Abstract
Since antibiotics show hormesis effects in cyanobacteria at the nanogram per liter concentration level, the possibility for two commonly used antibiotics (sulfamethoxazole and tetracycline) to increase lipid productivity in Synechocystis sp. PCC 6803 was assessed in the present study. The two target antibiotics significantly promoted (p < 0.05) the biofuel productivity of Synechocystis sp. PCC 6803 through the increase of both biomass and lipid content. Sulfamethoxazole and tetracycline significantly stimulated (p < 0.05) cyanobacterial growth by upregulating proteins related to cell differentiation, cell division, and gene expression; significantly enhanced (p < 0.05) the photosynthetic activity by upregulating photosynthesis-related proteins; and significantly increased (p < 0.05) the lipid content in cyanobacterial cells by downregulating carbohydrate catabolic proteins and carbohydrate transport proteins. Due to the altered expression pattern of biosynthesis-related proteins, the two antibiotics increased the proportion of monounsaturated fatty acids, while tetracycline reduced the proportions of saturated and polyunsaturated fatty acids. The changes in fatty acid composition may improve the combustion performance of biofuel. This study provided insights into the application of antibiotics in cyanobacteria-based biofuel production.
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References
Aderemi AO, Novais SC, Lemos MFL, Alves LM, Hunter C, Pahl O (2018) Oxidative stress responses and cellular energy allocation changes in microalgae following exposure to widely used human antibiotics. Aquat Toxicol 203:130–139. https://doi.org/10.1016/j.aquatox.2018.08.008
Adu-Mensah D, Mei D, Zuo L, Zhang Q, Wang J (2019) A review on partial hydrogenation of biodiesel and its influence on fuel properties. Fuel 251:660–668. https://doi.org/10.1016/j.fuel.2019.04.036
Anahas AMP, Muralitharan G (2015) Isolation and screening of heterocystous cyanobacterial strains for biodiesel production by evaluating the fuel properties from fatty acid methyl ester (FAME) profiles. Bioresour Technol 184:9–17. https://doi.org/10.1016/j.biortech.2014.11.003
Aslam A, Thomas-Hall SR, Manzoor M, Jabeen F, Iqbal M, Uz ZQ, Schenk PM, Asif TM (2018) Mixed microalgae consortia growth under higher concentration of CO2 from unfiltered coal fired flue gas: fatty acid profiling and biodiesel production. J Photochem Photobiol B 179:126–133. https://doi.org/10.1016/j.jphotobiol.2018.01.003
Ben Y, Fu C, Hu M, Liu L, Wong MH, Zheng C (2019) Human health risk assessment of antibiotic resistance associated with antibiotic residues in the environment: a review. Environ Res 169:483–493. https://doi.org/10.1016/j.envres.2018.11.040
Bharte S, Desai K (2019) The enhanced lipid productivity of Chlorella minutissima and Chlorella pyrenoidosa by carbon coupling nitrogen manipulation for biodiesel production. Environ Sci Pollut Res 26:3492–3500. https://doi.org/10.1007/s11356-018-3757-5
Biošić M, Mitrevski M, Babić S (2017) Environmental behavior of sulfadiazine, sulfamethazine, and their metabolites. Environ Sci Pollut Res 24:9802–9812. https://doi.org/10.1007/s11356-017-8639-8
Bland E, Angenent LT (2016) Pigment-targeted light wavelength and intensity promotes efficient photoautotrophic growth of Cyanobacteria. Bioresour Technol 216:579–586. https://doi.org/10.1016/j.biortech.2016.05.116
Casazza AA, Ferrari PF, Aliakbarian B, Converti A, Perego P (2015) Effect of UV radiation or titanium dioxide on polyphenol and lipid contents of Arthrospira (Spirulina) platensis. Algal Res 12:308–315. https://doi.org/10.1016/j.algal.2015.09.012
