1155/2015/929424 Ghosh S, Rysyn I, Dmytruk OV, Dmytruk KV, Onywaka H, Gyzanhout M, Gafforov Y (2023) Filamentous fungi for sustainable remediation of pharmaceutical compounds, heavy metal and oil hydrocarbons. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2023.1106973 Gil-Izquierdo A, Pedreno MA, Montoro-Garcia S, Tarraga-Martinez M, Iglesias P, Ferreres F, Barceló D, Nunez-Delicado E, Gabaldón JÁ (2021) A sustainable approach by using microalgae to minimize the eutrophication process of Mar Menor lagoon. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2020.143613 Gillard JTF, Hernandez AL, Contretas JA, Francis IM, Cabrales L (2021) Potential for biomass production and remediation by cultivation of the marine model diatom Phaeodactylum tricornutum in oil field produced wastewater media. Water 13:2021. https://doi.org/10.3390/w13192700 Gonçalves AHS, De Andrade FP, De Farias Silva CE, Medeiros JA, Santos GKS, Nascimento MAA, Tonholo J, Almeida RMRG (2023) Biological treatment of petroleum produced water ex situ using microorganisms: an overview, main developments and challenges. Energy, Ecol Environ 8:289–303. https://doi.org/10.1007/s40974-023-00284-7 Hakim MAA, Al-Ghouti MA, Das P, Abu-Dieyeh M, Ahmed TA, Aljabri HMSJ (2018) Potential application of microalgae in produced water treatment. Desalin Water Treat 135(47–58):2018. https://doi.org/10.5004/dwt.2018.23146 Hopkins TC, Graham EJS, Schwilling J, Ingram S, Gomez SM, Schuller AJ (2019) Effects of salinity and nitrogen source on growth and lipid production for a wild algal polyculture in produced water media. Algal Res. https://doi.org/10.1016/j.algal.2018.101406 IAL-Instituto Adolfo Lutz (2005) Métodos físico-químicos para análise de alimentos, 4th edn, Instituto Adolfo Lutz, São Paulo Ji X, Cheng J, Gong D, Zhao X, Qi Y, Su Y, Ma W (2018) The effect of NaCl stress on photosynthetic efficiency and lipid production in freshwater microalga-Scenedesmus obliquus XJ002. Sci Total Environ 633:593–599. https://doi.org/10.1016/j.scitotenv.2018.03.240 Kim GY, Yun YM, Shin HS, Kim HS, Han JI (2015) Scenedesmus-based treatment of nitrogen and phosphorus from effluent of anaerobic digester and bio-oil production. Biores Technol 196:235–240. https://doi.org/10.1016/j.biortech.2015.07.091 Kumar Y, Kaur S, Kheto A, Munshi M, Sarkar A, Pandey HO, Tarfdar A, Sindhu R, Sirohi R (2022) Cultivation of microalgae on food waste: recent advances and way forward. Biores Technol. https://doi.org/10.1016/j.biortech.2022.127834 Lin W, Chen L, Tan Z, Denq Z, Liu H (2022) Application of filamentous fungi in microalgae-based wastewater remediation for biomass harvesting and utilization: from mechanisms to practical application. Algal Res. https://doi.org/10.1016/j.algal.2021.102614 Maamar A, Lucchesi ME, Debaets S, Long NNV, Quemener M, Coton E, Bouderbala M, Burgaud G, Matallah-Boutiba A (2020) Highlighting the crude oil bioremediation potential of marine fungi isolated from the port of Oran (Algeria). Diversity. https://doi.org/10.3390/d12050196 Ojagh SMA, Fallah N, Nasernejad B (2020) Tratamento biológico de compostos orgânicos em água produzida com uso de bactérias halotolerantes. J Environ Chem Eng. https://doi.org/10.1016/j.jece.2020.104412 Okoro CC (2008) Biodegradation of hydrocarbons in untreated produce water using pure fungal cultures. Afr J Microbiol Res 2:217–223. https://doi.org/10.5897/AJMR.9000130 Okoro CC, Amund OO (2010) Biodegradation of produced water hydrocarbons by Aspergillus fumigatus. J Am Sci 6:143–149 Petrobras (2017) Informe Bacia de Santos, 6th edn. Santos-São Paulo Petrobras (2022) Laudo de certificado de qualidade. Pilar-AL Qiao N, Wang C, Du Y, Zhang X, Hu S, Yu D (2022) Cunninghamella echinulata produced from soybean wastewater cleanly harvests oleaginous yeasts in soybean oil refinery effluent by efficient adhesion and improves microbial lipid quality. J Clean Prod. https://doi.org/10.1016/j.jclepro.2022.132813 