The cadmium tolerance and bioaccumulation mechanism of Tetratostichococcus sp. P1: insight from transcriptomics analysis

References

• Baby J, Raj J, Biby E, et al. Toxic effect of heavy metals on aquatic environment. Int J Biol Chem Sci. 2010;4(4):939–16. doi: 10.4314/ijbcs.v4i4.62976
   Google Scholar
• Zakhama S, Dhaouadi H, M’Henni F. Nonlinear modelisation of heavy metal removal from aqueous solution using ulva lactuca algae. Bioresour Technol. 2011;102(2):786–796. doi: 10.1016/j.biortech.2010.08.107
   PubMed Web of Science ®Google Scholar
• Leong YK, Chang JS. Bioremediation of heavy metals using microalgae: recent advances and mechanisms. Bioresour Technol. 2020;303:122886. doi: 10.1016/j.biortech.2020.122886
   PubMed Web of Science ®Google Scholar
• Qi K, Ren L, Bai Z, et al. Detecting cadmium during ultrastructural characterization of hepatotoxicity. J Trace Elem Med Biol. 2020;62:126644. doi: 10.1016/j.jtemb.2020.126644
   PubMed Web of Science ®Google Scholar
• Yu Z, Wei H, Hao R, et al. Physiological changes in Chlamydomonas reinhardtii after 1000 generations of selection of cadmium exposure at environmentally relevant concentrations. Environ Sci Process Impacts. 2018;20(6):923–933. doi: 10.1039/c8em00106e
   PubMed Web of Science ®Google Scholar
• Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO. Heavy metal detoxification in eukaryotic microalgae. Chemosphere. 2006;64(1):1–10. doi: 10.1016/j.chemosphere.2005.11.024
   PubMed Web of Science ®Google Scholar
• Monteiro CM, Castro PML, Malcata FX. Cadmium Removal by Two Strains of Desmodesmus pleiomorphus Cells. Water Air Soil Pollut. 2010;208(1–4):17–27. doi: 10.1007/s11270-009-0146-1
   Web of Science ®Google Scholar
• Chandrashekharaiah PS, Sanyal D, Dasgupta S, et al. Cadmium biosorption and biomass production by two freshwater microalgae scenedesmus acutus and chlorella pyrenoidosa: an integrated approach. Chemosphere. 2021;269:128755. doi: 10.1016/j.chemosphere.2020.128755
   PubMed Web of Science ®Google Scholar
• Kumar KS, Dahms HU, Won EJ, et al. Microalgae - a promising tool for heavy metal remediation. Ecotoxicol Environ Saf. 2015;113:329–352. doi: 10.1016/j.ecoenv.2014.12.019
   PubMed Web of Science ®Google Scholar
• Zhu Q, Zhang M, Bao J, et al. Physiological, metabolomic, and transcriptomic analyses reveal the dynamic redox homeostasis upon extended exposure of Dunaliella salina GY-H13 cells to Cd. Ecotoxicol Environ Saf. 2021;223:112593. doi: 10.1016/j.ecoenv.2021.112593
   PubMed Web of Science ®Google Scholar
• Abinandan S, Subashchandrabose SR, Venkateswarlu K, Perera IA, Megharaj M. Acid-tolerant microalgae can withstand higher concentrations of invasive cadmium and produce sustainable biomass and biodiesel at pH 3.5. Bioresour Technol. 2020;281:469–473. doi: 10.1016/j.biortech.2019.03.001
   Web of Science ®Google Scholar
• Subashchandrabose SR, Megharaj M, Venkateswarlu K, et al. Interaction effects of polycyclic aromatic hydrocarbons and heavy metals on a soil microalga, Chlorococcum sp. MM11. Environ Sci Pollut Res. 2015;22(12):8876–8889. doi: 10.1007/s11356-013-1679-9
   PubMed Web of Science ®Google Scholar
• Birungi ZS, Chirwa EMN. Interpretation of uptake kinetic of thallium and cadmium on surfaces of immobilized green algae as biosorbents. Chem Eng Trans. 2016;49:421–426. doi: 10.3303/CET1649071
   Google Scholar
• Skowroński T. Uptake of cadmium by Stichococcus bacillaris. Chemosphere. 1984;13(12):1385–1389. doi: 10.1016/0045-6535(84)90052-3
   Web of Science ®Google Scholar
• Sahabudin E, Lee J, Asada R, et al. Isolation and characterization of acid-tolerant stichococcus-like microalga (Tetratostichococcus sp. P1) from a tropical peatland in Malaysia. J Appl Phycol. 2022a;34(4):1881–1892. doi: 10.1007/s10811-022-02762-7
   Web of Science ®Google Scholar