Cerqueira F, Matamoros V, Bayona J, Piña B (2019) Antibiotic resistance genes distribution in microbiomes from the soil-plant-fruit continuum in commercial Lycopersicon esculentum fields under different agricultural practices. Sci Total Environ 652:660–670. https://doi.org/10.1016/j.scitotenv.2018.10.268
Chandra R, Amit, Ghosh UK (2019) Effects of various abiotic factors on biomass growth and lipid yield of Chlorella minutissima for sustainable biodiesel production. Environ Sci Pollut Res 26:3848–3861. https://doi.org/10.1007/s11356-018-3696-1
Cordeiro RS, Vaz ICD, Magalhaes SMS, Barbosa FAR (2017) Effects of nutritional conditions on lipid production by cyanobacteria. An Acad Bras Cienc 89:2021–2031. https://doi.org/10.1590/0001-3765201720150707
Deng CN, Pan XL, Zhang DY (2015) Influence of ofloxacin on photosystems I and II activities of Microcystis aeruginosa and the potential role of cyclic electron flow. J Biosci Bioeng 119:159–164. https://doi.org/10.1016/j.jbiosc.2014.07.014
Deshmukh S, Bala K, Kumar R (2019a) Selection of microalgae species based on their lipid content, fatty acid profile and apparent fuel properties for biodiesel production. Environ Sci Pollut Res 26:24462–24473. https://doi.org/10.1007/s11356-019-05692-z
Deshmukh S, Kumar R, Bala K (2019b) Microalgae biodiesel: a review on oil extraction, fatty acid composition, properties and effect on engine performance and emissions. Fuel Process Technol 191:232–247. https://doi.org/10.1016/j.fuproc.2019.03.013
Dineshbabu G, Uma VS, Mathimani T, Prabaharan D, Uma L (2020) Elevated CO2 impact on growth and lipid of marine cyanobacterium Phormidium valderianum BDU 20041–towards microalgal carbon sequestration. Biocatal Agric Biotechnol 25:101606. https://doi.org/10.1016/j.bcab.2020.101606
Ellison CR, Overa S, Boldor D (2019) Central composite design parameterization of microalgae/cyanobacteria co-culture pretreatment for enhanced lipid extraction using an external clamp-on ultrasonic transducer. Ultrason Sonochem 51:496–503. https://doi.org/10.1016/j.ultsonch.2018.05.006
EN (2004) Automotive fuels-fatty acid methyl esters (FAME) for diesel engines-requirements and test methods
Eniola JO, Kumar R, Barakat MA (2019) Adsorptive removal of antibiotics from water over natural and modified adsorbents. Environ Sci Pollut Res 26:34775–34788. https://doi.org/10.1016/j.scitotenv.2015.05.130
Fu W, Li P, Wu Y (2012) Effects of different light intensities on chlorophyll fluorescence characteristics and yield in lettuce. Sci Hortic-Amsterdam 135:45–51. https://doi.org/10.1016/j.scienta.2011.12.004
González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rosal R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064. https://doi.org/10.1016/j.watres.2013.01.020
Han F, Pei HY, Hu WR, Jiang LQ, Cheng J, Zhang LJ (2016) Beneficial changes in biomass and lipid of microalgae Anabaena variabilis facing the ultrasonic stress environment. Bioresour Technol 209:16–22. https://doi.org/10.1016/j.biortech.2016.02.103
He J, Yang Y, Zhang J, Chen J, Wei X, He J, Luo L (2017) Ribosome biogenesis protein Urb1 acts downstream of mTOR complex 1 to modulate digestive organ development in zebrafish. J Genet Genomics 44:567–576. https://doi.org/10.1016/j.jgg.2017.09.013
Islam MA, Magnusson M, Brown RJ, Ayoko GA, Nabi MN, Heimann K (2013) Microalgal species selection for biodiesel production based on fuel properties derived from fatty acid profiles. Energies 6:5676–5702. https://doi.org/10.3390/en6115676
