Skip to main content

Advertisement

SpringerLink
Log in

Review of arsenic speciation, toxicity and metabolism in microalgae

  • Review paper
  • Published:
Reviews in Environmental Science and Bio/Technology Aims and scope Submit manuscript

Abstract

Arsenic is a toxic metalloid and its pollution has become a global environmental problem. This paper reviewed the current knowledge on the speciation, toxicity and metabolism of arsenic in microalgae. A number of arsenic species are present in various microalgae. Due to the great toxicity of inorganic arsenic, microalgae may undergo different processes to reduce the arsenic toxicity, including cell surface binding, arsenite [As(III)] oxidation, arsenate [As(V)] reduction, methylation, transformation into arsenosugars or arsenolipids, chelation of As(III) with glutathione and phytochelatins, as well as excretion from cells. Several genes and enzymes involved in arsenic transformations have been identified and characterized. Many factors, especially nutrient elements (e.g., nitrogen and phosphorus) in cells and in culture, affect arsenic metabolic pathways of microalgae. Arsenic metabolism in the unicellular algae has gained considerable interest because these processes control not only the effectiveness of arsenic phycoremediation, but also the risk of arsenic contamination in algal products. Future research need to focus on (1) the regulative mechanisms of arsenic absorption, biotransformation and excretion at molecular level; (2) the effects of intracellular nutrient dynamics on arsenic speciation; (3) the impacts of culture regime on the arsenic metabolism in microalgae; (4) the transfer of arsenic species across aquatic food web in order to better evaluate the roles of microalgae in arsenic cycling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahmad A, Ghufran R, Wahid ZA (2010) Cd, As, Cu, and Zn transfer through dry to rehydrated biomass of Spirulina platensis from wastewater. Pol J Environ Stud 19:887–893

    CAS  Google Scholar 

  • Ajees AA, Marapakala K, Packianathan C, Sankaran B, Rosen BP (2012) Structure of an As (III) S-adenosylmethionine methyltransferase: insights into the mechanism of arsenic biotransformation. Biochem US 51:5476–5485

    CAS  Google Scholar 

  • Andreae MO, Klumpp D (1979) Biosynthesis and release of organoarsenic compounds by marine algae. Environ Sci Technol 13:738–741

    CAS  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2013a) Toxicity, transformation and accumulation of inorganic arsenic species in a microalga Scenedesmus sp. isolated from soil. J Appl Phycol 25:913–917

    CAS  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2013b) Kinetics of arsenite oxidation by Variovorax sp. MM-1 isolated from a soil and identification of arsenite oxidase gene. J Hazard Mater 262:997–1003

    CAS  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2013c) Bioremediation of arsenic-contaminated water: recent advances and future prospects. Water Air Soil Poll 224:1–20

    CAS  Google Scholar 

  • Bhattacharjee H, Mukhopadhyay R, Thiyagarajan S, Rosen BP (2008) Aquaglyceroporins: ancient channels for metalloids. J Biol 7:33

    Google Scholar 

  • Bhumbla DK, Keefer RF (1994) Arsenic mobilization and bioavailability in soils. In: Nriagu JO (ed) Arsenic in the environment, part 1: cycling and characterization. Wiley, Hoboken, pp 51–82

    Google Scholar 

  • Bleeker PM, Schat H, Vooijs R, Verkleij JA, Ernst WH (2003) Mechanisms of arsenate tolerance in Cytisus striatus. New Phytol 157:33–38

    CAS  Google Scholar 

  • Bleeker PM, Hakvoort HW, Bliek M, Souer E, Schat H (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J 45:917–929

    CAS  Google Scholar 

  • Bottino NR, Newman RD, Cox ER, Stockton R, Hoban M, Zingaro RA, Irgolic KJ (1978) The effects of arsenate and arsenite on the growth and morphology of the marine unicellular algae Tetraselmis chui (Chlorophyta) and Hymenomonas carterae (Chrysophyta). J Exp Mar Biol Ecol 33:153–168

    CAS  Google Scholar 

  • Brinza L, Dring MJ, Gavrilescu M (2007) Marine micro- and macro-algal species as biosorbents for heavy metals. Environ Eng Manag J 6:237–251

    CAS  Google Scholar 

  • Budd K, Craig SR (1981) Resistance to arsenate toxicity in the blue-green alga Synechococcus leopoliensis. Can J Bot 59:1518–1521

    CAS  Google Scholar 

  • Casado-Martinez MC, Duncan E, Smith BD, Maher WA, Rainbow PS (2012) Arsenic toxicity in a sediment-dwelling polychaete: detoxification and arsenic metabolism. Ecotoxicology 21:576–590

    CAS  Google Scholar 

  • Caumette G, Koch I, Reimer KJ (2012) Arsenobetaine formation in plankton: a review of studies at the base of the aquatic food chain. J Environ Monitor 14:2841–2853

    CAS  Google Scholar 

  • Challenger F (1945) Biological methylation. Chem Rev 36:315–361

    CAS  Google Scholar 

  • Chaurasia N, Mishra Y, Rai LC (2008) Cloning expression and analysis of phytochelatin synthase (pcs) gene from Anabaena sp. PCC 7120 offering multiple stress tolerance in Escherichia coli. Biochem Bioph Res Commun 376:225–230

