Metals and linear alkylbenzene sulphonate as inhibitors of the algae Pseudokirchneriella subcapitata acid phosphatase activity
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Abstract
Sewage sludge applied to soils as a fertilizer often contains metals and linear alkylbenzene sulphonate (LAS) as contaminants. These pollutants can be transported to the aquatic environment where they can alter the phosphatase activity in living organisms. The acid phosphatase of algae plays important roles in metabolism such as decomposing organic phosphate into free phosphate and autophagic digestive processes. The order of in vitro inhibition of Pseudokirchneriella subcapitata acid phosphatase at the highest concentration tested was LAS > Hg2+ = Al3+ > Se4+ = Pb2+ > Cd2+. A non-competitive inhibition mechanism was obtained for Hg2+ (K i = 0.040 mM) and a competitive inhibition for LAS (K i = 0.007 mM). In vivo studies with treated algae cultures showed that the inhibition of specific activity was observed in algae exposed during 7 days, in contrast to short term (24 h) treatments with both these chemicals. Our results suggest that the inhibition parameters in vitro did not markedly differ between the two chemicals. On the other hand, in vivo evaluations showed strong differences between both pollutants regarding the concentration values and the degree of response.
Keywords
Mercury Toxicity Enzyme Pollutant Selenastrum capricornutum PhytoplanktonNotes
Acknowledgments
This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Empresa Brasileira de Pesquisa Agropecuária (Embrapa). We are grateful to Dr. Ladalav Sodek (Instituto de Biologia, UNICAMP) for helpful discussions and for critically reading the manuscript.
References
- Araujo GM, Silva CB, Hasson-Voloch A (1996) Comparison of the inhibitory effects of mercury and cadmium on the creatine kinase from electrophorous electricus (L). Int J Biochem Cell Biol 28:491–497. doi: 10.1016/1357-2725(95)00146-8 CrossRefGoogle Scholar
- Barceloux DG (1999) Selenium. J Toxicol Clin Toxicol 37:145–172. doi: 10.1081/CLT-100102417 CrossRefGoogle Scholar
- Bounias M, Kruk I, Nectoux M, Popeskovic D (1996) Toxicology of cupric salts on honeybees. V. Gluconate and sulfate action on gut alkaline and acid phosphatases. Ecotoxicol Environ Saf 35:67–76. doi: 10.1006/eesa.1996.0082 CrossRefGoogle Scholar
- Braten T (1975) Ultrastructural localization of phosphohydrolases in gametes, zygotes and zoospores of Ulva mutabilis FØYN. J Cell Sci 17:647–653Google Scholar
- Chaimovich H, Nome F (1970) Purification and properties of an acid phosphatase from bovine brain. Arch Biochem Biophys 139:9–16. doi: 10.1016/0003-9861(70)90039-1 CrossRefGoogle Scholar
- Chawla G, Viswanathan PN, Devi S (1987) Biochemical studies on the toxicity of linear alkylbenzene sulphonate to Scenedesmus quadricauda in culture. Environ Exp Bot 27:311–323. doi: 10.1016/0098-8472(87)90041-4 CrossRefGoogle Scholar
- Chen QX, Zheng WZ, Lin JY, Shi Y, Xie WZ, Zhou HM (2000) Effect of metal ions on the activity of green crab (Scylla serrata) alkaline phosphatase. Int J Biochem Cell Biol 32:879–885. doi: 10.1016/S1357-2725(00)00026-1 CrossRefGoogle Scholar
- Chetty CS, McBride V, Sands S, Rajanna B (1990) Effects in vitro of mercury on rat brain Mg2+-ATPase. Arch Int Physiol Biol 98:261–267. doi: 10.3109/13813459009113986 CrossRefGoogle Scholar
- CONAMA (2005) Resolução n. 357 de 17 de março de 2005. Diário Oficial da União. Ministério do Meio Ambiente. Conselho Nacional do Meio Ambiente, BrasíliaGoogle Scholar
- Cooper A, Bowen ID, Lloyd D (1974) The properties and subcellular localization of acid phosphatases in the colourless alga, Polytomella caeca. J Cell Sci 15:605–618Google Scholar
- Domozych DS (1989) The endomembrane system and mechanism of membrane flow in the green alga, Gloeomonas kupfferi (Volvocales, Chlorophyta) II. A cytochemical analysis. Protoplasma 149:108–119. doi: 10.1007/BF01322983 CrossRefGoogle Scholar
