Improvement of the Cd removal efficiency of a filamentous cyanobacterium Leptolyngbya sp. XZ1 through co-culture with Bacillus sp. S1

Springer Science and Business Media LLC - Tập 35 - Trang 2935-2944 - 2023
Changho Ri1,2, Yue Tao1, Jiawei Tu1, Xinyue Li1, Sijia She1, Lianghui Hou1, Yaojia Fu1, Lanzhou Chen1
1School of Resource and Environmental Sciences, Hubei Key Laboratory of Biomass-Resources Chemistry and Environmental Biotechnology, Wuhan University, Wuhan, People’s Republic of China
2Faculty of Life Science, Kim Il Sung University, Pyongyang, Democratic People’s Republic of Korea

Tóm tắt

The co-culture of cyanobacteria and heterotrophic bacteria can utilize the advantages of both bacteria, effectively remove pollutants and relieve the feedback inhibition effect in algae culture; however, little information is available in heavy metal removal. In this study, a filamentous cyanobacterium, Leptolyngbya sp. XZ1, isolated from biological soil crusts and four heterotrophic bacterial strains, namely, Y3, Y4, S1 and T2, isolated from the phycosphere were co-inoculated into BG-11 media containing Cd. Amongst co-culture systems, Leptolyngbya + S1 showed the highest Cd removal efficiencies of 93.2%, 71.8%, 60.7%, 56.8% and 41.0% at initial Cd concentrations of 2, 5, 10, 20 and 50 mg L−1, respectively. In this co-culture system, Cd adsorbed on the cell wall was increased by 42.8%, 52.9%, 50.0% and 22.6%, and the intracellular Cd was decreased by 37.9%, 37.0%, 51.0% and 50.6% at initial Cd concentrations of 5, 10, 20 and 50 mg L−1, respectively, compared with the Leptolyngbya monoculture. Under Cd stress, the biomass, extracellular polymeric substances (EPS)-polysaccharides and photosystem II activity of Leptolyngbya sp. XZ1 were increased by co-culture with Bacillus sp. S1. In addition, the Cd stress on Leptolyngbya was alleviated by co-culture with S1 as proven by the superoxide dismutase (SOD) activity, malondialdehyde (MDA) content, scanning electron microscopy (SEM) images, soluble protein content and SDS-PAGE analysis. Results indicated that the cyanobacteria-heterotrophic bacteria co-culture system can be used as an effective bioremediation method to remove heavy metals from aqueous solution.

