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Microalgal–Bacterial Synergistic Interactions and Their Potential Influence in Wastewater Treatment: a Review

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Abstract

Microalgae, as the most promising raw material for biodiesel, can absorb and transform N, P, and organic matter in wastewater into cell components such as oil, carbohydrate, and protein. The cultivation of microalgae in wastewater provides the possibility to realize harmless treatment and resource utilization of wastewater and reduce the cost of microalgal culture. Whether in a single microalgal culture process or wastewater system, there always be a large number of bacteria interacting with microalgae, forming a complex microecological system. Although microalgal–bacterial coculture system is feasible features for the higher biomass production and better nutrient adaptability from wastewater, the precise understanding of interaction and coexistence in water bodies is still unclear. Some major challenges are to develop sustainability in the microalgal–bacterial coculture system due to the incomplete knowledge about the mechanism of communication, algal growth promotion, and effect of microalgae on the indigenous bacteria in wastewater. In the present review, nutritional interaction and signal transduction, two main interaction models of algae and bacteria, and the effect of synergism of these two models on microalgal system are summarized. Moreover, the impact of algal–bacterial coculture on algal growth and removal of pollutants in wastewater treatment process was expounded systematically to develop highly efficient consortium systems by covering the sustainability limitations. This work would provide guidance for the establishment of efficient algal–bacterial symbiosis system in the wastewater with complex microecology and nutrient environment to improve the accumulation of microalgal biomass and reduce the cost of microalgal culture.

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References

  1. Han Y, Wu H, Geng Z, Zhu Q (2020) Review: energy efficiency evaluation of complex petrochemical industries. Energy. 203:117893. https://doi.org/10.1016/j.energy.2020.117893

    Article  CAS  Google Scholar 

  2. Jia H, Yuan Q (2016) Removal of nitrogen from wastewater using microalgae and microalgae-bacteria consortia. Cogent Environ Sci 2. https://doi.org/10.1080/23311843.2016.1275089

  3. Stark JS, Smith J, King CK, Lindsay M, Stark S, Palmer AS, Snape I, Bridgen P, Riddle M (2015) Physical, chemical, biological and ecotoxicological properties of wastewater discharged from Davis Station, Antarctica. Cold Reg Sci Technol 113:52–62. https://doi.org/10.1016/j.coldregions.2015.02.006

    Article  Google Scholar 

  4. Fan J, Chen Y, Zhang TC, Ji B, Cao L (2020) Performance of Chlorella sorokiniana-activated sludge consortium treating wastewater under light-limited heterotrophic condition. Chem Eng J 382:122799. https://doi.org/10.1016/j.cej.2019.122799

    Article  CAS  Google Scholar 

  5. Kumar PK, Krishna SV, Naidu SS, Verma K, Bhagawan D, Himabindu V (2019) Biomass production from microalgae Chlorella grown in sewage, kitchen wastewater using industrial CO2 emissions: comparative study. Carbon Resour Convers 2:126–133. https://doi.org/10.1016/j.crcon.2019.06.002

    Article  CAS  Google Scholar 

  6. Delgadillo-Mirquez L, Lopes F, Taidi B, Pareau D (2016) Nitrogen and phosphate removal from wastewater with a mixed microalgae and bacteria culture. Biotechnol Rep 11:18–26. https://doi.org/10.1016/j.btre.2016.04.003

    Article  Google Scholar 

  7. Wu Y, Hu H, Yu Y et al (2014) Microalgal species for sustainable biomass/lipid production using wastewater as resource: a review. Renew Sust Energ Rev 33:675–688. https://doi.org/10.1016/j.rser.2014.02.026

    Article  CAS  Google Scholar 

  8. Choi KJ, Han TH, Yoo G, Cho MH, Hwang SJ (2018) Co-culture consortium of Scenedesmus dimorphus and nitrifiers enhances the removal of nitrogen and phosphorus from artificial wastewater. KSCE J Civ Eng 22:3215–3221. https://doi.org/10.1007/s12205-017-0730-7

    Article  Google Scholar 

  9. Mohd-Sahib AA, Lim JW, Lam MK, Uemura Y, Isa MH, Ho CD, Kutty SRM, Wong CY, Rosli SS (2017) Lipid for biodiesel production from attached growth Chlorella vulgaris biomass cultivating in fluidized bed bioreactor packed with polyurethane foam material. Bioresour Technol 239:127–136. https://doi.org/10.1016/j.biortech.2017.04.118

    Article  CAS  PubMed  Google Scholar 

  10. Chowdhury H, Loganathan B, Mustary I et al (2019) Co-cultivation of activated sludge and microalgae for the simultaneous enhancements of nitrogen-rich wastewater bioremediation and lipid production. Sustain. https://doi.org/10.1016/B978-0-12-815162-4.00012-4

  11. Bhatia SK, Mehariya S, Bhatia RK, Kumar M, Pugazhendhi A, Awasthi MK, Atabani AE, Kumar G, Kim W, Seo SO, Yang YH (2020) Wastewater based microalgal biorefinery for bioenergy production: progress and challenges. Sci Total Environ 751:141599. https://doi.org/10.1016/j.scitotenv.2020.141599