• Sahabudin E, Othman NA, Suzuki I. High cadmium tolerance in stichoccocus-like microalgae (Tetratostichoccocus sp. P1) from Malaysia. IOP Conf Ser Earth Environ Sci. 2022b;1091(1):012045. doi: 10.1088/1755-1315/1091/1/012045
   Google Scholar
• Tripathi S, Arora N, Gupta P, et al. Microalgae: an emerging source for mitigation of heavy metals and their potential implications for biodiesel production, advanced biofuels: applications, technologies and environmental sustainability. Elsevier Ltd; 2019. doi: 10.1016/B978-0-08-102791-2.00004-0
   Google Scholar
• Priyadarshini E, Priyadarshini SS, Pradhan N. Heavy metal resistance in algae and its application for metal nanoparticle synthesis. Appl Microbiol Biotechnol. 2019;103(8):3297–3316. doi: 10.1007/s00253-019-09685-3
   PubMed Web of Science ®Google Scholar
• Tripathi S, Poluri KM. Heavy metal detoxification mechanisms by microalgae: insights from transcriptomics analysis. Environ Pollut. 2021;285:117443. doi: 10.1016/j.envpol.2021.117443
   PubMed Web of Science ®Google Scholar
• Blaby-Haas CE, Merchant SS. The ins and outs of algal metal transport. Biochim Biophys Acta, Mol Cell Res. 2012;1823(9):1531–1552. doi: 10.1016/j.bbamcr.2012.04.010
   Web of Science ®Google Scholar
• Lu JJ, Ma YL, Xing GL, et al. Revelation of microalgae’s lipid production and resistance mechanism to ultra-high Cd stress by integrated transcriptome and physiochemical analyses. Environ Pollut. 2019;250:186–195. doi: 10.1016/j.envpol.2019.04.018
   PubMed Web of Science ®Google Scholar
• Balzano S, Sardo A, Blasio M, et al. Microalgal metallothioneins and phytochelatins and their potential use in bioremediation. Front Microbiol. 2020;11:1–16. doi: 10.3389/fmicb.2020.00517
   PubMed Web of Science ®Google Scholar
• Ding N, Wang L, Kang Y, et al. The comparison of transcriptomic response of green microalga chlorella sorokiniana exposure to environmentally relevant concentration of cadmium(II) and 4-n-nonylphenol. Environ Geochem Health. 2020;42(9):2881–2894. doi: 10.1007/s10653-020-00526-1
   PubMed Web of Science ®Google Scholar
• Liao Y, Jiang X, Xiao Y, et al. Exposure of microalgae Euglena gracilis to polystyrene microbeads and cadmium: perspective from the physiological and transcriptional responses. Aquatic Toxicol. 2020;228:105650. doi: 10.1016/j.aquatox.2020.105650
   PubMed Web of Science ®Google Scholar
• Abinandan S, Subashchandrabose SR, Pannerselvan L, et al. Potential of acid-tolerant microalgae, Desmodesmus sp. MAS1 and Heterochlorella sp. MAS3, in heavy metal removal and biodiesel production at acidic pH. Bioresour Technol. 2019;278:9–16. doi: 10.1016/j.biortech.2019.01.053
   PubMed Web of Science ®Google Scholar
• Rashid MH, Fardous Z, Chowdhury MA, et al. Determination of heavy metals in the soils of tea plantations and in fresh and processed tea leaves: an evaluation of six digestion methods. Chem Cent J. 2016;10(1):7. doi: 10.1186/s13065-016-0154-3
   PubMedGoogle Scholar
• Jayakumar V, Govindaradjane S, Senthil Kumar P, et al. Sustainable removal of cadmium from contaminated water using green alga – optimization, characterization and modeling studies. Environ Res. 2021;199:111364. doi: 10.1016/j.envres.2021.111364
   PubMed Web of Science ®Google Scholar
• Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 2003;100(16):9440–9445. doi: 10.1073/pnas.1530509100
   PubMed Web of Science ®Google Scholar
• Wagner H, Liu Z, Langner U, et al. The use of FTIR spectroscopy to assess quantitative changes in the biochemical composition of microalgae. J Biophoto. 2010;3(8–9):557–566. doi: 10.1002/jbio.201000019
   PubMed Web of Science ®Google Scholar
• Nanda M, Jaiswal KK, Kumar V, et al. Bio-remediation capacity for Cd(II) and Pb(II) from the aqueous medium by two novel strains of microalgae and their effect on lipidomics and metabolomics. Water Proc Eng. 2021;44:102404. doi: 10.1016/j.jwpe.2021.102404