    CAS  Google Scholar 

  • Choi H, Park SK, Kim DS, Kim M (2011) Determination of 6 arsenic species present in seaweed by solvent extraction, clean-up, and LC-ICP/MS. Food Sci Biotechnol 20:39–44

    CAS  Google Scholar 

  • Chopin T, Cooper JA, Reid G, Cross S, Moore C (2012) Open-water integrated multi-trophic aquaculture: environmental biomitigation and economic diversification of fed aquaculture by extractive aquaculture. Rev Aquacult 4:209–220

    Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    CAS  Google Scholar 

  • Cullen WR (2014) Chemical mechanism of arsenic biomethylation. Chem Res Toxicol 27:457–461

    CAS  Google Scholar 

  • Cullen WR, Bentley R (2005) The toxicity of trimethylarsine: an urban myth. J Environ Monitor 7:11–15

    CAS  Google Scholar 

  • Cullen WR, Harrison LG, Li H, Hewitt G (1994) Bioaccumulation and excretion of arsenic compounds by a marine unicellular alga, Polyphysa peniculus. Appl Organomet Chem 8:313–324

    CAS  Google Scholar 

  • Dembitsky VM, Levitsky DO (2004) Arsenolipids. Prog Lipid Res 43:403–448

    CAS  Google Scholar 

  • Dhankher OP, Rosen BP, McKinney EC, Meagher RB (2006) Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase (ACR2). P Natl Acad Sci USA 103:5413–5418

    CAS  Google Scholar 

  • Doshi H, Ray A, Kothari IL (2009) Live and dead Spirulina sp. to remove arsenic (V) from water. Int J Phytoremediat 11:53–64

    CAS  Google Scholar 

  • Doucleff M, Terry N (2002) Pumping out the arsenic. Nat Biotechnol 20:1094–1095

    CAS  Google Scholar 

  • Duncan E, Foster S, Maher W (2010) Uptake and metabolism of arsenate, methylarsonate and arsenobetaine by axenic cultures of the phytoplankton Dunaliella tertiolecta. Bot Mar 53:377–386

  • Duncan EG, Maher WA, Foster SD, Krikowa F (2013a) Influence of culture regime on arsenic cycling by the marine phytoplankton Dunaliella tertiolecta and Thalassiosira pseudonana. Environ Chem 10:91–101

    CAS  Google Scholar 

  • Duncan EG, Maher WA, Foster SD, Krikowa F (2013b) The influence of arsenate and phosphate exposure on arsenic uptake, metabolism and species formation in the marine phytoplankton Dunaliella tertiolecta. Mar Chem 157:78–85

    CAS  Google Scholar 

  • Duncan EG, Maher WA, Foster SD, Mikac KM, Krikowa F (2014) The influence of bacteria on the arsenic species produced by laboratory cultures of the marine phytoplankton Dunaliella tertiolecta. J Appl Phycol 26:2129–2134

    CAS  Google Scholar 

  • Duncan EG, Maher WA, Foster SD (2015) Contribution of arsenic species in unicellular algae to the cycling of arsenic in marine ecosystems. Environ Sci Technol 49:33–50

    CAS  Google Scholar 

  • Edmonds JS, Francesconi KA (1983) Arsenic-containing ribofuranosides: isolation from brown kelp Ecklonia radiata and nuclear magnetic resonance spectra. J Chem Soc Perk T1(10):2375–2382

    Google Scholar 

  • Edmonds JS, Shibata Y, Francesconi KA, Rippington RJ, Morita M (1997) Arsenic transformations in short marine food chains studied by HPLC-ICP MS. Appl Organomet Chem 11:281–287

    CAS  Google Scholar 

  • Foster S, Thomson D, Maher W (2008) Uptake and metabolism of arsenate by anexic cultures of the microalgae Dunaliella tertiolecta and Phaeodactylum tricornutum. Mar Chem 108:172–183

    CAS  Google Scholar 

  • Fuhua C, Weiqi C, Shugui D (1994) Toxicities of four arsenic species to Scenedesmus obliguus and influence of phosphate on inorganic arsenic toxicities. Toxico Environ Chem 41:1–7

    Google Scholar 

  • Fujiwara S, Kobayashi I, Hoshino S, Kaise T, Shimogawara K, Usuda H, Tsuzuki M (2000) Isolation and characterization of arsenate-sensitive and resistant mutants of Chlamydomonas reinhardtii. Plant Cell Physiol 41:77–83

    CAS  Google Scholar 

  • García-Salgado S, Quijano MA, Bonilla MM (2006) Optimisation of sample treatment for arsenic speciation in alga samples by focussed sonication and ultrafiltration. Talanta 68:1522–1527

    Google Scholar 

  • García-Salgado S, Quijano MA, Bonilla MM (2012a) Arsenic speciation in edible alga samples by microwave-assisted extraction and high performance liquid chromatography coupled to atomic fluorescence spectrometry. Anal Chim Acta 714:38–46