- El Demerdash FM, Elagamy EI (1999) Biological effects in Tilapia nilotica fish as indicators of pollution by cadmium and mecury. Int J Environ Health Res 9:173–186. doi: 10.1080/09603129973146 CrossRefGoogle Scholar
- Erhardt W, Prüeß A (2001) Organic contaminants in sewage sludge for agriculture use. European commission, Joint Research Center, UMEG Center for Environmental Measurements, Karlsruhe, pp 1–73Google Scholar
- Farina M, Brandão R, Lara FS, Soares FA, Souza DO, Rocha JB (2003) Mechanisms of inhibitory effects of selenium and mercury on the activity of delta-aminolevulinate dehydratase from mouse liver, kidney and brain. Toxicol Lett 139:55–66. doi: 10.1016/S0378-4274(02)00454-X CrossRefGoogle Scholar
- Fathi AA (2002) Toxicological response of the green algae Scenedesmus bijuga to mercury and lead. Folia Microbiol (Praha) 47:667–671. doi: 10.1007/BF02818669 CrossRefGoogle Scholar
- Fernandez NA, Chacin E, Gutierrez E, Alastre N, Llamazo B, Forster CF (1995) Adsorption of lauryl benzyl sulphonate on algae. Bioresour Technol 54:111–115. doi: 10.1016/0960-8524(95)00000-3 CrossRefGoogle Scholar
- Gherardi-Goldstein E, Bertoletti E, Zagatto PA, Araujo RPA, Ramos MLLC (1990) Procedimentos para a utilização de testes de toxicidade no controle de efluentes líquidos. Série Manuais, CETESB, Secretaria do Meio Ambiente, São PauloGoogle Scholar
- Gill TS, Tewari H, Pande J (1991) In vivo and in vitro effects of cadmium on selected enzymes in different organs of the fish Barbus conchonius Ham. (Rosy barb). Comp Biochem Physiol C 100:501–505. doi: 10.1016/0742-8413(91)90030-W CrossRefGoogle Scholar
- Helisto P, Korpela T (1998) Effects of detergents on activity of microbial lipases as measured by the nitrophenyl alkanoate esters method. Enzyme Microb Technol 23:113–117. doi: 10.1016/S0141-0229(98)00024-6 CrossRefGoogle Scholar
- Ishikawa M, Sasaki M, Koiwai K, Ozaki M, Takayanagi Y, Sasaki K (1992) Inhibition of hepatic mixed-function oxidase enzymes in mice by acute and chronic treatment with selenium. J Pharmacobiodyn 15:377–385Google Scholar
- James SC (1977) Metals in municipal landfill leachate and their health effects. Am J Public Health 67:429–432. doi: 10.2105/AJPH.67.5.429 CrossRefGoogle Scholar
- Jensen J (1999) Fate and effects of linear alkylbenzene sulphonates (LAS) in the terrestrial environment. Sci Total Environ 226:93–111. doi: 10.1016/S0048-9697(98)00395-7 CrossRefGoogle Scholar
- Jonsson CM, Aoyama H (2007) In vitro effect of agriculture pollutants and their joint action on Pseudokirchneriella subcapitata acid phosphatase. Chemosphere 69:849–855. doi: 10.1016/j.chemosphere.2007.06.024 CrossRefGoogle Scholar
- Jonsson CM, Maia AHN (1999) Protocolo de avaliação de agentes microbianos de controle biológico de pragas para registro como biopesticidas. III Testes em organismos não alvo do ambiente aquático. Serie Documentos, Embrapa Meio Ambiente, JaguariúnaGoogle Scholar
- Jonsson CM, Maia AHN, Ferreira CJA, Ribeiro EO (1998) Risk assessment of the herbicide clomazone to aquatic life. Verh Int Ver Limnol 26:1724–1726Google Scholar
- Jonsson CM, Paraiba LC, Mendoza MT, Sabater C, Carrasco JM (2001) Bioconcentration of the insecticide pyridaphenthion by the green algae Chlorella saccharophila. Chemosphere 43:321–325. doi: 10.1016/S0045-6535(00)00145-4 CrossRefGoogle Scholar
- Keddy CJ, Greene JC, Bonnell MA (1995) Review of whole organism bioassays: soil, freshwater sediment, and freshwater assessment in Canada. Ecotoxicol Environ Saf 30:221–251. doi: 10.1006/eesa.1995.1027 CrossRefGoogle Scholar
- Kong FX, Chen Y (1995) Effect of aluminium and zinc on enzyme activities in the green alga Selenastrum capricornutum. Bull Environ Contam Toxicol 55:759–765. doi: 10.1007/BF00203764 CrossRefGoogle Scholar
- Lowry OH, Rosebrough NJ, Farr AF, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