   Web of Science ®Google Scholar
• Fathi A. Effects of Ph on toxicity of cadmium, cobalt and copper to the green alga Scenedesmus bijuga. Egyptian J Phycol. 2004;5(1):107–117. doi: 10.21608/egyjs.2004.113991
   Google Scholar
• Xu Y, Shi D, Aristilde L, et al. The effect of pH on the uptake of zinc and cadmium in marine phytoplankton: possible role of weak complexes. Limnol Oceanogr. 2012;57(1):293–304. doi: 10.4319/lo.2012.57.1.0293
   Web of Science ®Google Scholar
• Díaz S, de Francisco P, Olsson S, et al. Toxicity, physiological, and ultrastructural effects of arsenic and cadmium on the extremophilic microalga Chlamydomonas acidophila. Int J Environ Res Public Health. 2020;17(5):1650. doi: 10.3390/ijerph17051650
   PubMed Web of Science ®Google Scholar
• Skowroński T, Szubiflska S, Pawlik B, et al. The influence of pH on cadmium toxicity to the green alga Stichococcus bacillaris and on the cadmium forms present in the culture medium. Environ Pollut. 1991;74(2):89–100. doi: 10.1016/0269-7491(91)90106-7
   PubMed Web of Science ®Google Scholar
• Sbihi K, Cherifi O, El Gharmali A, et al. Toxicity and biosorption of chromium from aqueous solutions by the diatom Planothidium lanceolatum (brébisson) lange-bertalot. J Mater Environ Sci. 2012;3(1):27–38. doi: 10.5251/ajsir.2012.3.1.27.38
   Google Scholar
• Hanikenne M, Krämer U, Demoulin V, et al. A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Plant Physiol. 2005;137(2):428–446. doi: 10.1104/pp.104.054189
   PubMed Web of Science ®Google Scholar
• Lamai C, Kruatrachue M, Pokethitiyook P, et al. Toxicity and accumulation of lead and cadmium in the filamentous green alga Cladophora fracta (O.F. Muller ex vahl) Kutzing: a laboratory study. Science Asia. 2005;31(2):121–127. doi: 10.2306/scienceasia1513-1874.2005.31.121
   Google Scholar
• León-Vaz A, Romero LC, Gotor C, et al. Effect of cadmium in the microalga Chlorella sorokiniana: a proteomic study. Ecotoxicol Environ Saf. 2021;207:111301. doi: 10.1016/j.ecoenv.2020.111301
   PubMed Web of Science ®Google Scholar
• Carfagna S, Lanza N, Salbitani G, et al. Physiological and morphological responses of lead or cadmium exposed Chlorella sorokiniana 211-8K (chlorophyceae). Springerplus. 2013;2(1):1–7. doi: 10.1186/2193-1801-2-147
   PubMedGoogle Scholar
• Cobbett CS. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 2000;123(3):825–832. doi: 10.1104/pp.123.3.825
   PubMed Web of Science ®Google Scholar
• Wang S, Zhang D, Pan X. Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. Chemosphere. 2013;93(2):230–237. doi: 10.1016/j.chemosphere.2013.04.070
   PubMed Web of Science ®Google Scholar
• Mao Y, Ai H, Chen Y, et al. Phytoplankton response to polystyrene microplastics: perspective from an entire growth period. Chemosphere. 2018;208:59–68. doi: 10.1016/j.chemosphere.2018.05.170
   PubMed Web of Science ®Google Scholar
• Santiago-Martínez MG, Lira-Silva E, Encalada R, et al. Cadmium removal by Euglena gracilis is enhanced under anaerobic growth conditions. J Hazard Mater. 2015;288:104–112. doi: 10.1016/j.jhazmat.2015.02.027
   PubMed Web of Science ®Google Scholar
• Chia MA, Lombardi AT, da Melão MGG, et al. Phosphorus levels determine changes in growth and biochemical composition of Chlorella vulgaris during cadmium stress. J Appl Phycol. 2017;29(4):1883–1891. doi: 10.1007/s10811-017-1111-9
   Web of Science ®Google Scholar
• Pokora W, Baścik-Remisiewicz A, Tukaj S, et al. Adaptation strategies of two closely related Desmodesmus armatus (green alga) strains contained different amounts of cadmium: a study with light-induced synchronized cultures of algae. J Plant Physiol. 2014;171(2):69–77. doi: 10.1016/j.jplph.2013.10.006
   PubMed Web of Science ®Google Scholar