Tài liệu tham khảo

Angelis S, Novak AC, Sydney EB, Soccol VT, Carvalho JC, Pandey A, Noseda MD, Tholozan JL, Lorquin J, Soccol CR (2012) Co-culture of microalgae, cyanobacteria, and macromycetes for exopolysaccharides production: Process preliminary optimization and partial characterization. Appl Biochem Biotech 167:1092–1106 Azizi SN, Colagar AH, Hafeziyan SM (2012) Removal of Cd(II) from aquatic system using Oscillatoria sp. biosorbent. Sci World J 2012:347053 Badr OAM, EL-Shawaf IIS, El-Garhy HAS, Moustafa MMA, Ahmed-Farid OA (2019) Antioxidant activity and phycoremediation ability of four cyanobacterial isolates obtained from a stressed aquatic system. Mol Phylogenet Evol 134:300-310 Baścik RA, Tomaszewska E, Labuda K, Tukaj Z (2009) The Effect of Zn and Mn on the Toxicity of Cd to the green microalga Desmodesmus armatus cultured at ambient and elevated (2%) CO2 concentrations. Pol J Environ Stud 18:775–780 Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 Chen H, Fu L, Luo L, Lu J, White WL, Hu Z (2012) Induction and resuscitation of the viable but nonculturable state in a cyanobacteria-lysing bacterium isolated from cyanobacterial bloom. Microb Ecol 63:64–73 Clares ME, Guerrero MG, García-González M (2015) Cadmium removal by Anabaena sp. ATCC 33047 immobilized in polyurethane foam. Int J Environ Sci Technol 12:1793–1798 Cui L, Fan L, Li Z, Wang J, Chen R, Zhang Y, Cheng J, Wu X, Li J, Yin H, Zeng W, Shen L (2021) Characterization of extracellular polymeric substances from Synechocystis sp. PCC6803 under Cd(II), Pb(II) and Cr(VI) stress. J Environ Chem Eng 9:105347 Damatac AM, Cao EP (2022) Identification and diversity assessment of cyanobacterial communities from some mine tailing sites in Benguet Province, Philippines using isolation-dependent and isolation-independent methods. Environ Dev Sustain 24:1166–1187 Danouche M, El Ghatchouli N, Arroussi H (2022) Overview of the management of heavy metals toxicity by microalgae. J Appl Phycol 34:475–488 D’Costa PM, Kunkolienkar RSS, Naik AG, Naik RK, Roy R (2019) The response of Prorocentrum sigmoides and its associated culturable bacteria to metals and organic pollutants. J Basic Microbiol 59:979–991 Ding J, Chen W, Zhang Z, Qin F, Jiang J, He A, Sheng GD (2021) Enhanced removal of cadmium from wastewater with coupled biochar and Bacillus subtilis. Water Sci Technol 83:2075–2086 Dixit S, Singh DP (2014) An evaluation of phycoremediation potential of cyanobacterium Nostoc muscorum: characterization of heavy metal removal efficiency. J Appl Phycol 26:1331–1342 Fawzy MA (2016) Phycoremediation and adsorption isotherms of cadmium and copper ions by Merismopedia tenuissima and their effect on growth and metabolism. Environ Toxicol Phar 46:116–121 Gao L, Shen G, Zhang J (2015) Accumulation and distribution of cadmium in flue-cured tobacco and its impact on rhizosphere microbial community. Pol J Environ Stud 24:1563–1569 Giannakoula A, Moustakas M, Mylona P, Papadakis I, Yupsanis T (2008) Aluminum tolerance in maize is correlated with increased levels of mineral nutrients, carbohydrates and proline, and decreased levels of lipid peroxidation and Al accumulation. J Plant Physiol 165:385–396 Giannopolitis CN, Ries SK (1977) Superoxide dismutases. Plant Physiol 59:309–314 Goswami S, Syiem MB, Pakshirajan K (2015) Cadmium removal by Anabaena doliolum Ind1 isolated from a coal mining area in Meghalaya, India: associated structural and physiological alterations. Environ Eng Res 20:41–50 Gupta A, Singhal GS (1995) Inhibition of PS II activity by copper and its effect on spectral properties on intact cells in Anacystis nidulans. Environ Exp Bot 35:435–439 Hazra P, Kesh GS (2017) Isolation and purification of phycocyanin from cyanobacteria of a mangrove forest. Appl Biol Chem 60:631–636 Heimann K, Cirés S (2015) N2-Fixing cyanobacteria: Ecology and biotechnological applications. In: Kim S (ed) Handbook of Marine Microalgae. Academic Press, Boston, pp 501–515 Hussein MH, Hamouda RA, Elhadary AMA, Abuelmagd MA, Ali S, Rizwan M (2019) Characterization and chromium biosorption potential of extruded polymeric substances from Synechococcus mundulus induced by acute dose of gamma irradiation. Environ Sci Pollut Res 26:31998–32012 IARC (2012) Arsenic, metals, fibres, and dusts. IARC Monogr Eval Carcinog Risks Humans 100:11–465 Ivanova J, Stoyancheva G, Pouneva I (2014) Lysis of Antarctic algal strains by bacterial pathogen. Antonie Van Leeuwenhoek 105:997–1005 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 Jiang J, Zhang N, Yang X, Song L, Yang S (2016) Toxic metal biosorption by macrocolonies of cyanobacterium Nostoc sphaeroides Kützing. J Appl Phycol 28:2265–2277 Kim M, Shin B, Lee J, Park HY, Park W (2019) Culture-independent