- Machreki-Ajmi M, Ketata I, Ladhar-Chaabouni R, Hamza-Chaffai A (2008) The effect of in situ cadmium contamination on some biomarkers in Cerastoderma glaucum. Ecotoxicol 17:1–11. doi: 10.1007/s10646-007-0166-9 CrossRefGoogle Scholar
- Mamais D, Kouzeli KA, Christoulas DG, Andreadakis A, Aftias E (2000) Evaluation of agricultural utilization of the sludge produced at Psyttalia WWTP. Water Sci Technol 42:21–27Google Scholar
- Marcelino J, Lima JL, Reis S, Matos C (2007) Assessing the effects of surfactants on the physical properties of liposome membranes. Chem Phys Lipids 146:94–103. doi: 10.1016/j.chemphyslip.2006.12.008 CrossRefGoogle Scholar
- Martinez-Tabche L, Mora BR, Faz CG, Castelan IG, Ortiz MM, Gonzalez VU, Flores MO (1988) Toxic effect of sodium dodecylbenzenesulfonate, lead, petroleum, and their mixtures on the activity of acetylcholinesterase of Moina macrocopa in vitro. Environ Toxicol Water Qual 12:211–215. doi: 10.1002/(SICI)1098-2256(1997)12:3<211::AID-TOX2>3.0.CO;2-B CrossRefGoogle Scholar
- Mazorra MT, Rubio JA, Blasco J (2002) Acid and alkaline phosphatase activities in the clam Scrobicularia plana: kinetic characteristics and effects of heavy metals. Comp Biochem Physiol B 131:241–249. doi: 10.1016/S1096-4959(01)00502-4 CrossRefGoogle Scholar
- Misra V, Kumar V, Pandey SD, Viswanathan PN (1991) Biochemical alterations in fish fingerlings (Cyprinus carpio) exposed to sublethal concentration of linear alkyl benzene sulphonate. Arch Environ Contam Toxicol 21:514–517. doi: 10.1007/BF01183872 CrossRefGoogle Scholar
- Mohan D, Verma SR (1981) Effects of synthetic detergents on in vivo activity of tissue phosphatases and succinic dehydrogenase from Mystus vittatus. Toxicol Lett 8:171–178. doi: 10.1016/0378-4274(81)90046-1 CrossRefGoogle Scholar
- Munkegaard M, Abbaspoor M, Cedergreen N (2008) Organophosphorous insecticides as herbicide synergists on the green algae Pseudokirchneriella subcapitata and the aquatic plant Lemna minor. Ecotoxicol 17:29–35. doi: 10.1007/s10646-007-0173-x CrossRefGoogle Scholar
- Obst U (1988) Application of enzyme assays for toxicological water testing. Toxicol Assess Int J 3:81–91. doi: 10.1002/tox.2540030108 CrossRefGoogle Scholar
- OECD (1984) Guidelines for Testing of Chemicals. Alga, Growth Inhibition Test. Organization for Economic Cooperation and DevelopmentGoogle Scholar
- Omar HH (2002) Bioremoval of zinc by Scenedesmus obliquus and Scenedesmus quadricauda and its effects on growth and metabolism. Int Biodeterior Biodegradation 50:95–100. doi: 10.1016/S0964-8305(02)00048-3 CrossRefGoogle Scholar
- Patni NJ, Aaronson S (1974) Partial characterization of the intra- and extracellular acid phosphatase of an alga, Ochromonas danica. J Gen Microbiol 83:9–20Google Scholar
- Peterson SM, Stauber JL (1996) New algal enzyme bioassay for the rapid assessement of aquatic toxicity. Bull Environ Contam Toxicol 56:750–757. doi: 10.1007/s001289900110 CrossRefGoogle Scholar
- Prasad MN, Drej K, Skawińska A, Strzałka K (1998) Toxicity of cadmium and copper in Chlamydomonas reinhardtii wild-type (WT 2137) and cell wall deficient mutant strain (CW 15). Bull Environ Contam Toxicol 60:306–311. doi: 10.1007/s001289900626 CrossRefGoogle Scholar
- Prazeres JN, Ferreira CV, Aoyama H (2004) Acid phosphatase activities during the germination of Glycine max seeds. Plant Physiol Biochem 42:15–20. doi: 10.1016/j.plaphy.2003.10.009 CrossRefGoogle Scholar
- Rai LC, Husaini Y, Mallick N (1998) pH altered interaction of aluminium and fluoride on nutrient uptake, photosynthesis and other variables of Chlorella vulgaris. Aquat Toxicol 42:67–84. doi: 10.1016/S0166-445X(97)00098-2 CrossRefGoogle Scholar
- Rand GM, Petrocelli SR (1985) Fundamentals of aquatic toxicology: methods and application. Hemisphere, WashingtonGoogle Scholar
- Sartory DP, Grobbelaar JU (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiol 114:177–187Google Scholar
