Abstract
Exposure time, metal bio-accumulation, and upregulation of ascorbate-glutathione (AsA-GSH) cycle are the key factor that provide tolerance against heavy metal stress. Thus, the current study is an endeavor to prove our hypothesis that regulation of arsenate (AsV: 50, 100, and 150 mM) and arsenite (AsIII: 50, 100, and 150 μM) toxicity is time dependent (48–96 h) due to modulation in bio-accumulation pattern, AsA-GSH cycle, and non-enzymatic antioxidants in two paddy field cyanobacteria Nostoc muscorum ATCC27893 and Anabaena sp. PCC7120. After 48 h, reduction in growth associated with increased sensitivity index, As bio-accumulation, and oxidative stress was observed which further intensified after 96 h but the degree of damage was lesser than 48 h. It denotes a significant recovery in growth after 96 h which is correlated with decreased As bio-accumulation and oxidative stress due to increased efficiency of AsA-GSH cycle and non-enzymatic antioxidants. Both the species of As caused significant rise in oxidative biomarkers as evident by in -vitro analysis of O2·−, H2O2, and MDA equivalent contents despite appreciable rise in the activity antioxidative enzymes APX, DHAR, and GR. The study concludes that among both forms of arsenic, AsIII induced more toxic effect on growth by over-accumulating the ROS as evident by weak induction of AsA-GSH cycle to overcome the stress as compared to AsV. Further, with increasing the time exposure, apparent recovery was noticed with the lower doses of AsV, i.e., 50 and 100 mM and AsIII, i.e., 50 and 100 μM; however, the toxicity further aggravated with higher dose of both AsV and AsIII. Study proposes the deleterious impact of AsV and AsIII on cyanobacteria N. muscorum and Anabaena sp. but the toxicity was overcome by time-dependent recovery.
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Asad ikarama E, Batool K, Sergio S, Viviana M, Zahra A, Hossein M, Adriana B (2017) Interaction of triacontanol and arsenic on the ascorbate-glutathione cycle and their effects on the ultrastructure in Coriandrum sativum L. Ecotoxicol Environ Saf 144:268–274
Aslam M, Saeed MS, Sattar S, Sajad S, Sajjad M, Adnan M, Iqbal M, Sharif MT (2017) Specific role of proline against heavy metals toxicity in plants. Int J Pure App Biosci 5:27–34
Awasthi S, Chauhana R, Dwivedi S, Srivastava S, Tripathi RD (2018) A consortium of alga (Chlorella vulgaris) and bacterium (Pseudomonas putida) for amelioration of arsenic toxicity in rice: a promising and feasible approach. Environ Exp Bot 150:115–126
Banerjee M, Chakravarty D, Ballal A (2017) Molecular basis of function and the unusual antioxidant activity of a cyanobacterial cysteine desulfurase. Biochem J 474:2435–2447
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of the free proline for water stress studies. Plant Soil 39:205–207
Begum MC, Islam MS, Islam M, Amin R, Parvez MS, Kabir AH (2016) Biochemical and molecular responses underlying differential arsenic tolerance in rice (Oryza sativa L.). Plant Physiol Biochem 104:266–277
Bhattacharjee H, Mukhopadhyay R, Thiyagarajan S, Rosen BP (2008) Aquaglyceroporin: ancient channel for metalloids. J Biol 7:33–35
Bhattacharya P, Pal R (2012) Scope of phycoremediation of arsenic using Phormidium tenue with special reference to modulation in cellular biochemistry. J Algal Biomass Utln 3:1–8
Borella J, Becker R, Lima MC, de Oliveira DSC, Braga EJB, de Oliveira ACB, do Amarante L (2019) Nitrogen source influences the antioxidative system of soybean plants under hypoxia and re-oxygenation. Sci Agric 76:51–62
Brehe JE, Burch HB (1976) Enzymatic assay for glutathione. Anal Biochem 74:189–197
Cavet JS, Borrelly GPM, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181
Chac´on-Lee TL, Gonz´alez-Marino GE (2010) Microalgae for healthy food-possibilities and challenges. Compr Rev Food Sci Food Saf 9:655–675
Chattergee P, Biswas S, Biswas AK (2018) Sodium chloride primed seeds modulate glutathione metabolism in legume cultivars under NaCl stress. Am J Plant Physiol 13:8–22