    Google Scholar 

  • García-Salgado S, Raber G, Raml R, Magnes C, Francesconi KA (2012b) Arsenosugar phospholipids and arsenic hydrocarbons in two species of brown macroalgae. Environ Chem 9:63–66

    Google Scholar 

  • Goessler W, Lintschinger J, Száková J, Mader P, Kopecky J, Doucha J, Irgolic KJ (1997) Chlorella sp. and arsenic compounds: an attempt to prepare an algal reference material for arsenic compounds. Appl Organomet Chem 11:57–66

    CAS  Google Scholar 

  • Gong Y, Chou HN, Tu CD, Liu X, Liu J, Song L (2009) Effects of arsenate on the growth and microcystin production of Microcystis aeruginosa isolated from Taiwan as influenced by extracellular phosphate. J Appl Phycol 21:225–231

    CAS  Google Scholar 

  • Gunaratna KR, Bulbul A, Imamul Huq SM, Bhattacharya P (2006) Arsenic uptake by fresh water green alga, Chlamydomonas species. Presented at the Philadelphia Annual Meeting of GSA, Oct 22–25. Abstract 110153

  • Guo P, Gong Y, Wang C, Liu X, Liu J (2011) Arsenic speciation and effect of arsenate inhibition in a Microcystis aeruginosa culture medium under different phosphate regimes. Environ Toxicol Chem 30:1754–1759

    CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    CAS  Google Scholar 

  • Hartley-Whitaker J, Woods C, Meharg AA (2002) Is differential phytochelatin production related to decreased arsenate influx in arsenate tolerant Holcus lanatus? New Phytol 155:219–225

    CAS  Google Scholar 

  • Hasegawa H, Sohrin Y, Seki K, Sato M, Norisuye K, Naito K, Matsui M (2001) Biosynthesis and release of methylarsenic compounds during the growth of freshwater algae. Chemosphere 43:265–272

    CAS  Google Scholar 

  • Hellweger FL, Farley KJ, Lall U, Di Toro DM (2003) Greedy algae reduce arsenate. Limnol Oceanogr 48:2275–2288

    CAS  Google Scholar 

  • Hirano S, Kobayashi Y, Cui X, Kanno S, Hayakawa T, Shraim A (2004) The accumulation and toxicity of methylated arsenicals in endothelial cells: important roles of thiol compounds. Toxicol Appl Pharm 198:458–467

    CAS  Google Scholar 

  • Hosseini Tafreshi A, Shariati M (2009) Dunaliella biotechnology: methods and applications. J Appl Microbiol 107:14–35

    CAS  Google Scholar 

  • Hsieh YJ, Jiang SJ (2012) Application of HPLC-ICP-MS and HPLC-ESI-MS procedures for arsenic speciation in seaweeds. J Agr Food Chem 60:2083–2089

    CAS  Google Scholar 

  • Huang YK, Lin KH, Chen HW, Chang CC, Liu CW, Yang MH, Hsueh YM (2003) Arsenic species contents at aquaculture farm and in farmed mouthbreeder (Oreochromis mossambicus) in blackfoot disease hyperendemic areas. Food Chem Toxicol 41:1491–1500

    CAS  Google Scholar 

  • Irgolic KJ, Woolson EA, Stockton RA, Newman RD, Bottino NR, Zingaro RA, Kearney PC, Pyles RA, Maeda S, McShane WJ, Cox ER (1977) Characterization of arsenic compounds formed by Daphnia magna and Tetraselmis chuii from inorganic arsenate. Environ Health Persp 19:61–66

    CAS  Google Scholar 

  • Jahan K, Mosto P, Mattson C, Frey E, Derchak L (2006) Microbial removal of arsenic. Water Air Soil Poll 6:71–82

    CAS  Google Scholar 

  • Jiang Y, Purchase D, Jones H, Garelick H (2011) Technical note: effects of arsenate (As5+) on growth and production of glutathione (GSH) and phytochelatins (PCS) in Chlorella vulgaris. Int J Phytoremediat 13:834–844

    CAS  Google Scholar 

  • Johnson DL (1971) Simultaneous determination of arsenate and phosphate in natural waters. Environ Sci Technol 5:411–414

    CAS  Google Scholar 

  • Kaise T, Ogura M, Nozaki T, Saitoh K, Sakurai T, Matsubara C, Watanabe C, Hanaoka KI (1997) Biomethylation of arsenic in an arsenic-rich freshwater environment. Appl Organomet Chem 11:297–304

    CAS  Google Scholar 

  • Kaise T, Fujiwara S, Tsuzuki M, Sakurai T, Saitoh T, Mastubara C (1999) Accumulation of arsenic in a unicellular alga Chlamydomonas reinhardtii. Appl Organomet Chem 13:107–111

    CAS  Google Scholar 

  • Karadjova IB, Slaveykova VI, Tsalev DL (2008) The biouptake and toxicity of arsenic species on the green microalga Chlorella salina in seawater. Aquat Toxicol 87:264–271

    CAS  Google Scholar 

  • Katsoyiannis IA, Zouboulis AI (2002) Removal of arsenic from contaminated water sources by sorption onto iron-oxide-coated polymeric materials. Water Res 36:5141–5155