- Shubo H, Min Z, Zhuobin Y, Xin L (2001) A methylene blue mediated enzyme electrode for the determination of trace mercury (II), mercury (I), methylmercury, and mercury glutathione complex. Biosens Bioelectron 16:9–16. doi: 10.1016/S0956-5663(00)00114-7 CrossRefGoogle Scholar
- Sommer JR, Blum JJ (1965) Cytochemical localization of acid phosphatase in Euglena gracilis. J Cell Biol 24:235–251. doi: 10.1083/jcb.24.2.235 CrossRefGoogle Scholar
- Srikanth R, Kumar CS, Khanum A (1992) Heavy metal content in forage grass grown in urban sewage sludge. Indian J Environ Health 34:103–107Google Scholar
- Sugiura Y, Kawabe H, Tanaka H, Fujimoto S, Ohara A (1981) Purification, enzymatic properties and active site environment of a novel manganese(III)-containing acid phosphatase. J Biol Chem 256:10664–10670Google Scholar
- Tanaka H, Horiuchi Y, Konishi K (1975) Determination of surfactants by use of acid phosphatase. Anal Biochem 66:489–497. doi: 10.1016/0003-2697(75)90616-8 CrossRefGoogle Scholar
- Tang J, Hoagland KD, Siegfried BD (1997) Differential toxicity of atrazine to selected freshwater algae. Bull Environ Contam Toxicol 59:631–637. doi: 10.1007/s001289900526 CrossRefGoogle Scholar
- Theodorou ME, Elrifi IR, Turpin DH, Plaxton WC (1991) Effect of phosphorus limitation on respiratory metabolism in the green algae Selenastrum minutum. Plant Physiol 95:1089–1095. doi: 10.1104/pp.95.4.1089 CrossRefGoogle Scholar
- Trivedi SP, Manoj K, Abha M, Indrani B, Ajay S (2001) Impact of linear alkyl benzene sulphonate (LAS) on phosphatase activity in testis of the teleostean fish, Heteropneustes fossilis (Bloch). J Environ Biol 22:263–266Google Scholar
- Tsekos I, Schnepf E (1991) Acid phosphatase activity during spore differentiation of the red algae Gigartina teedii and Chondria tenuissima. Plant Syst Evol 176:35–51. doi: 10.1007/BF00937944 CrossRefGoogle Scholar
- Tukaj Z, Aksmann A (2007) Toxic effects of anthraquinone and phenanthrenequinone upon Scenedesmus strains (green algae) at low and elevated concentration of CO2. Chemosphere 66:480–487. doi: 10.1016/j.chemosphere.2006.05.072 CrossRefGoogle Scholar
- Utsunomiya A, Watanuki T, Matsushita K, Tomita J (1997) Toxic effect of linear alkylbenzenesulfonate and quaternary alkylammonium chloride on Dunaliella sp. as measured by 1H-NMR analysis of glycerol. Chemosphere 35:1215–1226. doi: 10.1016/S0045-6535(97)00194-X CrossRefGoogle Scholar
- Van Assche F, Clijsters H (1990) Effect of metals on enzyme activity in plants. Plant Cell Environ 13:195–206. doi: 10.1111/j.1365-3040.1990.tb01304.x CrossRefGoogle Scholar
- Verma SR, Tonk IP, Chand R (1985) In vivo accumulation and effects of mercuric chloride on tissue phosphatases of Notopterus notopterus. Clin Physiol Biochem 3:199–203. doi: 10.1159/000169414 Google Scholar
- Verma SR, Pal N, Tyagi AK, Dalela RC (1979) Toxicity of Swascol® 1P (SLS) to Channa punctatus and Cirrhina mrigala: biochemical alterations. Bull Environ Contam Toxicol 21:711–718. doi: 10.1007/BF01685493 CrossRefGoogle Scholar
- Vincenzini MT, Favilli F, Terves C, Vanni P (1982) Specific interaction among some enzymes and sodium dodecyl sulfate. Life Sci 31:463–470. doi: 10.1016/0024-3205(82)90332-0 CrossRefGoogle Scholar
- Wells TN, Payton MA, Proudfoot AE (1994) Inhibition of phosphomannose isomerase by mercury ions. Biochem 33:7641–7646. doi: 10.1021/bi00190a018 CrossRefGoogle Scholar
- WHO (1989) Mercury. Environmental aspects. Environmental health criteria 86. International programme on chemical safety. World Health Organization, GenevaGoogle Scholar
- WHO (1996) Linear alkylbenzene sulfonates and related compounds. Environmental health criteria 169. International programme on chemical safety. World Health Organization, Safety, GenevaGoogle Scholar
- Zeitler R, Branzer JP, Bauer C, Reutter W (1992) Inhibition of the biosynthesis of N-acetylneuraminic acid by metal ions and selenium in vitro. Biometals 5:103–109. doi: 10.1007/BF01062221 CrossRefGoogle Scholar