• Mitra M, Kirst H, Dewez D, et al. Modulation of the light-harvesting chlorophyll antenna size in Chlamydomonas reinhardtii by TLA1 gene over-expression and RNA interference. Philos Trans R Soc B. 2012;367(1608):3430–3443. doi: 10.1098/rstb.2012.0229
   PubMed Web of Science ®Google Scholar
• Singh S, Kumar V. Mercury detoxification by absorption, mercuric ion reductase, and exopolysaccharides: a comprehensive study. Environ Sci Pollut Res. 2020;27(22):27181–27201. doi: 10.1007/s11356-019-04974-w
   PubMed Web of Science ®Google Scholar
• Ziller A, Fraissinet-Tachet L. Metallothionein diversity and distribution in the tree of life: a multifunctional protein. Metallomics. 2018;10(11):1549–1559. doi: 10.1039/c8mt00165k
   PubMed Web of Science ®Google Scholar
• Capdevila M, Atrian S. Metallothionein protein evolution: a miniassay. J Biol Inorg Chem. 2011;16(7):977–989. doi: https://doi.org/10.1007/s00775-011-0798-3
   PubMed Web of Science ®Google Scholar
• Olsson S, Penacho V, Puente-Sánchez F, et al. Horizontal gene transfer of phytochelatin synthases from bacteria to extremophilic green algae. Microb Ecol. 2017;73(1):50–60. doi: 10.1007/s00248-016-0848-z
   PubMed Web of Science ®Google Scholar
• Puente-Sánchez F, Díaz S, Penacho V, et al. Basis of genetic adaptation to heavy metal stress in the acidophilic green alga Chlamydomonas acidophila. Aquatic Toxicol. 2018;200:62–72. doi: 10.1016/j.aquatox.2018.04.020
   PubMed Web of Science ®Google Scholar
• Hartwig A. Zinc finger proteins as potential targets for toxic metal ions: differential effects on structure and function. Antioxid Redox Signal. 2001;3(4):625–634. doi: 10.1089/15230860152542970
   PubMed Web of Science ®Google Scholar
• Ebersbach G, Galli E, Møller-Jensen J, et al. Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol Microbiol. 2008;68(3):720–735. doi: 10.1111/j.1365-2958.2008.06190.x
   PubMed Web of Science ®Google Scholar
• Volland S, Bayer E, Baumgartner V, et al. Rescue of heavy metal effects on cell physiology of the algal model system micrasterias by divalent ions. J Plant Physiol. 2014;171(2):154–163. doi: 10.1016/j.jplph.2013.10.002
   PubMed Web of Science ®Google Scholar
• Gai WX, Ma X, Qiao YM, et al. Characterization of the bZIP transcription factor family in pepper (Capsicum annuum L.): CabZIP25 positively modulates the salt tolerance. Front Plant Sci. 2020;11:1–18. doi: 10.3389/fpls.2020.00139
   PubMed Web of Science ®Google Scholar
• Han Y, Hou Z, He Q, et al. Genome-wide characterization and expression analysis of bZIP gene family under abiotic stress in Glycyrrhiza uralensis. Front Genet. 2021;12:1–17. doi: 10.3389/fgene.2021.754237
   Web of Science ®Google Scholar
• Ji C, Mao X, Hao J, et al. Analysis of bZIP transcription factor family and their expressions under salt stress in Chlamydomonas reinhardtii. Int J Mol Sci. 2018;19(9):2800. doi: 10.3390/ijms19092800
   PubMed Web of Science ®Google Scholar
• Bai F, Zhang Y, Liu J. A bZIP transcription factor is involved in regulating lipid and pigment metabolisms in the green alga Chlamydomonas reinhardtii. Algal Res. 2021;59:102450. doi: 10.1016/j.algal.2021.102450
   Google Scholar
• Puente-Sánchez F, Olsson S, Aguilera A. Comparative Transcriptomic Analysis of the Response of Dunaliella acidophila (Chlorophyta) to Short-Term Cadmium and Chronic Natural Metal-Rich Water Exposures. Microb Ecol. 2016;72(3):595–607. doi: 10.1007/s00248-016-0824-7
   PubMed Web of Science ®Google Scholar
• Zheng C, Aslam M, Liu X, et al. Impact of Pb on chlamydomonas reinhardtii at physiological and transcriptional levels. Front Microbiol. 2020;11:1443. doi: 10.3389/fmicb.2020.01443
   PubMedGoogle Scholar
• Mullineaux PM, Exposito-Rodriguez M, Laissue PP, et al. ROS-dependent signalling pathways in plants and algae exposed to high light: comparisons with other eukaryotes. Free Radic Biol Med. 2018;122:52–64. doi: 10.1016/j.freeradbiomed.2018.01.033
   PubMed Web of Science ®Google Scholar