    CAS  Google Scholar 

  • Khan Z, Bhadouria P, Bisen PS (2005) Nutritional and therapeutic potential of Spirulina. Curr Pharm Biotechno 6:373–379

    CAS  Google Scholar 

  • Knauer K, Hemond H (2000) Accumulation and reduction of arsenate by the freshwater green alga Chlorella sp. (Chlorophyta). J Phycol 36:506–509

    CAS  Google Scholar 

  • Kneer R, Zenk MH (1992) Phytochelatins protect plant enzymes from heavy metal poisoning. Phytochemistry 31:2663–2667

    CAS  Google Scholar 

  • Kobayashi I, Fujiwara S, Shimogawara K, Kaise T, Usuda H, Tsuzuki M (2003) Insertional mutagenesis in a homologue of a Pi transporter gene confers arsenate resistance on Chlamydomonas. Plant Cell Physiol 44:597–606

    CAS  Google Scholar 

  • Kobayashi I, Fujiwara S, Shimogawara K, Sakuma C, Shida Y, Kaise T, Usuda H, Tsuzuki M (2005) High intracellular phosphorus contents exhibit a correlation with arsenate resistance in Chlamydomonas mutants. Plant Cell Physiol 46:489–496

    CAS  Google Scholar 

  • Lai VWM, Cullen WR, Harrington CF, Reimer KJ (1997) The characterization of arsenosugars in commercially available algal products including a Nostoc species of terrestrial origin. Appl Organomet Chem 11:797–803

    CAS  Google Scholar 

  • Lee RE (2008) Phycology, 1st edn. Cambridge University Press, Oxford, p 31

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Lloyd JR, Oremland RS (2006) Microbial transformations of arsenic in the environment: from soda lakes to aquifers. Elements 2:85–90

    CAS  Google Scholar 

  • López-Maury L, Florencio FJ, Reyes JC (2003) Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp strain PCC 6803. J Bacteriol 185:5363–5371

    Google Scholar 

  • López-Maury L, Sánchez-Riego AM, Reyes JC, Florencio FJ (2009) The glutathione/glutaredoxin system is essential for arsenate reduction in Synechocystis sp strain PCC 6803. J Bacteriol 191:3534–3543

    Google Scholar 

  • Lunde G (1972) The analysis of arsenic in the lipid phase from marine and limnetic algae. Acta Chem Scand 26:2642–2644

    CAS  Google Scholar 

  • Lunde G (1973) The synthesis of fat and water soluble arseno organic compounds in marine and limnetic algae. Acta Chem Scand 27:1586–1594

    CAS  Google Scholar 

  • Lunde G (1974) The analysis and characterization of trace elements, in particular bromine, selenium and arsenic in marine organisms, 1st edn. Central Institute for Industrial Research, Blindern, p 150

    Google Scholar 

  • Maeda S, Kumamoto T, Yonemoto M, Nakajima S, Takeshita T, Higashi S, Ueno K (1983) Bioaccumulation of arsenic by freshwater algae and the application to the removal of inorganic arsenic from an aqueous phase Part I Screening of freshwater algae having high resistance to inorganic arsenic. Sep Sci Technol 18:375–385

    CAS  Google Scholar 

  • Maeda S, Nakashima S, Takeshita T, Higashi S (1985) Bioaccumulation of arsenic by freshwater algae and the application to the removal of inorganic arsenic from an aqueous phase Part II By Chlorella vulgaris isolated from arsenic-polluted environment. Sep Sci Technol 20:153–161

    CAS  Google Scholar 

  • Maeda S, Ohki A, Tokuda T, Ohmine M (1990) Transformation of arsenic compounds in a freshwater food chain. Appl Organomet Chem 4:251–254

    CAS  Google Scholar 

  • Maeda S, Kusadome K, Arima H, Ohki A, Naka K (1992) Biomethylation of arsenic and its excretion by the alga Chlorella vulgaris. Appl Organomet Chem 6:407–413

    CAS  Google Scholar 

  • Maeda S, Mawatari K, Ohki A, Naka K (1993) Arsenic metabolism in a freshwater food chain: blue–green alga (Nostoc sp) → shrimp (Neocaridina denticulata) → carp (Cyprinus carpio). Appl Organomet Chem 7:467–476

    CAS  Google Scholar 

  • Mahdavi H, Ulrich AC, Liu Y (2012) Metal removal from oil sands tailings pond water by indigenous micro-alga. Chemosphere 89:350–354

    CAS  Google Scholar 

  • Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235

    CAS  Google Scholar 

  • Merchant RE, Carmack CA, Wise CM (2000) Nutritional supplementation with Chlorella pyrenoidosa for patients with fibromyalgia syndrome: a pilot study. Phytother Res 14:167–173

    CAS  Google Scholar 

  • Mertens J (2011) Al nanoclusters in coagulants and granulates: application in arsenic removal from water. Rev Environ Sci Biol 10:111–117

    CAS  Google Scholar 

  • Mestrot A, Planer-Friedrich B, Feldmann J (2013) Biovolatilisation: a poorly studied pathway of the arsenic biogeochemical cycle. Environ Sci Proc Impacts 15:1639–1651

