Abstract
Leptolyngbya boryana (L. boryana) is a typical filamentous cyanobacterium that is widely distributed in aquatic ecosystems and is considered to play an important role in the arsenic biogeochemical cycle. Our results showed that L. boryana resisted arsenite (As(III)) and arsenate (As(V)) concentrations up to 0.25 mM and 5 mM, respectively. When exposed to 100 μM As(III) or As(V) for 4 weeks, L. boryana accumulated as much arsenic as 570.0 mg kg−1 and 268.5 mg kg−1, respectively. After the 4-week exposure to As(III) and As(V), organoarsenicals including dimethylarsenate (DMAs(V)) and oxo-arsenosugar-phosphate (Oxo-PO4) were detected in the cells of L. boryana, while inorganic arsenic, especially As(V), was still the main species in both the cells and medium. Furthermore, arsenic oxidation was observed to be solely caused by L. boryana cells and was considered the dominant detoxification pathway. In conclusion, due to its powerful arsenic accumulation, biotransformation, and detoxification abilities, L. boryana might play an important role in arsenic remediation in aquatic environments.
Similar content being viewed by others
References
Arora N, Gulati K, Patel A, Pruthi PA, Poluri KM, Pruthi V (2017) A hybrid approach integrating arsenic detoxification with biodiesel production using oleaginous microalgae. Algal Res 24:29–39. https://doi.org/10.1016/j.algal.2017.03.012
Baeyens W, Mirlean N, Bundschuh J, de Winter N, Baisch P, da Silva FMR, Gao Y (2019) Arsenic enrichment in sediments and beaches of Brazilian coastal waters: a review. Sci Total Environ 681:143–154. https://doi.org/10.1016/j.scitotenv.2019.05.126
Chen J, Madegowda M, Bhattacharjee H, Rosen BP (2015) ArsP: a methylarsenite efflux permease. Mol Microbiol 98:625–635. https://doi.org/10.1111/mmi.13145
Dheeman DS, Packianathan C, Pillai JK, Rosen BP (2014) Pathway of human AS3MT arsenic methylation. Chem Res Toxicol 27:1979–1989. https://doi.org/10.1021/tx500313k
Garbinski LD, Rosen BP, Chen J (2019) Pathways of arsenic uptake and efflux. Environ Int 126:585–597. https://doi.org/10.1016/j.envint.2019.02.058
Ge Y, Ning ZB, Wang Y, Zheng YH, Zhang CH, Figeys D (2016) Quantitative proteomic analysis of Dunaliella salina upon acute arsenate exposure. Chemosphere 145:112–118. https://doi.org/10.1016/j.chemosphere.2015.11.049
Guo PR, Gong Y, Wang C, Liu X, Liu JT (2011) Arsenic speciation and effect of arsenate inhibition in a Microcystis aeruginosa culture medium under different phosphate regimes. Environ Toxicol Chem 30:1754–1759. https://doi.org/10.1002/etc.567
Hasegawa H, Papry RI, Ikeda E, Omori Y, Mashio AS, Maki T, Rahman MA (2019) Freshwater phytoplankton: biotransformation of inorganic arsenic to methylarsenic and organoarsenic. Sci Rep 9:12074. https://doi.org/10.1038/s41598-019-48477-7
Hayakawa T, Kobayashi Y, Cui X, Hirano S (2005) A new metabolic pathway of arsenite: arsenic-glutathione complexes are substrates for human arsenic methyltransferase Cyt19. Arch Toxicol 79:183–191. https://doi.org/10.1007/s00204-004-0620-x
Khanam R, Kumar A, Nayak AK, Shahid M, Tripathi R, Vijayakumar S, Bhaduri D, Kumar U, Mohanty S, Panneerselvam P, Chatterjee D, Satapathy BS, Pathak H (2020) Metal(loid)s (As, Hg, Se, Pb and Cd) in paddy soil: bioavailability and potential risk to human health. Sci Total Environ 699:134330. https://doi.org/10.1016/j.scitotenv.2019.134330