Chen J, Rosen BP (2016) Organoarsenical biotransformations by Shewanella putrefaciens. Environ Sci Technol 50:7956–7963
Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L (2013) Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J Exp Bot 64:3339–3349
Demay J, Bernard C, Reinhardt A, Marie B (2019) Natural products from cyanobacteria: focus on beneficial activities. Mar Drugs 17:320
Dhuldhaja U, Pandyab U, Singh S (2018) Anti-oxidative response of cyanobacterium Anabaena sp. strain PCC 7120 to arsenite (As(III)). Microbiology 87:848–856
Ellmann GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620
Farooq MA, Gill RA, Ali B, Wang J, Islam F, Ali S, Zhou WJ (2015) Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Brassica napus L. Ecotoxicology 25:350–366
Ferrari SG, Silvaa PG, Gonzálezb DM, Navonic JA, Silvaa HJ (2013) Arsenic tolerance of cyanobacterial strains with potential use in bio-technology. Rev Argent Microbiol 45:174–179
Finnegan PM, Chenm W (2012) Arsenic toxicity: the effects on plant metabolism. Front Plant Sci 3:182
Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627–633
Gebel T (2000) Confounding variables in the environmental toxicology of arsenic. Toxicology 144:155–162
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gossett DR, Millhollon EP, Cran LM (1994) Antioxidant response to NaCl stress in salt-sensitive cultivars of cotton. Crop Sci 34:706–714
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hurtado-Gallego J, Martín-Betancor K, Rodea-Palomares I, Leganés F, Rosal R, Fernández-Piñas F (2018) Two novel cyanobacterial bioluminescent whole-cell bioreporters based on superoxide dismutases MnSod and FeSod to detect superoxide anion. Chemosphere 201:772–779
Itri R, Junqueira HC, Mertins O, Baptista MS (2014) Membarne changes under oxidative stress: the impact of oxidized lipids. Biophys Rev 6(1):47–61
Jain M, Mathur G, Koul S, Sarin N (2001) Ameliorative effects of proline on salt stress-induced lipid peroxidation in cell lines of groundnut (Arachis hypogaea L.). Plant Cell Rep 20:463–468
Jedynak L, Kowalska J, Kossykowska M, Golimowski M (2010) Studies on the uptake of different arsenic forms and the influence of sample pretreatment on arsenic speciation in white mustard (Sinapis alba). Microchem J 94:125–129
Kulp TR, Hoeft SE, Asao N, Madigan MT, Hollibaugh JT, Fisher JC, Stolz JF, Culbertson CW, Miller LG, Oremland RS (2008) Arsenic (III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California. Sci 321:967
Kumar J, Singh VP, Prasad SM (2017) An investigation on involvement of the ascorbate-glutathione cycle in modulating NaCl toxicity in two cyanobacteria photoacclimatized to different photosynthetic active radiation. Algal Res 28:70–78
Mishra S, Dubey RS (2006) Inhibition of ribonuclease and protease activities in arsenic-exposed rice seedlings: role of proline as enzyme protectant. J Plant Physiol 163:927–936
Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate–dependent reduction of nitroblue tetrazolium. Anal Biochem 212:540–546
Miyashita S, Murota C, Kondo K, Fujiwara S, Tsuzuki M (2015) Arsenic metabolism in cyanobacteria. Environ Chem 13:4
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Pandey S, Shrivastava AK, Singh VK, Rai R, Singh PK, Rai S, Rai LC (2013) A new arsenate reductase involved in arsenic detoxification in Anabaena sp. PCC7120. Funct Integr Genom 13:43–55
Patel A, Tiwari S, Prasad SM (2018) Toxicity assessment of arsenate and arsenite on growth, chlorophyll fluorescence and antioxidant machinery in Nostoc muscorum. Ecotoxicol Environ Saf 157:369–379
Perales-Vela HV, Pena-Castro J, Canizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10
Piotrowska-Niczyporuk A, Bajguz A, Talarek M, Bralska M, Zambrzycka E (2015) The effect of lead on the growth, content of primary metabolites, and antioxidant response of green alga Acutodesmus obliquus (Chlorophyceae). Environ Sci Pollut Res 22:19112–19123
Prajapati R, Yadav S, Atri N (2018) Nickel and arsenite-induced differential oxidative stress and antioxidant responses in two Anabaena species. J Basic Microbiol 58:1061–1070