    CAS  Google Scholar 

  • Meyer S, Schulz J, Jeibmann A, Taleshi MS, Ebert F, Francesconi KA, Schwerdtle T (2014) Arsenic-containing hydrocarbons are toxic in the in vivo model Drosophila melanogaster. Metallomics 6:2010–2014

    CAS  Google Scholar 

  • Michalke K, Wickenheiser EB, Mehring M, Hirner AV, Hensel R (2000) Production of volatile derivatives of metal(loid)s by microflora involved in anaerobic digestion of sewage sludge. Appl Environ Microbiol 66:2791–2796

    CAS  Google Scholar 

  • Michels MH, Vaskoska M, Vermuë MH, Wijffels RH (2014) Growth of Tetraselmis suecica in a tubular photobioreactor on wastewater from a fish farm. Water Res 65:290–296

    CAS  Google Scholar 

  • Milledge JJ (2011) Commercial application of microalgae other than as biofuels: a brief review. Rev Environ Sci Biol 10:31–41

    Google Scholar 

  • Miyashita S, Fujiwara S, Tsuzuki M, Kaise T (2011) Rapid biotransformation of arsenate into oxo-arsenosugars by a freshwater unicellular green alga, Chlamydomonas reinhardtii. Biosci Biotech Bioch 75:522–530

    CAS  Google Scholar 

  • Miyashita S, Fujiwara S, Tsuzuki M, Kaise T (2012) Cyanobacteria produce arsenosugars. Environ Chem 9:474–484

    CAS  Google Scholar 

  • Mok WJ, Senoo S, Itoh T, Tsukamasa Y, Kawasaki KI, Ando M (2012) Assessment of concentrations of toxic elements in aquaculture food products in Malaysia. Food Chem 133:1326–1332

    CAS  Google Scholar 

  • Moreda-Piñeiro J, Alonso-Rodríguez E, Moreda-Piñeiro A, Moscoso-Pérez C, Muniategui-Lorenzo S, López-Mahía P, Prada-Rodríguez D, Bermejo-Barrera P (2010) Simultaneous pressurized enzymatic hydrolysis extraction and clean up for arsenic speciation in seafood samples before high performance liquid chromatography-inductively coupled plasma-mass spectrometry determination. Anal Chim Acta 679:63–73

    Google Scholar 

  • Moreda-Piñeiro A, Moreda-Piñeiro J, Herbello-Hermelo P, Bermejo-Barrera P, Muniategui-Lorenzo S, López-Mahía P, Prada-Rodríguez D (2011) Application of fast ultrasound water-bath assisted enzymatic hydrolysis-high performance liquid chromatography-inductively coupled plasma-mass spectrometry procedures for arsenic speciation in seafood materials. J Chromatogr A 1218:6970–6980

    Google Scholar 

  • Morelli E, Mascherpa MC, Scarano G (2005) Biosynthesis of phytochelatins and arsenic accumulation in the marine microalga Phaeodactylum tricornutum in response to arsenate exposure. Biometals 18:587–593

    CAS  Google Scholar 

  • Morris RJ, McCartney MJ (1984) The ability of a field population of diatoms to discriminate between phosphate and arsenate. Mar Chem 14:259–265

    CAS  Google Scholar 

  • Munoz LP (2014) The mechanisms of arsenic detoxification by the green microalgae Chlorella vulgaris. Dissertation, Middlesex University

  • Munoz LP, Purchase D, Jones H, Feldmann J, Garelick H (2014) Enhanced determination of As-phytochelatin complexes in Chlorella vulgaris using focused sonication for extraction of water-soluble species. Anal Methods UK 6:791–797

    CAS  Google Scholar 

  • Murota C, Matsumoto H, Fujiwara S, Hiruta Y, Miyashita S, Shimoya M, Kobayashi I, Hudock MO, Togasaki RK, Sato N, Tsuzuki M (2012) Arsenic tolerance in a Chlamydomonas photosynthetic mutant is due to reduced arsenic uptake even in light conditions. Planta 236:1395–1403

    CAS  Google Scholar 

  • Murray LA, Raab A, Marr IL, Feldmann J (2003) Biotransformation of arsenate to arsenosugars by Chlorella vulgaris. Appl Organomet Chem 17:669–674

    CAS  Google Scholar 

  • Naranmandura H, Suzuki N, Suzuki KT (2006) Trivalent arsenicals are bound to proteins during reductive methylation. Chem Res Toxicol 19:1010–1018

    CAS  Google Scholar 

  • Nearing MM, Koch I, Reimer KJ (2014) Complementary arsenic speciation methods: a review. Spectrochim Acta B 99:150–162

    CAS  Google Scholar 

  • Nriagu JO, Bhattacharya P, Mukherjee AB, Bundschuh J, Zevenhoven R, Loeppert RH (2007) Arsenic in soil and groundwater: an overview. Trace Metal Contam Environ 9:3–60

    CAS  Google Scholar 

  • Ohki A, Maeda S (2001) Biotransformation of arsenite in freshwater food-chain models. Appl Organomet Chem 15:277–284