    Article  CAS  PubMed  Google Scholar 

  12. Krug L, Morauf C, Donat C, Müller H, Cernava T, Berg G (2020) Plant growth-promoting Methylobacteria selectively increase the biomass of biotechnologically relevant microalgae. Front Microbiol 11. https://doi.org/10.3389/fmicb.2020.00427

  13. Huo S, Kong M, Zhu F, Qian J, Huang D, Chen P, Ruan R (2020) Co-culture of Chlorella and wastewater-borne bacteria in vinegar production wastewater: enhancement of nutrients removal and influence of algal biomass generation. Algal Res 45:101744. https://doi.org/10.1016/j.algal.2019.101744

    Article  Google Scholar 

  14. Daverey A, Pandey D, Verma P, Verma S, Shah V, Dutta K, Arunachalam K (2019) Recent advances in energy efficient biological treatment of municipal wastewater. Bioresour Technol Rep 7:100252. https://doi.org/10.1016/j.biteb.2019.100252

    Article  Google Scholar 

  15. Mujtaba G, Rizwan M, Kim G, Lee K (2018) Removal of nutrients and COD through co-culturing activated sludge. Chem Eng J 343:155–162. https://doi.org/10.1016/j.cej.2018.03.007

    Article  CAS  Google Scholar 

  16. Russel M, Meixue Q, Alam A et al (2019) Investigating the potentiality of Scenedesmus obliquus and Acinetobacter pittii partnership system and their effects on nutrients removal from synthetic domestic wastewater. Bioresour Technol 299:122571. https://doi.org/10.1016/j.biortech.2019.122571

    Article  CAS  PubMed  Google Scholar 

  17. Ji X, Jiang M, Zhang J, Jiang X, Zheng Z (2018) The interactions of algae-bacteria symbiotic system and its effects on nutrients removal from synthetic wastewater. Bioresour Technol 247:44–50. https://doi.org/10.1016/j.biortech.2017.09.074

    Article  CAS  PubMed  Google Scholar 

  18. Kouzuma A, Watanabe K (2015) Exploring the potential of algae/bacteria interactions. Curr Opin Biotechnol 33:125–129. https://doi.org/10.1016/j.copbio.2015.02.007

    Article  CAS  PubMed  Google Scholar 

  19. Xue L, Shang H, Ma P, Wang X, He X, Niu J, Wu J (2018) Analysis of growth and lipid production characteristics of Chlorella vulgaris in artificially constructed consortia with symbiotic bacteria. J Basic Microbiol 58:358–367. https://doi.org/10.1002/jobm.201700594

    Article  CAS  PubMed  Google Scholar 

  20. Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS (2016) Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003

    Article  CAS  PubMed  Google Scholar 

  21. Fuentes JL, Garbayo I, Cuaresma M, Montero Z, González-del-Valle M, Vílchez C (2016) Impact of microalgae-bacteria interactions on the production of algal biomass and associated compounds. Mar Drugs 14. https://doi.org/10.3390/md14050100

  22. Zhang J, Tian Y, Zuo W et al (2016) Effect of aeration rate on performance and stability of algal-bacterial symbiosis system to treat domestic wastewater in sequencing batch reactors. Bioresour Technol 222:156–164. https://doi.org/10.1016/j.biortech.2016.09.123

    Article  CAS  PubMed  Google Scholar 

  23. Sutherland DL, Park J, Heubeck S, Ralph PJ, Craggs RJ (2020) Size matters-microalgae production and nutrient removal in wastewater treatment high rate algal ponds of three different sizes. Algal Res 45:101734. https://doi.org/10.1016/j.algal.2019.101734

    Article  Google Scholar 

  24. Wollmann F, Walther T, Dietze S et al (2019) Microalgae wastewater treatment: biological and technological approaches. Eng Life Sci 19:860–871. https://doi.org/10.1002/elsc.201900071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mohd Udaiyappan AF, Hasan HA, Takriff MS, Abdullah SRS, Maeda T, Mustapha NA, Mohd Yasin NH, Nazashida Mohd Hakimi NI (2020) Microalgae-bacteria interaction in palm oil mill effluent treatment. J Water Process Eng 35:101203. https://doi.org/10.1016/j.jwpe.2020.101203

    Article  Google Scholar 

  26. Ramanan R, Kang Z, Kim BH, Cho DH, Jin L, Oh HM, Kim HS (2015) Phycosphere bacterial diversity in green algae reveals an apparent similarity across habitats. Algal Res 8:140–144. https://doi.org/10.1016/j.algal.2015.02.003

    Article  Google Scholar 

  27. Randrianarison G, Ashraf MA (2017) Microalgae: a potential plant for energy production. Geol Ecol Landsc 1:104–120. https://doi.org/10.1080/24749508.2017.1332853

    Article  Google Scholar 

  28. Xiao-qian Z, Zhe-yu LI, Xiao-yan Z et al (2017) Advance in bacteria chemotaxis on microfluidic devices. Chin J Anal Chem 45:1734–1744. https://doi.org/10.1016/S1872-2040(17)61050-8

    Article  Google Scholar 

  29. Cooper MB, Smith AG (2015) Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr Opin Plant Biol 26:147–153. https://doi.org/10.1016/j.pbi.2015.07.003