Jones-Dias D, Carvalho AS, Moura IB, Manageiro V, Igrejas G, Caniça M, Matthiesen R (2017) Quantitative proteome analysis of an antibiotic resistant Escherichia coli exposed to tetracycline reveals multiple affected metabolic and peptidoglycan processes. J Proteome 156:20–28. https://doi.org/10.1016/j.jprot.2016.12.017
Le Page G, Gunnarsson L, Trznadel M, Wedgwood KCA, Baudrot V, Snape J, Tyler CR (2019) Variability in cyanobacteria sensitivity to antibiotics and implications for environmental risk assessment. Sci Total Environ 695:133804. https://doi.org/10.1016/j.scitotenv.2019.133804
Lepage G, Roy CC (1984) Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res 25:1391
Liu Y, Chen S, Zhang J, Gao B (2016) Growth, microcystin-production and proteomic responses of Microcystis aeruginosa under long-term exposure to amoxicillin. Water Res 93:141–152. https://doi.org/10.1016/j.watres.2016.01.060
Liu Y, Chen S, Zhang J, Li X, Gao B (2017) Stimulation effects of ciprofloxacin and sulphamethoxazole in Microcystis aeruginosa and isobaric tag for relative and absolute quantitation-based screening of antibiotic targets. Mol Ecol 26:689–701. https://doi.org/10.1111/mec.13934
Maul JD, Schuler LJ, Belden JB, Whiles MR, Lydy MJ (2006) Effects of the antibiotic ciprofloxacin of stream microbial communities and detritivorous macroinvertebrates. Environ Toxicol Chem 25:1598–1606. https://doi.org/10.1897/05-441R.1
Opoku-Temeng C, Onyedibe KI, Aryal UK, Sintim HO (2019) Proteomic analysis of bacterial response to a 4-hydroxybenzylidene indolinone compound, which re-sensitizes bacteria to traditional antibiotics. J Proteome 202:103368. https://doi.org/10.1016/j.jprot.2019.04.018
Pattanaik B, Englund E, Nolte N, Lindberg P (2020) Introduction of a green algal squalene synthase enhances squalene accumulation in a strain of Synechocystis sp. PCC 6803. Metab Eng Commun 10:e125. https://doi.org/10.1016/j.mec.2020.e00125
Paul MJ (2013) Photosynthetic carbon dioxide fixation. 497-502*497-502. In: Lennarz WJ, Lane MD (eds) Encyclopedia of Biological chemistry, Second edn. Academic Press, Waltham. https://doi.org/10.1016/B978-0-12-378630-2.00050-5
Pomati F, Netting AG, Calamari D, Neilan BA (2004) Effects of erythromycin, tetracycline and ibuprofen on the growth of Synechocystis sp. and Lemna minor. Aquat Toxicol 67:387–396. https://doi.org/10.1016/j.aquatox.2004.02.001
Raheem A, Prinsen P, Vuppaladadiyam AK, Zhao M, Luque R (2018) A review on sustainable microalgae based biofuel and bioenergy production: recent developments. J Clean Prod 181:42–59. https://doi.org/10.1016/j.jclepro.2018.01.125
Rowland JG, William JS, Yoshitaka N, Antoni RS (2010) Differential proteomic analysis using iTRAQ reveals changes in thylakoids associated with Photosystem II-acquired thermotolerance in Synechocystis sp. PCC 6803. Proteomics 10. https://doi.org/10.1002/pmic.200900337
Shuba ES, Kifle D (2018) Microalgae to biofuels: ‘promising’ alternative and renewable energy, review. Renew Sust Energ Rev 81:743–755. https://doi.org/10.1016/j.rser.2017.08.042
Singh D, Sharma D, Soni SL, Sharma S, Kumari D (2019) Chemical compositions, properties, and standards for different generation biodiesels: a review. Fuel 253:60–71. https://doi.org/10.1016/j.fuel.2019.04.174
Sivaramakrishnan R, Incharoensakdi A (2018) Enhancement of lipid production in Synechocystis sp. PCC 6803 overexpressing glycerol kinase under oxidative stress with glycerol supplementation. Bioresour Technol 267:532–540. https://doi.org/10.1016/j.biortech.2018.07.058