Qiu Y, Ma Z, Liu X, Zheng R, Xiao Y, Wang M (2022) The Detrimental effect of high salinity on the growth and microcystins contamination of Microcystis aeruginosa. Water. https://doi.org/10.3390/w14182871 Rippka R, Deruelles JJBW, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology. https://doi.org/10.1099/00221287-111-1-1 Rosli SS, Kadir WNA, Wong CY, Han FY, Lim JW, Lam MK, Yusup S, Kiatkittipong W, Kiatkittipong K, Usman A (2020) Insight review of attached microalgae growth focusing on support material packed in photobioreactor for sustainable biodiesel production and wastewater bioremediation. Renew Sustain Energy Rev. https://doi.org/10.1016/j.rser.2020.110306 Salazar J, Santana-Sánchez A, Nakkila J, Sirin S, Allahverdiyeva Y (2023) Complete N and P removal from hydroponic greenhouse wastewater by Tetradesmus obliquus: a strategy for algal bioremediation and cultivation in Nordic countries. Algal Res. https://doi.org/10.1016/j.algal.2023.102988 Silva CS (2021) Valoração da eficiência de tratamento de água produzida através do cultivo de microalgas para produção de lipídios e pigmentos. Dissertation, Federal University of Bahia Singh A, Ward OP (2004) Biodegradation and bioremediation. In: Singh N (ed) Soil biology. Springer, New York Ślizewska W, Struszczyk-Swita K, Marchut-Mikolajczyk O (2022) Metabolic potential of halophilic filamentous fungi—current perspective. Int J Mol Sci. https://doi.org/10.3390/ijms23084189 Song H, Qian J, Fan L, Toda T, Li H, Sekine M, Song P, Takayama Y, Koga S, Li J, Lu Q, Li J, Xu P, Zhou W (2022) Enhancing biomass yield, nutrient removal, and decolorization from soy sauce wastewater using an algae-fungus consortium. Algal Res. https://doi.org/10.1016/j.algal.2022.102878 Tang W, Xu X, Ye BC, Cao P, Ali A (2019) Decolorization and degradation analysis of disperse red 3B by a consortium of the fungus Aspergillus sp. XJ-2 and the microalgae Chlorella sorokiniana XJK. RSC Adv 9:14558–14566. https://doi.org/10.1039/C9RA01169B Varjani SJ (2016) Microbial degradation of petroleum hydrocarbons. Biores Technol 223:277–286. https://doi.org/10.1016/j.biortech.2016.10.037 Wang SK, Yang KX, Zhu YR, Zhu XY, Nie DF, Jiao N, Angelidaki I (2022) One-step co-cultivation and flocculation of microalgae with filamentous fungi to valorize starch wastewater into high-value biomass. Biores Technol. https://doi.org/10.1016/j.biortech.2022.127625 Wrede D, Taha M, Miranda AF, Kadali K, Stevenson T, Ball AS, Mouradov A (2014) Co-cultivation of fungal and microalgal cells as an efficient system for harvesting microalgal cells, lipid production and wastewater treatment. PLoS ONE. https://doi.org/10.1371/journal.pone.0113497 Xie S, Sun S, Dai SY, Yuan JS (2013) Efficient coagulation of microalgae in cultures with filamentous fungi. Algal Res 2:28–33. https://doi.org/10.1016/j.algal.2012.11.004 Yang L, Li H, Wang Q (2019) A novel one-step method for oil-rich biomass production and harvesting by co-cultivating microalgae with filamentous fungi in molasses wastewater. Biores Technol 275:35–43. https://doi.org/10.1016/j.biortech.2018.12.036 Yang Q, Zhang M, Alwathnani HA, Usman M, Mohamad BA, Anomohra AEF, Salama ES (2022) Cultivation of freshwater microalgae in effluent under high salinity for biomass, nutrient removal and fatty acid/biodiesel production. Valoriz Residues Biomass 13:3245–3254. https://doi.org/10.1007/s12649-022-01712-1 Zandonade TA, Sanjombi BA (2015) Gerenciamento de injeção de água: análise qualitativa a partir dos resultados da salinidade da água produzida e testes com traçadores. Lat Am J Energy Res 2:1–7. https://doi.org/10.21712/lajer.2015.v2.n1.p1-7 Zorn SMFE, Reis CER, Silva MB, Hu B, De Castro HF (2020) Consortium growth of filamentous fungi and microalgae: Evaluation of different cultivation strategies to optimize cell harvesting and lipid accumulation. Energies. https://doi.org/10.3390/en13143648