    Article  PubMed  Google Scholar 

  30. Hong J, Luo Y, Mou M, Fu J, Zhang Y, Xue W, Xie T, Tao L, Lou Y, Zhu F (2019) Convolutional neural network-based annotation of bacterial type IV secretion system effectors with enhanced accuracy and reduced false discovery. Brief Bioinform 21:1825–1836. https://doi.org/10.1093/bib/bbz120

    Article  Google Scholar 

  31. Zhao R, Chen G, Liu L, Zhang W, Sun Y, Li B, Wang G (2020) Bacterial foraging facilitates aggregation of Chlamydomonas microsphaera in an organic carbon source-limited aquatic. Environ Pollut 259:113924. https://doi.org/10.1016/j.envpol.2020.113924

    Article  CAS  PubMed  Google Scholar 

  32. Khan MI, Shin JH, Kim JD (2018) The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Factories 17:36. https://doi.org/10.1186/s12934-018-0879-x

    Article  Google Scholar 

  33. Tandon P, Jin Q, Huang L (2017) A promising approach to enhance microalgae productivity by exogenous supply of vitamins. Microb Cell Factories 16:219. https://doi.org/10.1186/s12934-017-0834-2

    Article  CAS  Google Scholar 

  34. Lépinay A, Turpin V, Mondeguer F, Grandet-marchant Q (2018) First insight on interactions between bacteria and the marine diatom Haslea ostrearia: algal growth and metabolomic fingerprinting. Algal Res 31:395–405. https://doi.org/10.1016/j.algal.2018.02.023

    Article  Google Scholar 

  35. Chi W, Zheng L, He C et al (2017) Quorum sensing of microalgae associated marine Ponticoccus sp. PD-2 and its algicidal function regulation. AMB Express. https://doi.org/10.1186/s13568-017-0357-6

  36. Han S, Jeon MS, Heo YM et al (2020) Effect of Pseudoalteromonas sp. MEBiC 03485 on biomass production and sulfated polysaccharide biosynthesis in Porphyridium cruentum UTEX 161. Bioresour Technol. https://doi.org/10.1016/j.biortech.2020.122791

  37. Paddock MB, Fernández-Bayo JD, VanderGheynst JS (2020) The effect of the microalgae-bacteria microbiome on wastewater treatment and biomass production. Appl Microbiol Biotechnol 104:893–905. https://doi.org/10.1007/s00253-019-10246-x

    Article  CAS  PubMed  Google Scholar 

  38. Hai C, Vu T, Lee H et al (2017) Axenic cultures for microalgal biotechnology: establishment, assessment, maintenance, and applications. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2017.12.018

  39. Yao S, Lyu S, An Y, Lu J, Gjermansen C, Schramm A (2019) Microalgae-bacteria symbiosis in microalgal growth and biofuel production: a review. J Appl Microbiol 126:359–368. https://doi.org/10.1111/jam.14095

    Article  CAS  PubMed  Google Scholar 

  40. Palacios OA, Lopez BR, Bashan Y, de-Bashan LE (2019) Early changes in nutritional conditions affect formation of synthetic mutualism between Chlorella sorokiniana and the bacterium Azospirillum brasilense. Microb Ecol 77:980–992. https://doi.org/10.1007/s00248-018-1282-1

    Article  CAS  PubMed  Google Scholar 

  41. Trögl SRAPBJ (2020) New perspectives on the bioremediation of endocrine disrupting compounds from wastewater using algae-, bacteria- and fungi-based technologies. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-020-02691-3

  42. Lam TP, Lee T, Chen C, Chang J (2017) Strategies to control biological contaminants during microalgal cultivation in open ponds. Bioresour Technol 252:180–187. https://doi.org/10.1016/j.biortech.2017.12.088

    Article  CAS  PubMed  Google Scholar 

  43. Guo Z, Tong YW (2014) The interactions between Chlorella vulgaris and algal symbiotic bacteria under photoautotrophic and photoheterotrophic conditions. J Appl Phycol 26:1483–1492. https://doi.org/10.1007/s10811-013-0186-1

    Article  CAS  Google Scholar 

  44. Hoseinifar SH, Sun Y, Wang A et al (2018) Probiotics as means of diseases control in aquaculture, a review of current knowledge and future perspectives. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.02429

  45. Seymour JR, Amin SA, Raina JB, Stocker R (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2. https://doi.org/10.1038/nmicrobiol.2017.65

  46. Li Q, Ren Y, Fu X (2019) Inter-kingdom signaling between gut microbiota and their host. Cell Mol Life Sci 76:2383–2389. https://doi.org/10.1007/s00018-019-03076-7

    Article  CAS  PubMed  Google Scholar 

  47. Padmaperuma G, Kapoore RV, Gilmour DJ, Group F (2017) Microbial consortia: a critical look at microalgae co-cultures for enhanced biomanufacturing. Crit Rev Biotechnol 38:690–703. https://doi.org/10.1080/07388551.2017.1390728

    Article  CAS  PubMed  Google Scholar 

  48. Pacheco D, Rocha AC, Pereira L, Verdelhos T (2020) Microalgae water bioremediation: trends and hot topics. Appl Sci. https://doi.org/10.3390/app10051886