Touloupakis E, Cicchi B, Torzillo G (2015) A bioenergetic assessment of photosynthetic growth of Synechocystis sp. PCC 6803 in continuous cultures. Biotechnol Biofuels 8:133. https://doi.org/10.1186/s13068-015-0319-7
Vranakis I, Goniotakis I, Psaroulaki A, Sandalakis V, Tselentis Y, Gevaert K, Tsiotis G (2014) Proteome studies of bacterial antibiotic resistance mechanisms. J Proteome 97:88–99. https://doi.org/10.1016/j.jprot.2013.10.027
Wahlen BD, Willis RM, Seefeldt LC (2011) Biodiesel production by simultaneous extraction and conversion of total lipids from microalgae, cyanobacteria, and wild mixed-cultures. Bioresour Technol 102:2724–2730. https://doi.org/10.1016/j.biortech.2010.11.026
Wan J, Guo P, Peng X, Wen K (2015) Effect of erythromycin exposure on the growth, antioxidant system and photosynthesis of Microcystis flos-aquae. J Hazard Mater 283:778–786. https://doi.org/10.1016/j.jhazmat.2014.10.026
Wang Z, Chen Q, Zhang J, Dong J, Ao Y, Wang M, Wang X (2019) Long-term exposure to antibiotic mixtures favors microcystin synthesis and release in Microcystis aeruginosa with different morphologies. Chemosphere 235:344–353. https://doi.org/10.1016/j.chemosphere.2019.06.192
Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359–362. https://doi.org/10.1038/nmeth.1322
Wu K, Zhang C, Liu T, Lei H, Yang S, Jin P (2020) The removal of tetracycline, oxytetracycline, and chlortetracycline by manganese oxide–doped copper oxide: the behaviors and insights of Cu-Mn combination for enhancing antibiotics removal. Environ Sci Pollut Res 27:12613–12623. https://doi.org/10.1007/s11356-020-07810-8
Yang Y, Song W, Lin H, Wang W, Du L, Xing W (2018) Antibiotics and antibiotic resistance genes in global lakes: a review and meta-analysis. Environ Int 116:60–73. https://doi.org/10.1016/j.envint.2018.04.011
Zhao F, Chen L, Yen H, Sun L, Li S, Li M, Feng Q, Yang L (2020) Multimedia mass balance approach to characterizing the transport potential of antibiotics in soil–plant systems following manure application. J Hazard Mater 393:122363. https://doi.org/10.1016/j.jhazmat.2020.122363
Živković SB, Veljković MV, Banković-Ilić IB, Krstić IM, Konstantinović SS, Ilić SB, Avramović JM, Stamenković OS, Veljković VB (2017) Technological, technical, economic, environmental, social, human health risk, toxicological and policy considerations of biodiesel production and use. Renew Sust Energ Rev 79:222–247. https://doi.org/10.1016/j.rser.2017.05.048
Zou X, Lin Z, Deng Z, Yin D (2013) Novel approach to predicting hormetic effects of antibiotic mixtures on Vibrio fischeri. Chemosphere 90:2070–2076. https://doi.org/10.1016/j.chemosphere.2012.09.042
Zuñiga-Navarrete F, Flores-Ramirez G, Danchenko M, Benada O, Skriba A, Skultety L (2019) Proteomic analysis revealed the survival strategy of Coxiella burnetii to doxycycline exposure. J Proteome 208:103479. https://doi.org/10.1016/j.jprot.2019.103479
Acknowledgments
This work was supported by the National Natural Science Foundation of China (51679130) partly by the Fundamental Research Funds of Shandong University (2017WLJH35).
Funding
This study was funded by the National Natural Science Foundation of China (51679130) partly by the Fundamental Research Funds of Shandong University (2017WLJH35).
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Cui, M., Liu, Y. & Zhang, J. Sulfamethoxazole and tetracycline induced alterations in biomass, photosynthesis, lipid productivity, and proteomic expression of Synechocystis sp. PCC 6803. Environ Sci Pollut Res 27, 30437–30447 (2020). https://doi.org/10.1007/s11356-020-09327-6
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DOI: https://doi.org/10.1007/s11356-020-09327-6