    Google Scholar 

  • Ohki A, Kuroiwa T, Maeda S (1999) Arsenic compounds in the freshwater green microalga Chlorella vulgaris after exposure to arsenite. Appl Organomet Chem 13:127–133

    Google Scholar 

  • Olguín EJ, Sánchez-Galván G (2012) Heavy metal removal in phytofiltration and phycoremediation: the need to differentiate between bioadsorption and bioaccumulation. New Biotechnol 30:3–8

    Google Scholar 

  • Paikaray S (2012) Environmental hazards of arsenic associated with black shales: a review on geochemistry, enrichment and leaching mechanism. Rev Environ Sci Biol 11:289–303

    CAS  Google Scholar 

  • Pandey S, Rai R, Rai LC (2012) Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J Proteomics 75:921–937

    CAS  Google Scholar 

  • Patel PC, Goulhen F, Boothman C, Gault AG, Charnock JM, Kalia K, Lloyd JR (2007) Arsenate detoxification in a Pseudomonad hypertolerant to arsenic. Arch Microbiol 187:171–183

    CAS  Google Scholar 

  • Pawlik-Skowrońska B, Pirszel J, Kalinowska R, Skowroński T (2004) Arsenic availability, toxicity and direct role of GSH and phytochelatins in As detoxification in the green alga Stichococcus bacillaris. Aquat Toxicol 70:201–212

    Google Scholar 

  • Petrick JS, Ayala-Fierro F, Cullen WR, Carter DE, Vasken Aposhian H (2000) Monomethylarsonous acid (MMAIII) is more toxic than arsenite in chang human hepatocytes. Toxicol Appl Pharm 163:203–207

    CAS  Google Scholar 

  • Phillips DJH, Depledge MH (1985) Metabolic pathways involving arsenic in marine organisms: a unifying hypothesis. Mar Environ Res 17:1–12

    CAS  Google Scholar 

  • Planas D, Healey FP (1978) Effects of arsenate on growth and phosphorus metabolism of phytoplankton. J Phycol 14:337–341

    CAS  Google Scholar 

  • Posadas E, Muñoz A, García-González MC, Muñoz R, García-Encina PA (2015) A case study of a pilot high rate algal pond for the treatment of fish farm and domestic wastewaters. J Chem Technol Biot 90:1094–1101

    CAS  Google Scholar 

  • Qin J, Rosen BP, Zhang Y, Wang GJ, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci USA 103:2075–2080

    CAS  Google Scholar 

  • Qin J, Lehr CR, Yuan C, Le XC, McDermott TR, Rosen BP (2009) Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proc Natl Acad Sci USA 106:5213–5217

    CAS  Google Scholar 

  • Raja R, Hemaiswarya S, Rengasamy R (2007) Exploitation of Dunaliella for β-carotene production. Appl Microbiol Biotechnol 74:517–523

    CAS  Google Scholar 

  • Rosen BP (1999) Families of arsenic transporters. Trends Microbiol 7:207–212

    CAS  Google Scholar 

  • Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92

    CAS  Google Scholar 

  • Saha JC, Dikshit AK, Bandyopadhyay M, Saha KC (1999) A review of arsenic poisoning and its effects on human health. Crit Rev Environ Sci Technol 29:281–313

    CAS  Google Scholar 

  • Samal AC, Bhar G, Santra SC (2004) Biological process of arsenic removal using selected microalgae. Indian J Exp Biol 42:522–528

    CAS  Google Scholar 

  • Sanders JG (1979) Effects of arsenic speciation and phosphate concentration on arsenic inhibition of Skeletonema costatum (bacillariophyceae). J Phycol 15:424–428

    CAS  Google Scholar 

  • Sanders JG, Windom HL (1980) The uptake and reduction of arsenic species by marine algae. Estuar Coast Mar Sci 10:555–567

    CAS  Google Scholar 

  • Schmidt AC, Koppelt J, Neustadt M, Otto M (2007) Mass spectrometric evidence for different complexes of peptides and proteins with arsenic(III), arsenic(V), copper(II), and zinc(II) species. Rapid Commun Mass Spectrom 21:153–163

    CAS  Google Scholar 

  • Schmöger ME, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–802

    Google Scholar 

  • Scott N, Hatlelid KM, MacKenzie NE, Carter DE (1993) Reactions of arsenic(III) and arsenic(V) species with glutathione. Chem Res Toxicol 6:102–106

    CAS  Google Scholar 

  • Shariatpanahi M, Anderson AC, Abdelghani AA, Englande AJ, Hughes J, Wilkinson RF (1981) Biotransformation of the pesticide sodium arsenate. J Environ Sci Heal B 16:35–47

    CAS  Google Scholar 

  • Smedley P, Kinniburgh D (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568

    CAS  Google Scholar 

  • Sohrin Y, Matsui M, Kawashima M, Hojo M, Hasegawa H (1997) Arsenic biogeochemistry affected by eutrophication in Lake Biwa, Japan. Environ Sci Technol 31:2712–2720

    CAS  Google Scholar 

  • Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96

    CAS  Google Scholar 

  • Sulaymon AH, Mohammed AA, Al-Musawi TJ (2013) Competitive biosorption of lead, cadmium, copper, and arsenic ions using algae. Environ Sci Pollut R 20:3011–3023