  49. Wei Z, Huang S, Zhang Y (2017) Characterization of extracellular polymeric substances produced during nitrate removal by a thermophilic bacterium Chelatococcus daeguensis TAD1 in batch cultures. RSC Adv 7:44265–44271. https://doi.org/10.1039/C7RA08147B

    Article  CAS  Google Scholar 

  50. Eigemann F, Hilt S, Salka I, Grossart H (2012) Bacterial community composition associated with freshwater algae: species specificity vs. dependency on environmental conditions and source community. FEMS Microbiol Ecol. https://doi.org/10.1111/1574-6941.12022

  51. Ryu BG, Kim W, Nam K, Kim S, Lee B, Park MS, Yang JW (2015) A comprehensive study on algal-bacterial communities shift during thiocyanate degradation in a microalga-mediated process. Bioresour Technol 191:496–504. https://doi.org/10.1016/j.biortech.2015.03.136

    Article  CAS  PubMed  Google Scholar 

  52. Dao GH, Wu GX, Wang XX et al (2018) Enhanced microalgae growth through stimulated secretion of indole acetic acid by symbiotic bacteria. Algal Res 33:345–351. https://doi.org/10.1016/j.algal.2018.06.006

    Article  Google Scholar 

  53. Yang W, Zheng Z, Lu K, Zheng C, du Y, Wang J, Zhu J (2019) Manipulating the phytoplankton community has the potential to create a stable bacterioplankton community in a shrimp rearing environment. Aquaculture. 520:734789. https://doi.org/10.1016/j.aquaculture.2019.734789

    Article  CAS  Google Scholar 

  54. Sandhya SV, Sandeep KP, Vijayan KK (2020) In vivo evaluation of microbial cocktail of microalgae-associated bacteria in larval rearing from zoea I to mysis I of the Indian white shrimp, Penaeus indicus. J Appl Phycol. https://doi.org/10.1007/s10811-020-02230-0

  55. Dobretsov S, Rittschof D (2020) Love at first taste: induction of larval settlement by marine microbes. Int J Mol Sci 21. https://doi.org/10.3390/ijms21030731

  56. Nie X, Mubashar M, Zhang S, Qin Y, Zhang X (2020) Current progress, challenges and perspectives in microalgae-based nutrient removal for aquaculture waste: a comprehensive review. J Clean Prod 277:124209. https://doi.org/10.1016/j.jclepro.2020.124209

    Article  CAS  Google Scholar 

  57. Zhang Z, Chen M, Li J, Zhao B, Wang L (2019) Significance of transparent exopolymer particles derived from aquatic algae in membrane fouling. Arab J Chem 13:4577–4585. https://doi.org/10.1016/j.arabjc.2019.10.004

    Article  CAS  Google Scholar 

  58. Shahid A, Malik S, Zhu H, Xu J, Nawaz MZ, Nawaz S, Asraful Alam M, Mehmood MA (2019) Cultivating microalgae in wastewater for biomass production, pollutant removal, and atmospheric carbon mitigation; a review. Sci Total Environ 704:135303. https://doi.org/10.1016/j.scitotenv.2019.135303

    Article  CAS  PubMed  Google Scholar 

  59. Sciences M (2019) Metabolic pathway analysis of nitrogen and phosphorus uptake by the consortium between C. vulgaris and P. aeruginosa. Int J Mol Sci. https://doi.org/10.3390/ijms20081978

  60. Cui Y, Chun S, Baek S et al (2020) Unique microbial module regulates the harmful algal bloom (Cochlodinium polykrikoides) and shifts the microbial community along the southern coast of Korea. Sci Total Environ 721:137725. https://doi.org/10.1016/j.scitotenv.2020.137725

    Article  CAS  PubMed  Google Scholar 

  61. Silva L, Ll M, Ivetic S et al (2021) Heterotrophic bacterioplankton responses in coral- and algae-dominated Red Sea reefs show they might benefit from future regime shift. Sci Total Environ 751:141628. https://doi.org/10.1016/j.scitotenv.2020.141628

    Article  CAS  PubMed  Google Scholar 

  62. Xiao R, Zheng Y (2016) Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnol Adv 34:1225–1244. https://doi.org/10.1016/j.biotechadv.2016.08.004

    Article  CAS  PubMed  Google Scholar 

  63. Wang J, Lei Z, Tian C, Liu S, Wang Q, Shimizu K, Zhang Z, Adachi Y, Lee DJ (2020) Ionic response of algal-bacterial granular sludge system during biological phosphorus removal from wastewater. Chemosphere. 264:128534. https://doi.org/10.1016/j.chemosphere.2020.128534

    Article  CAS  PubMed  Google Scholar 

  64. Zhang X, Ye X, Chen L, Zhao H, Shi Q, Xiao Y, Ma L, Hou X, Chen Y, Yang F (2020) Functional role of bloom-forming cyanobacterium Planktothrix in ecologically shaping aquatic environments. Sci Total Environ 710:136314. https://doi.org/10.1016/j.scitotenv.2019.136314