Knauer K, Hemond H (2000) Accumulation and reduction of arsenate by the freshwater green alga Chlorella sp (Chlorophyta). J Phycol 36:506–509. https://doi.org/10.1046/j.1529-8817.2000.99056.x
Levy JL, Stauber JL, Adams MS, Maher WA, Kirby JK, Jolley DF (2005) Toxicity, biotransformation, and mode of action of arsenic in two freshwater microalgae (Chlorella sp and Monoraphidium arcuatum). Environ Toxicol Chem 24:2630–2639. https://doi.org/10.1897/04-580R.1
Li L, Ren JL, Cao XH, Liu SM, Hao Q, Zhou F, Zhang J (2017) Process study of biogeochemical cycling of dissolved inorganic arsenic during spring phytoplankton bloom, southern Yellow Sea. Sci Total Environ 593:430–438. https://doi.org/10.1016/j.scitotenv.2017.03.113
Madsen AD, Goessler W, Pedersen SN, Francesconi KA (2000) Characterization of an algal extract by HPLC-ICP-MS and LC-electrospray MS for use in arsenosugar speciation studies. J Anal Atom Spectrom 15:657–662. https://doi.org/10.1039/b001418o
Miyashita S, Fujiwara S, Tsuzuki M, Kaise T (2012) Cyanobacteria produce arsenosugars. Environ Chem 9:474–484. https://doi.org/10.1071/EN12061
Munoz LP, Purchase D, Jones H, Raab A, Urgast D, Feldmann J, Garelick H (2016) The mechanisms of detoxification of As(III), dimethylarsinic acid (DMA) and As(V) in the microalga Chlorella vulgaris. Aquat Toxicol 175:56–72. https://doi.org/10.1016/j.aquatox.2016.02.020
Murray LA, Raab A, Marr IL, Feldmann J (2003) Biotransformation of arsenate to arsenosugars by Chlorella vulgaris. Appl Organomet Chem 17:669–674. https://doi.org/10.1002/aoc.498
Myashita S, Fujiwara S, Tsuzuki M, Kaise T (2011) Rapid biotransformation of arsenate into Oxo-arsenosugars by a freshwater unicellular green alga, Chlamydomonas reinhardtii. Biosci Biotechnol Biochem 75:522–530. https://doi.org/10.1271/bbb.100751
Packianathan C, Li JJ, Kandavelu P, Sankaran B, Rosen BP (2018) Reorientation of the methyl group in MAs(III) is the rate-limiting step in the ArsM As(III) S-adenosylmethionine methyltransferase reaction. ACS Omega 3:3104–3112. https://doi.org/10.1021/acsomega.8b00197
Qin J, Lehr CR, Yuan CG, Le XC, McDermott TR, Rosen BP (2009) Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proc Natl Acad Sci U S A 106:5213–5217. https://doi.org/10.1073/pnas.0900238106
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiol 111(1):1–61. https://doi.org/10.1099/00221287-111-1-1
Sharma VK, Sohn M (2009) Aquatic arsenic: toxicity, speciation, transformations, and remediation. Environ Int 35:743–759. https://doi.org/10.1016/j.envint.2009.01.005
Shi KX, Li C, Rensing C, Dai XL, Fan X, Wang GJ (2018) Efflux transporter ArsK is responsible for bacterial resistance to arsenite, antimonite, trivalent roxarsone, and methylarsenite. Appl Environ Microbiol 84:e01842–e01818. https://doi.org/10.1128/AEM.01842-18
Wang ZH, Luo ZX, Yan CZ (2013) Accumulation, transformation, and release of inorganic arsenic by the freshwater cyanobacterium Microcystis aeruginosa. Environ Sci Pollut Res 20:7286–7295. https://doi.org/10.1007/s11356-013-1741-7
Wang Y, Wang S, Xu PP, Liu C, Liu MS, Wang YL, Wang CH, Zhang CH, Ge Y (2015) Review of arsenic speciation, toxicity and metabolism in microalgae. Rev Environ Sci Biotechnol 14:427–451. https://doi.org/10.1007/s11157-015-9371-9
Xue XM, Raber G, Foster S, Chen SC, Francesconi KA, Zhu YG (2014) Biosynthesis of arsenolipids by the cyanobacterium Synechocystis sp. PCC 6803. Environ Chem 11:506–513. https://doi.org/10.1071/EN14069