and culture-dependent analyses of the bacterial community in the phycosphere of cyanobloom-forming Microcystis aeruginosa. Sci Rep 9:20416 King J, Laemmli UK (1971) Polypeptides of the tail fibres of bacteriophage T4. J Mol Biol 62:465–477 Koedrith P, Kim H, Weon J, Seo YR (2013) Toxicogenomic approaches for understanding molecular mechanisms of heavy metal mutagenicity and carcinogenicity. Int J Hyg Environ Health 216:587–598 Kumar D, Dhar DW, Pabbi S, Kumar N, Walia S (2014) Extraction and purification of C-phycocyanin from Spirulina platensis (CCC540). Indian J Plant Physiol 19:184–188 Li T, Jiang L, Hu Y, Paul JT, Zuniga C, Zengler K, Betenbaugh MJ (2020) Creating a synthetic lichen: Mutualistic co-culture of fungi and extracellular polysaccharide-secreting cyanobacterium Nostoc PCC 7413. Algal Res 45:101755 Lin S, Pan J, Li Z, Liu X, Tan J, Yang H (2014) Characterization of an algicidal bacterium Brevundimonas J4 and chemical defense of Synechococcus sp. BN60 against bacterium J4. Harmful Algae 37:1–7 Nambiar KR, Bokil SD (1981) Luxury uptake of nitrogen in flocculating algal-bacterial system. Water Res 15:667–669 Peng H, De-Bashan LE, Higgins BT (2021) Comparison of algae growth and symbiotic mechanisms in the presence of plant growth promoting bacteria and non-plant growth promoting bacteria. Algal Res 53:102156 Raghavan PS, Potnis AA, Bhattacharyya K, Salaskar DA, Rajaram H (2020) Axenic cyanobacterial (Nostoc muscorum) biofilm as a platform for Cd(II) sequestration from aqueous solutions. Algal Res 46:101778 Rahman Z, Singh VP (2020) Bioremediation of toxic heavy metals (THMs) contaminated sites: concepts, applications and challenges. Environ Sci Pollut R 27:27563–27581 Raj K, Sardar UR, Bhargavi E, Devi I, Bhunia B, Tiwari ON (2018) Advances in exopolysaccharides based bioremediation of heavy metals in soil and water: A critical review. Carbohydr Polym 199:353–364 Ruan G, Mi W, Yin X, Song G, Bi Y (2022) Molecular responses mechanism of Synechocystis sp. PCC 6803 to cadmium stress. Water 14:4032 Saffar B, Mehri Ghahfarrokhi A, Mahnam K, Mobini-Dehkordi M (2015) Improvement of Cd2+ uptake ability of SmtA protein by Lys/Cys mutation; experimental and theoretical studies. J Biomol Struct Dyn 33:2347–2359 Selmi A, Khiari R, Snoussi A, Bouzouita N (2021) Analysis of minerals and heavy metals using ICP-OES and FTIR techniques in two red seaweeds (Gymnogongrus griffithsiae and Asparagopsis taxiformis) from Tunisia. Biol Trace Elem Res 199:2342–2350 Shen L, Li Z, Wang J, Liu A, Li Z, Yu R, Wu X, Liu Y, Li J, Zeng W (2018) Characterization of extracellular polysaccharide/protein contents during the adsorption of Cd(II) by Synechocystis sp. PCC6803. Environ Sci Pollut Res 25:20713–20722 Sher D, Thompson JW, Kashtan N, Croal L, Chisholm SW (2011) Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria. Isme J 5:1125–1132 Sial A, Zhang B, Zhang A, Liu K, Imtiaz SA, Yashir N (2021) Microalgal–bacterial synergistic interactions and their potential influence in wastewater treatment: a review. Bioenerg Res 14:723–738 Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: A precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:529 Singh MPVV, Prasad SM, Singh VP, Singh M (2015) Antioxidant system against active oxygen species in cyanobacterium Aphanothece stagnina: Response to excess light under cadmium stress. Proc Nat Acad Sci India B 85:535–543 Singh S, Singh A, Srivastava PK, Prasad SM (2018) Cadmium toxicity and its amelioration by kinetin in tomato seedlings vis-à-vis ascorbate-glutathione cycle. J Photochem Photobiol B 178:76–84 Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R (2011) Consortia of cyanobacteria/microalgae and bacteria: Biotechnological potential. Biotechnol Adv 29:896–907 Sun T, Xu L, Wu L, Song Z, Chen L, Zhang W (2017) Identification of a new target slr0946 of the response regulator Sll0649 involving cadmium tolerance in Synechocystis sp. PCC 6803. Front Microbiol 8:1582 Surosz W, Palinska KA (2004) Effects of heavy-metal stress on cyanobacterium Anabaena flos-aquae. Arch Environ Contam Toxicol 48:40–48 Zamora LC, Negrete BD, Figueroa F, Zamora LE, Ni M, Alexis F, Guerrero VH (2021) Heavy metal water pollution: A fresh look about hazards, novel and conventional remediation methods. Environ Technol Innov 22:101504 Zeng G, He Y, Liang D, Wang F, Luo Y, Yang H, Wang Q, Wang J, Gao P, Wen X, Yu C, Sun D (2022) Adsorption of heavy metal ions copper, cadmium and nickel by Microcystis aeruginosa. Int J Environ Res Public Health 19:13867 Zhou Q, Yang N, Li Y, Ren B, Ding X, Bian H, Yao X (2020) Total concentrations and sources of heavy metal pollution in global river and lake water bodies from 1972 to 2017. Glob Ecol Conserv 22:e925