    Article  CAS  PubMed  Google Scholar 

  65. Amin SA, Hmelo LR, Van Tol HM et al (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 522:98–101. https://doi.org/10.1038/nature14488

    Article  CAS  PubMed  Google Scholar 

  66. Leong WH, Lim JW, Lam MK, Uemura Y, Ho CD, Ho YC (2018) Co-cultivation of activated sludge and microalgae for the simultaneous enhancements of nitrogen-rich wastewater bioremediation and lipid production. J Taiwan Inst Chem Eng 87:216–224. https://doi.org/10.1016/j.jtice.2018.03.038

    Article  CAS  Google Scholar 

  67. Gude S, Taga ME (2020) Multi-faceted approaches to discovering and predicting microbial nutritional interactions. Curr Opin Biotechnol 62:58–64. https://doi.org/10.1016/j.copbio.2019.08.005

    Article  CAS  PubMed  Google Scholar 

  68. Schoffman H, Lis H, Shaked Y, Keren N (2016) Iron-nutrient interactions within phytoplankton. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.01223

  69. Kurth C, Wasmuth I, Wichard T, Pohnert G, Nett M (2019) Algae induce siderophore biosynthesis in the freshwater bacterium Cupriavidus necator H16. BioMetals. 32:77–88. https://doi.org/10.1007/s10534-018-0159-6

    Article  CAS  PubMed  Google Scholar 

  70. Leong WH, Azella Zaine SN, Ho YC, Uemura Y, Lam MK, Khoo KS, Kiatkittipong W, Cheng CK, Show PL, Lim JW (2019) Impact of various microalgal-bacterial populations on municipal wastewater bioremediation and its energy feasibility for lipid-based biofuel production. J Environ Manag 249:109384. https://doi.org/10.1016/j.jenvman.2019.109384

    Article  CAS  Google Scholar 

  71. Mukherjee S, Bassler BL (2019) Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol 17:371–382. https://doi.org/10.1038/s41579-019-0186-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Prescott RD, Decho AW (2019) Flexibility and adaptability of quorum sensing in nature. Trends Microbiol 28:436–444. https://doi.org/10.1016/j.tim.2019.12.004

    Article  CAS  Google Scholar 

  73. Mangwani N, Dash HR, Chauhan A, Das S (2012) Bacterial quorum sensing: functional features and potential applications in biotechnology. J Mol Microbiol Biotechnol 22:215–227. https://doi.org/10.1159/00034184

    Article  CAS  PubMed  Google Scholar 

  74. Jatt AN, Tang K, Liu J, Zhang Z, Zhang XH (2015) Quorum sensing in marine snow and its possible influence on production of extracellular hydrolytic enzymes in marine snow bacterium Pantoea ananatis B9. FEMS Microbiol Ecol 91:1–13. https://doi.org/10.1093/femsec/fiu030

    Article  CAS  PubMed  Google Scholar 

  75. Singh AA, Singh AK (2020) Bacteria associated with marine macroorganisms as potential source of quorum-sensing antagonists. J Basic Microbiol. https://doi.org/10.1002/jobm.202000231

  76. Zhang B, Li W, Guo Y, Zhang Z, Shi W, Cui F, Lens PNL, Tay JH (2020) Microalgal-bacterial consortia: from interspecies interactions to biotechnological applications. Renew Sust Energ Rev 118:109563. https://doi.org/10.1016/j.rser.2019.109563

    Article  Google Scholar 

  77. Li Q, Gu P, Zhang H et al (2019) Response of submerged macrophytes and leaf biofilms to the decline phase of Microcystis aeruginosa: antioxidant response, ultrastructure, microbial properties, and potential mechanism. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.134325

  78. Girard L (2019) Quorum sensing in Vibrio spp.: the complexity of multiple signalling molecules in marine and aquatic environments. Crit Rev Microbiol. https://doi.org/10.1080/1040841X.2019.1624499

  79. Durham BP, Sharma S, Luo H, Smith CB, Amin SA, Bender SJ, Dearth SP, van Mooy BAS, Campagna SR, Kujawinski EB, Armbrust EV, Moran MA (2015) Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci U S A 112:453–457. https://doi.org/10.1073/pnas.1413137112

    Article  CAS  PubMed  Google Scholar 

  80. Kazamia E, Czesnick H, Van Nguyen TT et al (2012) Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria. Environ Microbiol 14:1466–1476. https://doi.org/10.1111/j.1462-2920.2012.02733.x

    Article  CAS  PubMed  Google Scholar 

  81. Wang M, Chen S, Zhou W, Yuan W, Wang D (2020) Algal cell lysis by bacteria: a review and comparison to conventional methods. Algal Res 46:101794. https://doi.org/10.1016/j.algal.2020.101794

    Article  Google Scholar 

  82. Lopez BR, Palacios OA, Bashan Y, Hernández-Sandoval FE, de-Bashan LE (2019) Riboflavin and lumichrome exuded by the bacterium Azospirillum brasilense promote growth and changes in metabolites in Chlorella sorokiniana under autotrophic conditions. Algal Res 44:101696. https://doi.org/10.1016/j.algal.2019.101696