Xue XM, Yan Y, Xiong C, Raber G, Francesconi K, Pan T, Ye J, Zhu YG (2017a) Arsenic biotransformation by a cyanobacterium Nostoc sp PCC 7120. Environ Pollut 228:111–117. https://doi.org/10.1016/j.envpol.2017.05.005
Xue XM, Ye J, Raber G, Francesconi KA, Li G, Gao H, Yan Y, Rensing C, Zhu YG (2017b) Arsenic methyltransferase is involved in arsenosugar biosynthesis by providing DMA. Environ Sci Technol 51:1224–1230. https://doi.org/10.1021/acs.est.6b04952
Xue XM, Ye J, Raber G, Rosen BP, Francesconi K, Xiong C, Zhu Z, Rensing C, Zhu YG (2019) Identification of steps in the pathway of arsenosugar biosynthesis. Environ Sci Technol 53:634–641. https://doi.org/10.1021/acs.est.8b04389
Yang J, Zhu YG (2009) Progress in study of mechanisms of microbial arsenic transformation in environment. Asian J Ecotoxicol 4:761–769 (in Chinese)
Ye J, Rensing C, Rosen BP, Zhu YG (2012) Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci 17:155–162. https://doi.org/10.1016/j.tplants.2011.12.003
Yin XX, Wang LH, Bai R, Huang H, Sun GX (2011a) Accumulation and transformation of arsenic in the blue-green alga Synechocysis sp. PCC6803. Water Air Soil Pollut 223:1183–1190. https://doi.org/10.1007/s11270-011-0936-0
Yin XX, Chen J, Qin J, Sun GX, Rosen BP, Zhu YG (2011b) Biotransformation and volatilization of arsenic by three photosynthetic cyanobacteria. Plant Physiol 156:1631–1638. https://doi.org/10.1104/pp.111.178947
Yin XX, Wang LH, Duan GL, Sun GX (2011c) Characterization of arsenate transformation and identification of arsenate reductase in a green alga Chlamydomonas reinhardtii. J Environ Sci 23:1186–1193. https://doi.org/10.1016/S1001-0742(10)60492-5
Yin XX, Wang LH, Zhang ZC, Fan GL, Liu JJ, Sun KZ, Sun GX (2017) Biomethylation and volatilization of arsenic by model protozoan tetrahymena pyriformis under different phosphate regimes. Int J Environ Res Public Health 14:188. https://doi.org/10.3390/ijerph14020188
Zhang X, Zhao FJ, Huang Q, Williams PN, Sun GX, Zhu YG (2009) Arsenic uptake and speciation in the rootless duckweed Wolffia globosa. New Phytol 182:421–428. https://doi.org/10.1111/j.1469-8137.2008.02758.x
Zhang SY, Sun GX, Yin XX, Rensing C, Zhu YG (2013) Biomethylation and volatilization of arsenic by the marine microalgae Ostreococcus tauri. Chemosphere 93:47–53. https://doi.org/10.1016/j.chemosphere.2013.04.063
Zhang SY, Rensing C, Zhu YG (2014) Cyanobacteria-mediated arsenic redox dynamics is regulated by phosphate in aquatic environments. Environ Sci Technol 48:994–1000. https://doi.org/10.1021/es403836g
Zhu YG, Xue XM, Kappler A, Rosen BP, Meharg AA (2017) Linking genes to microbial biogeochemical cycling: lessons from arsenic. Environ Sci Technol 51:7326–7339. https://doi.org/10.1021/acs.est.7b00689
Acknowledgments
This work was financially supported by the National Natural Science Foundation of China (41807410), and the Scientific Research Funds of Huaqiao University (Z18Y0021), and Guangxi Key Science and Technology Innovation Base on Karst Dynamics (KDL&Guangxi202011).
Author information
Authors and Affiliations
Corresponding author
Additional information
Editorial Responsibility: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 285 kb).
Rights and permissions
About this article
Cite this article
Zhu, F., Yang, M., Luo, Zx. et al. Bioaccumulation and biotransformation of arsenic in Leptolyngbya boryana. Environ Sci Pollut Res 27, 29993–30000 (2020). https://doi.org/10.1007/s11356-020-09294-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-09294-y