    CAS  Google Scholar 

  • Sundaram S, Rathinasabapathi B, Ma LQ, Rosen BP (2008) An arsenate-activated glutaredoxin from the arsenic hyperaccumulator fern Pteris vittata L. regulates intracellular arsenite. J Biol Chem 283:6095–6101

    CAS  Google Scholar 

  • Taboada-de la Calzada A, Villa-Lojo MC, Beceiro-González E, Alonso-Rodríguez E, Prada-Rodríguez D (1999) Accumulation of arsenic(III) by Chlorella vulgaris. Appl Organomet Chem 13:159–162

    Google Scholar 

  • Takimura O, Fuse H, Yamaoka Y (1990) Effect of metal ions on accumulation of arsenic in marine green algae, Dunaliella sp. Appl Organomet Chem 4:265–268

    CAS  Google Scholar 

  • Takimura O, Fuse H, Murakami K, Kamimura K, Yamaoka Y (1996) Uptake and reduction of arsenate by Dunaliella sp. Appl Organomet Chem 10:753–756

    CAS  Google Scholar 

  • Taleshi MS, Seidler-Egdal RK, Jensen KB, Schwerdtle T, Francesconi KA (2014) Synthesis and characterization of arsenolipids: naturally occurring arsenic compounds in fish and algae. Organometallics 33:1397–1403

    CAS  Google Scholar 

  • Thomas DJ, Li J, Waters SB, Xing W, Adair BM, Drobna Z, Devesa V, Styblo M (2007) Arsenic (+3 oxidation state) methyltransferase and the methylation of arsenicals. Exp Biol Med 232:3–13

    CAS  Google Scholar 

  • Ting YP, Prince IG, Lawson F (1991) Uptake of cadmium and zinc by the alga Chlorella vulgaris: II. Multi-ion situation. Biotechnol Bioeng 37:445–455

    CAS  Google Scholar 

  • Velizarov S, Crespo JG, Reis MA (2004) Removal of inorganic anions from drinking water supplies by membrane bio/processes. Rev Environ Sci Biol 3:361–380

    CAS  Google Scholar 

  • Villaescusa I, Bollinger JC (2008) Arsenic in drinking water: sources, occurrence and health effects (a review). Rev Environ Sci Biol 7:307–323

    CAS  Google Scholar 

  • Wang G, Kennedy SP, Fasiludeen S, Rensing C, DasSarma S (2004) Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. J Bacteriol 186:3187–3194

    CAS  Google Scholar 

  • Wang ZZ, Liu GH, Gong DH, Qiao C, Yao Y, Mu QE (2012) Tracking sources of arsenic in the Spirulina Platensis power from the Ordos Alkali lake in Inner Mongolia. Chinese Agr Sci Bull 28:108–111 (in Chinese)

    Google Scholar 

  • Wang NX, Li Y, Deng XH, Miao AJ, Ji R, Yang LY (2013a) Toxicity and bioaccumulation kinetics of arsenate in two freshwater green algae under different phosphate regimes. Water Res 47:2497–2506

    CAS  Google Scholar 

  • Wang ZH, Luo ZX, Yan CZ (2013b) Accumulation, transformation, and release of inorganic arsenic by the freshwater cyanobacterium Microcystis aeruginosa. Environ Sci Pollut R 20:7286–7295

    CAS  Google Scholar 

  • Wang Y, Zhang CH, Wang S, Shen LY, Ge Y (2013c) Accumulation and transformation of different arsenic species in nonaxenic Dunaliella salina. Environ Sci 34:4257–4265 (in Chinese)

    Google Scholar 

  • Wang NX, Huang B, Xu S, Wei ZB, Miao AJ, Ji R, Yang LY (2014a) Effects of nitrogen and phosphorus on arsenite accumulation, oxidation, and toxicity in Chlamydomonas reinhardtii. Aquat Toxicol 157:167–174

    CAS  Google Scholar 

  • Wang PP, Sun GX, Jia Y, Meharg AA, Zhu YG (2014b) A review on completing arsenic biogeochemical cycle: microbial volatilization of arsines in environment. J Environ Sci China 26:371–381

    Google Scholar 

  • Wang ZH, Luo ZX, Yan CZ, Che FF, Yan YM (2014c) Arsenic uptake and depuration kinetics in Microcystis aeruginosa under different phosphate regimes. J Hazard Mater 276:393–399

    CAS  Google Scholar 

  • Wang S, Xu PP, Liu C, Wang Y, Zhang CH, Ge Y (2015) Effects of phosphorus at various concentrations on adsorption, uptake and transformation of arsenate by Spirulina platensis. J Agr Environ Sci 34:1034–1040 (in Chinese)

    Google Scholar 

  • Wesenberg D, Krauss GJ, Schaumlöffel D (2011) Metallo-thiolomics: investigation of thiol peptide regulated metal homeostasis in plants and fungi by liquid chromatography-mass spectrometry. Int J Mass Spectrom 307:46–54

    CAS  Google Scholar 

  • Wrench JJ, Addison RF (1981) Reduction, methylation, and incorporation of arsenic into lipids by the marine phytoplankton Dunaliella tertiolecta. Can J Fish Aquat Sci 38:518–523