    Article  Google Scholar 

  83. Pagnussat LA, Maroniche G, Curatti L, Creus C (2020) Auxin-dependent alleviation of oxidative strecass and growth promotion of Scenedesmus obliquus C1S by Azospirillum brasilense. Algal Res 47:101839. https://doi.org/10.1016/j.algal.2020.101839

    Article  Google Scholar 

  84. Rajapitamahuni S, Bachani P, Sardar RK, Mishra S (2019) Co-cultivation of siderophore-producing bacteria Idiomarina loihiensis RS14 with Chlorella variabilis ATCC 12198, evaluation of micro-algal growth, lipid, and protein content under iron starvation. J Appl Phycol 31:29–39. https://doi.org/10.1007/s10811-018-1591-2

    Article  CAS  Google Scholar 

  85. Santos CA, Reis A (2014) Microalgal symbiosis in biotechnology. Appl Microbiol Biotechnol 98:5839–5846. https://doi.org/10.1007/s00253-014-5764-x

    Article  CAS  PubMed  Google Scholar 

  86. Amin SA, Green DH, Hart MC, Ku FC (2009) Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Proc Natl Acad Sci 106:17071–17076. https://doi.org/10.1073/pnas.0905512106

    Article  PubMed  PubMed Central  Google Scholar 

  87. Leyva LA, Bashan Y, Mendoza A, Luz E (2014) Accumulation fatty acids of in Chlorella vulgaris under heterotrophic conditions in relation to activity of acetyl-CoA carboxylase, temperature, and co-immobilization with Azospirillum brasilense. Naturwissenschaften. 101:819–830. https://doi.org/10.1007/s00114-014-1223-x

    Article  CAS  PubMed  Google Scholar 

  88. Choix FJ, Luz E, Bashan Y (2012) Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense: II. Heterotrophic conditions. Enzym Microb Technol. https://doi.org/10.1016/j.enzmictec.2012.07.012

  89. Zhang C, Li Q, Fu L, Zhou D, Crittenden JC (2018) Quorum sensing molecules in activated sludge could trigger microalgae lipid synthesis. Bioresour Technol 263:576–582. https://doi.org/10.1016/j.biortech.2018.05.045

    Article  CAS  PubMed  Google Scholar 

  90. Laganenka L, Sourjik V (2018) Autoinducer 2-dependent Escherichia coli biofilm formation is enhanced in a dual-species coculture. Appl Environ Microbiol 84. https://doi.org/10.1128/AEM.02638-17

  91. Zhao J, Li X, Hou X et al (2019) Widespread existence of quorum sensing inhibitors in marine bacteria: potential drugs to combat pathogens with novel strategies. Mar Drugs. https://doi.org/10.3390/md17050275

  92. Meschwitz SM, Teasdale ME, Mozzer A, Martin N, Liu J, Forschner-Dancause S, Rowley DC (2019) Antagonism of quorum sensing phenotypes by analogs of the marine bacterial secondary. Mar Drugs 17. https://doi.org/10.3390/md17070389

  93. Hu Z, Qi Y, Zhao L, Chen G (2018) Interactions between microalgae and microorganisms for wastewater remediation and biofuel production. Waste Biomass Valoriz 10:3907–3919. https://doi.org/10.1007/s12649-018-0325-7

    Article  CAS  Google Scholar 

  94. Zhou D, Zhang C, Fu L et al (2017) Responses of the microalga Chlorophyta sp. to bacterial quorum sensing molecules (N-acylhomoserine lactones): aromatic protein-induced self-aggregation. Environ Sci Technol. https://doi.org/10.1021/acs.est.7b00355

  95. Natrah FMI, Kenmegne MM, Wiyoto W, Sorgeloos P, Bossier P, Defoirdt T (2011) Effects of micro-algae commonly used in aquaculture on acyl-homoserine lactone quorum sensing. Aquaculture. 317:53–57. https://doi.org/10.1016/j.aquaculture.2011.04.038

    Article  CAS  Google Scholar 

  96. Ghimire U, Nandimandalam H, Martinez-guerra E, Gude VG (2019) Wetlands for wastewater treatment. Water Environ Fed 91:1378–1389. https://doi.org/10.1002/wer.1232

    Article  CAS  Google Scholar 

  97. Kohlheb N, Van Afferden M, Lara E et al (2020) Assessing the life-cycle sustainability of algae and bacteria-based wastewater treatment systems: high-rate algae pond and sequencing batch reactor. J Environ Manag 264:110459. https://doi.org/10.1016/j.jenvman.2020.110459

    Article  CAS  Google Scholar 

  98. Victoria M, Capson-tojo G, Gal A et al (2020) Microalgae-bacteria consortia in high-rate ponds for treating urban wastewater: elucidating the key state indicators under dynamic conditions. J Environ Manag 261:110244. https://doi.org/10.1016/j.jenvman.2020.110244

    Article  CAS  Google Scholar 

  99. Loganathan BG, Orsat V, Lefsrud M (2020) Phycoremediation and valorization of synthetic dairy wastewater using microalgal consortia of Chlorella variabilis and Scenedesmus obliquus. Environ Technol 1–14. https://doi.org/10.1080/09593330.2020.1725143