Rensing C, Rosen B (2009) Heavy metals cycle (arsenic, mercury, selenium, others). In: Schaeter M (ed) Encyclopedia of Microbiology. Elsevier, Oxford, pp 205–219
Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012
Singh M, Singh VP, Dubey G, Prasad SM (2015) Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings. Ecotoxicol Environ Saf 117:164–173
Singh JS, Kumar A, Rai AN, Singh DP (2016a) Cyanobacteria: a precious bioresource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 21:529
Singh R, Singh S, Parihar P, Mishra RK, Tripathi DK, Singh VP, Chauhan DK, Prasad SM (2016b) Reactive oxygen species (ROS): beneficial companions of plants’ developmental processes. Front Plant Sci 7:1299
Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Plant Sci 19:267–290
Srivastava S, Sharma YK (2012) Arsenic induced changes in growth and metabolism of black gram seedlings (Vigna Mungo L.) and the role of phosphate as an ameliorating agent. Environ Sci Process 1:431–445
Sure S, Ackland ML, Gaur A, Gupta P, Adholeya A, Kochar M (2016) Probing synechocystis-arsenic interactions through extracellular nanowires. Front Microbiol 7:1134
Upadhyay AK, Mandotra SK, Kumar N, Singh NK, Singh L, Rai UN (2016) Augmentation of arsenic enhances lipid yield and defense responses in alga Nannochloropsis sp. Bioresour Technol 221:430–437
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant system in acid rain-treated bean plants. Plant Sci 151:59–66
Waterhouse AL (2001) Determination of total phenolics in current protocols. In: Wrolstad RE (ed) Food and analytical chemistry. Wiley, USA, pp 1111–1118
Whitton BA (2000) Soils and rice fields. In: Whitton BA, Potts M (Eds.), The ecology of cyanobacteria: their diversity in time and space, Alphen aan den Rijn: Kluwer Academic 233–255
Wu Z, Liu S, Zhao J, Wang F, Du Y, Zou S, Li H, Wen D, Huang Y (2017) Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress. Environ Exp Bot 133:1–11
Yadav G, Srivastava PK, Parihar P, Tiwari S, Prasad SM (2016) Oxygen toxicity and antioxidative responses in arsenic stressed Helianthus annuus L. seedlings against UV-B. J Photochem Photobiol B 165:58–70
Ye B, Gitler C, Gressel J (1997) A High–sensitivity, single–gel, polyacrylamide gel electrophoresis method for the quantitative determination of glutathione reductases. Anal Biochem 246:159–165
Ye J, Rensing C, Rosen BP, Zhu YG (2012) Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci 17:155–162
Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173
Zhao W, Ye Z, Zhao JA (2007) Membrane-associated Mn-superoxide dismutase protects the photosynthetic apparatus and nitrogenase from oxidative damage in the cyanobacterium Anabaena sp. PCC7120. Plant Cell Physiol 48:563–572
Zheng Y, Ayotte DJ (2015) At the crossroads: hazard assessment and reduction of health risks from arsenic in private well waters of the northeastern United States and Atlantic Canada. Sci Total Environ 505:1237–1247
Zutshi S, Bano F, Ningthoujam M, Habib K, Fatma T (2014) Metabolic adaptations to arsenic-induced oxidative stress in Hapalosiphon fontinalis-339. Int J Innov Res Sci Eng Tech 3:9386–9394
Acknowledgements
Anuradha Patel is thankful to NFO as ‘SRF’ with award letter number (NFO-2015-17-OBC-UTT-41056) and Sanjesh Tiwari is thankful to CSIR-UGC New Delhi as ‘SRF’ with award letter number 2121430412, EU-V, 29-06-15. Authors are thankful to the Head, Department of Botany for providing necessary lab facilities.
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SMP designed the experiment, AP and ST planned and performed the experiment, AP and ST analyzed the data, and SMP, AP, and ST wrote the manuscript.
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Patel, A., Tiwari, S. & Prasad, S.M. Arsenate and arsenite-induced inhibition and recovery in two diazotrophic cyanobacteria Nostoc muscorum and Anabaena sp.: study on time-dependent toxicity regulation. Environ Sci Pollut Res 28, 51088–51104 (2021). https://doi.org/10.1007/s11356-021-13800-1
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DOI: https://doi.org/10.1007/s11356-021-13800-1