    CAS  Google Scholar 

  • Wurl O, Zimmer L, Cutter GA (2013) Arsenic and phosphorus biogeochemistry in the ocean: arsenic species as proxies for P-limitation. Limnol Oceanogr 58:729–740

    CAS  Google Scholar 

  • Xue HB, Sigg L (1990) Binding of Cu(II) to algae in a metal buffer. Water Res 24:1129–1136

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Yamaoka Y, Takimura O, Fuse H, Kamimura K (1990) Accumulation of arsenic and selenium by Dunaliella sp. Appl Organomet Chem 4:261–264

    CAS  Google Scholar 

  • Yamaoka Y, Takimura O, Fuse H, Kamimura K, Murakami K (1996) Accumulation of arsenic by rhaphydophyceae Chattonella antiqua (Hada) Ono. Appl Organomet Chem 10:721–726

    CAS  Google Scholar 

  • Yamaoka Y, Takimura O, Fuse H, Murakami K (1999) Effect of glutathione on arsenic accumulation by Dunaliella salina. Appl Organomet Chem 13:89–94

    CAS  Google Scholar 

  • Yan C, Wang Z, Luo Z (2014) Arsenic efflux from Microcystis aeruginosa under different phosphate regimes. PLoS ONE 9:e116099

    Google Scholar 

  • Yang J, Zhu YG (2009) Progress in study of mechanisms of microbial arsenic transformation in environment. Asian J Ecotox 4:761–769

    Google Scholar 

  • Ye J, Rensing C, Rosen BP, Zhu YG (2012) Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci 17:155–162

    CAS  Google Scholar 

  • Yin XX, Wang LH, Duan GL, Sun GX (2011a) Characterization of arsenate transformation and identification of arsenate reductase in a green alga Chlamydomonas reinhardtii. J Environ Sci China 23:1186–1193

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Yin XX, Wang LH, Bai R, Huang H, Sun GX (2012) Accumulation and transformation of arsenic in the blue-green alga Synechocysis sp. PCC6803. Water Air Soil Poll 223:1183–1190

    CAS  Google Scholar 

  • Zaman K, Pardini RS (1996) An overview of the relationship between oxidative stress and mercury and arsenic. Toxic Subst Mech 15:151–181

    Google Scholar 

  • Zhang B, Wang LH, Xu YX (2011) Study on absorption and transformation of arsenic in blue alga (Synechocystis sp. PCC6803). Asian J Ecotox 6:629–633 (in Chinese)

    CAS  Google Scholar 

  • Zhang JY, Ding TD, Zhang CL (2013a) Biosorption and toxicity responses to arsenite (As(III)) in Scenedesmus quadricauda. Chemosphere 92:1077–1084

    CAS  Google Scholar 

  • Zhang SY, Sun GX, Yin XX, Rensing C, Zhu YG (2013b) Biomethylation and volatilization of arsenic by the marine microalgae Ostreococcus tauri. Chemosphere 93:47–53

    CAS  Google Scholar 

  • Zhang SY, Rensing C, Zhu YG (2014) Cyanobacteria-mediated arsenic redox dynamics is regulated by phosphate in aquatic environments. Environ Sci Technol 489:994–1000

    Google Scholar 

  • Zhao FJ, Wang JR, Barker JHA, Schat H, Bleeker PM, McGrath SP (2003) The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol 159:403–410

    CAS  Google Scholar 

  • Zhao FJ, Zhu YG, Meharg AA (2013) Methylated arsenic species in rice: geographical variation, origin, and uptake mechanisms. Environ Sci Technol 47:3957–3966

    CAS  Google Scholar 

  • Zhu YG, Yoshinaga M, Zhao FJ, Rosen BP (2014) Earth abides arsenic biotransformations. Annu Rev Earth Planet Sci 42:443–467

    CAS  Google Scholar 

Download references

Acknowledgments

This research is supported by Natural Science Foundation of China (41371468, 31400450), China Scholarship Council (201308320137), Jiangsu Provincial Graduate Student Innovation Project (KYZZ_0182) and Undergraduate Student Research Training Program in Nanjing Agricultural University (1313A22). We are also very grateful to three anonymous reviewers for their constructive comments which greatly improved the quality of this manuscript.

Author information

Authors and Affiliations

  1. Jiangsu Provincial Key Laboratory of Marine Biology, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Ya Wang, Shu Wang, Pingping Xu, Cong Liu, Misha Liu, Yulan Wang, Changhai Wang & Ying Ge

  2. Demonstration Laboratory of Element and Life Science Research, Laboratory Centre of Life Science, College of Life Science, Nanjing Agricultural University, Nanjing, China

    Chunhua Zhang

Authors
  1. Ya Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pingping Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Misha Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yulan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Changhai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chunhua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ying Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ying Ge.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Wang, S., Xu, P. et al. Review of arsenic speciation, toxicity and metabolism in microalgae. Rev Environ Sci Biotechnol 14, 427–451 (2015). https://doi.org/10.1007/s11157-015-9371-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11157-015-9371-9

Keywords

Search

Navigation