  100. Ji X, Li H, Zhang J, Saiyin H, Zheng Z (2019) The collaborative effect of Chlorella vulgaris-Bacillus licheniformis consortia on the treatment of municipal water. J Hazard Mater 365:483–493. https://doi.org/10.1016/j.jhazmat.2018.11.039

    Article  CAS  PubMed  Google Scholar 

  101. Tait K, White DA, Kimmance SA, Tarran G, Rooks P, Jones M, Llewellyn CA (2019) Characterisation of bacteria from the cultures of a Chlorella strain isolated from textile wastewater and their growth enhancing effects on the axenic cultures of Chlorella vulgaris in low nutrient media. Algal Res 44:101666. https://doi.org/10.1016/j.algal.2019.101666

    Article  Google Scholar 

  102. Mujtaba G, Lee K (2016) Advanced treatment of wastewater using symbiotic co-culture of microalgae and bacteria. Appl Chem Eng. https://doi.org/10.14478/ace.2016.1002

  103. Lee CS, Oh HSHM, Oh HSHM et al (2016) Two-phase photoperiodic cultivation of algal-bacterial consortia for high biomass production and efficient nutrient removal from municipal wastewater. Bioresour Technol 200:867–875. https://doi.org/10.1016/j.biortech.2015.11.007

    Article  CAS  PubMed  Google Scholar 

  104. Ferro L, Colombo M, Posadas E et al (2019) Elucidating the symbiotic interactions between a locally isolated microalga Chlorella vulgaris and its co-occurring bacterium Rhizobium sp. in synthetic municipal wastewater. J Appl Phycol. https://doi.org/10.1007/s10811-019-1741-1

  105. Ho S-H, Chen Y-D, Qu W-Y et al (2019) Algal culture and biofuel production using wastewater. Biofuels Algae. https://doi.org/10.1016/B978-0-444-64192-2.00008-1

  106. Wang S, Liu J, Li C, Chung BM (2018) Efficiency of Nannochloropsis oculata and Bacillus polymyxa symbiotic composite at ammonium and phosphate removal from synthetic wastewater. Environ Technol 40:2494–2503. https://doi.org/10.1080/09593330.2018.1444103

    Article  CAS  PubMed  Google Scholar 

  107. Gonçalves AL, Pires JCM, Simões M (2017) A review on the use of microalgal consortia for wastewater treatment. Algal Res 24:403–415. https://doi.org/10.1016/j.algal.2016.11.008

    Article  Google Scholar 

  108. Zhao X, Zhou Y, Huang S, Qiu D, Schideman L, Chai X, Zhao Y (2014) Characterization of microalgae-bacteria consortium cultured in landfill leachate for carbon fixation and lipid production. Bioresour Technol 156:322–328. https://doi.org/10.1016/j.biortech.2013.12.112

    Article  CAS  PubMed  Google Scholar 

  109. Ren HY, Liu BF, Kong F, Zhao L, Ren N (2015) Hydrogen and lipid production from starch wastewater by co-culture of anaerobic sludge and oleaginous microalgae with simultaneous COD, nitrogen and phosphorus removal. Water Res 85:404–412. https://doi.org/10.1016/j.watres.2015.08.057

    Article  CAS  PubMed  Google Scholar 

  110. Qi W, Mei S, Yuan Y, Li X, Tang T, Zhao Q, Wu M, Wei W, Sun Y (2018) Enhancing fermentation wastewater treatment by co-culture of microalgae with volatile fatty acid- and alcohol-degrading bacteria. Algal Res 31:31–39. https://doi.org/10.1016/j.algal.2018.01.012

    Article  Google Scholar 

  111. Higgins BT (2017) Algal-bacterial synergy in treatment of winery wastewater. NPJ Clean Water. https://doi.org/10.1038/s41545-018-0005-y

  112. Ye J, Song Z, Wang L, Zhu J (2016) Metagenomic analysis of microbiota structure evolution in phytoremediation of a swine lagoon wastewater. Bioresour Technol 219:439–444. https://doi.org/10.1016/j.biortech.2016.08.013

    Article  CAS  PubMed  Google Scholar 

  113. Bernard O, Shoener BD, Schramm SM et al (2019) Microalgae and cyanobacteria modeling in water resource recovery facilities: a critical review. Water Res X 2:100024. https://doi.org/10.1016/j.wroa.2018.100024

    Article  CAS  PubMed  Google Scholar 

  114. Quijano G, Arcila JS, Buitrón G (2017) Microalgal-bacterial aggregates: applications and perspectives for wastewater treatment. Biotechnol Adv 35:772–781. https://doi.org/10.1016/j.biotechadv.2017.07.003

    Article  CAS  PubMed  Google Scholar 

  115. Zhai J, Li X, Li W, Rahaman MH, Zhao Y, Wei B, Wei H (2017) Optimization of biomass production and nutrients removal by Spirulina platensis from municipal wastewater. Ecol Eng 108:83–92. https://doi.org/10.1016/j.ecoleng.2017.07.023

    Article  Google Scholar 

  116. Zhu S, Wu H, Wu C, Qiu G, Feng C, Wei C (2019) Structure and function of microbial community involved in a novel full-scale prefix oxic coking wastewater treatment O/H/O system. Water Res 164:114963. https://doi.org/10.1016/j.watres.2019.114963

    Article  CAS  PubMed  Google Scholar 

  117. Nagarajan D, Lee D, Chang J (2019) Integration of anaerobic digestion and microalgal cultivation for digestate bioremediation and biogas upgrading. Bioresour Technol 290:121804. https://doi.org/10.1016/j.biortech.2019.121804

    Article  CAS  PubMed  Google Scholar 

  118. Gram L (2018) A novel microbial culture chamber co-cultivation system to study algal-bacteria interactions using Emiliania huxleyi and Phaeobacter inhibens as model organisms. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.01705

  119. Shirzad M, Karimi M, Silva JAC, Rodrigues E (2019) Moving bed reactors : challenges and progress of experimental and theoretical studies in a century of research. Ind Eng Chem Res 58:9179–9198. https://doi.org/10.1021/acs.iecr.9b01136

    Article  CAS  Google Scholar 

  120. Orfanos AG, Manariotis ID (2019) Algal biofilm ponds for polishing secondary effluent and resource recovery. J Appl Phycol 31:1765–1772. https://doi.org/10.1007/s10811-018-1731-8

    Article  CAS  Google Scholar 

  121. Keyvan A, Ahmadzadeh H, Farhad A et al (2016) Potential use of algae for heavy metal bioremediation, a critical review. J Environ Manag 181:817–831. https://doi.org/10.1016/j.jenvman.2016.06.059

    Article  CAS  Google Scholar 

  122. Gentili FG, Fick J (2017) Algal cultivation in urban wastewater: an efficient way to reduce pharmaceutical pollutants. J Appl Phycol 29:255–262. https://doi.org/10.1007/s10811-016-0950-0

    Article  CAS  PubMed  Google Scholar 

  123. Sutherland DL, Ralph PJ (2019) Microalgal bioremediation of emerging contaminants-opportunities and challenges. Water Res 164:114921. https://doi.org/10.1016/j.watres.2019.114921

    Article  CAS  PubMed  Google Scholar 

  124. Asselborn V, Fernández C, Zalocar Y, Parodi ER (2015) Effects of chlorpyrifos on the growth and ultrastructure of green algae, Ankistrodesmus gracilis. Ecotoxicol Environ Saf 120:334–341. https://doi.org/10.1016/j.ecoenv.2015.06.015

    Article  CAS  PubMed  Google Scholar 

  125. Arbib Z, De Godos I, Ruiz J, Perales JA (2017) Optimization of pilot high rate algal ponds for simultaneous nutrient removal and lipids production. Sci Total Environ 589:66–72. https://doi.org/10.1016/j.scitotenv.2017.02.206

    Article  CAS  PubMed  Google Scholar 

  126. Boshir M, Zhou JL, Hao H et al (2016) Progress in the biological and chemical treatment technologies for emerging contaminant removal from wastewater: a critical review. J Hazard Mater 323:274–298. https://doi.org/10.1016/j.jhazmat.2016.04.045

    Article  CAS  Google Scholar 

  127. Pal S, Banat F, Almansoori A, Haija MA (2016) Review of technologies for biotreatment of refinery wastewaters: progress, challenges and future opportunities. Environ Technol Rev 5:12–38. https://doi.org/10.1080/21622515.2016.1164252

    Article  CAS  Google Scholar 

  128. Jassim SAA, Limoges RG (2016) Bacteriophage biocontrol in wastewater treatment. World J Microbiol Biotechnol 32:70. https://doi.org/10.1007/s11274-016-2028-1

    Article  CAS  PubMed  Google Scholar 

  129. Ratzke C, Barrere J, Gore J (2020) Strength of species interactions determines biodiversity and stability in microbial communities. Nat Ecol Evol 4:376–383. https://doi.org/10.1038/s41559-020-1099-4

    Article  PubMed  Google Scholar 

  130. Decho AW, Gutierrez T (2017) Microbial extracellular polymeric substances (EPSs) in ocean systems. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.00922

  131. Marella TK, López-pacheco IY, Parra- R (2020) Wealth from waste: diatoms as tools for phycoremediation of wastewater and for obtaining value from the biomass. Sci Total Environ 724:137960. https://doi.org/10.1016/j.scitotenv.2020.137960

    Article  CAS  PubMed  Google Scholar 

  132. Liu J, Wu Y, Wu C, Muylaert K, Vyverman W, Yu HQ, Muñoz R, Rittmann B (2017) Advanced nutrient removal from surface water by a consortium of attached microalgae and bacteria: a review. Bioresour Technol 241:1127–1137. https://doi.org/10.1016/j.biortech.2017.06.054

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the Basic Research Program for Natural Science of Shaanxi Province (2020JQ-714) “Study on the Growth-promoting Mechanism of Microalgae Symbiotic Bacteria on Chlorella in Wastewater Based on Quorum Sensing.”

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Sial, A., Zhang, B., Zhang, A. et al. Microalgal–Bacterial Synergistic Interactions and Their Potential Influence in Wastewater Treatment: a Review. Bioenerg. Res. 14, 723–738 (2021). https://doi.org/10.1007/s12155-020-10213-9

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