Algas y Cyanobacteria presentes en la rizosfera de plantas acumuladoras de plomo
DOI:
https://doi.org/10.31055/1851.2372.v56.n1.29317Palavras-chave:
Cianobacterias, Metales pesados, Planta, Plomo, Rizósfera, Trebouxia, VaucheriaResumo
Introducción y objetivos: Las especies de algas y Cyanobacteria que crecen en sitios contaminados pueden acumular altas concentraciones de metales pesados. En este trabajo se propuso a) caracterizar la comunidad de algas y Cyanobacteria y b) evaluar el efecto del plomo (Pb) sobre la composición de algas presentes en la rizosfera de plantas capaces de acumular Pb en la provincia de Córdoba.
M&M: Se tomaron muestras de suelo de la rizosfera de Sorghum halepense, Bidens pilosa y Tagetes minuta en sitios con diferentes niveles de Pb. En el laboratorio, el suelo se sembró en cápsulas con medio de Watanabe esterilizado. Los cultivos crecieron 9 semanas. Se identificó en el tiempo y analizó la frecuencia relativa final de las algas y Cyanobacteria.
Resultados: En suelos contaminados se identificaron 24 especies de Cyanobacteria, Chloroplastida y Xanthophyceae. Las Cyanobacteria con heterocitos Cylindrospermum muscicola, Nostoc commune y Calothrix clavata registraron una frecuencia media relativa (entre 21 y 60%). Trebouxia parmeliae (Chloroplastida) y Vaucheria sp. (Xanthophyceae) estuvieron presentes en los suelos con mayor nivel de Pb. La mayor parte de las especies se concentraron en los niveles más bajos de Pb.
Conclusiones: Se observó un efecto negativo del Pb sobre la riqueza de especies de algas y Cyanobacteria en la rizosfera de las plantas evaluadas. En base a la composición de la comunidad de algas y Cyanobacteria del suelo se determinan dos grandes grupos que podrían ser considerados como comunidades tolerantes y no tolerantes a la contaminación de Pb.
Referências
ALVAREZ, R., A. DEL HOYO, F. G. GARCÍA BREIJO, A. J. REIG, E. M. DEL CAMPO, A. GUÉRA & L. M. CASANO. 2012. Different strategies to achieve Pb-tolerance by the two Trebouxia algae coexisting in the lichen Ramalina farinacea. J. Plant Physiol. 169: 1797-1808. https://doi.org/10.1016/j.jplph.2012.07.005
ARICA, M.Y., I. TÜZÜM, E. YALCIN, Ö, I. & G. BAYRAMOGLU. 2005. Utilisation of native, heat and acid-treated microalgae Chlamydomonas reinhardtii preparations for biosorption of Cr(VI) ions. Proc. Biochem. 40: 2351-2358. https://doi.org/10.1016/j.procbio.2004.09.008
BAČKOR, M. & P. VÁCZI. 2002. Copper tolerance in the lichen photobiont Trebouxia erici (Chlorophyta). Environ. Exp. Bot. 48: 11-20. https://doi.org/10.1016/S0098-8472(02)00004-7
BAČKOR, M., J. HUDÁK, M. REPČÁK, W. ZIEGLER & M. BAČKOROVÁ. 1998. The influence of pH and lichen metabolites (vulpinic acid and (+) usnic acid) on the growth of lichen photobiont Trebouxia irregularis. The Lichenologist 30: 577-582. https://doi.org/10.1017/S0024282992000574
BAUER, D. E., V. CONFORTI, L. RUIZ & N. GÓMEZ. 2012. An in situ test to explore the responses of Scenedesmus acutus and Lepocinclis acus as indicators of the changes in water quality in lowland streams. Ecotoxicol. Environ. Safety 77: 71-78. https://doi.org/10.1016/j.ecoenv.2011.10.021
BELNAP, J. 1993. Recovery rates of cryptobiotic soil crusts: inoculant use and assessment methods. Great Basin Nat. 53: 89-95.
BIRUK, L. N., J. MORETTON, A. FABRIZIO DE IORIO, C. WEIGANDT, J. ETCHEVERRY, J. FILIPETTO & A. MAGDALENO. 2017. Toxicity and genotoxicity assessment in sediments from the Matanza-Riachuelo river basin (Argentina) under the influence of heavy metals and organic contaminants. Ecotoxicol. Environ. Safety 135: 302-311. https://doi.org/10.1016/j.ecoenv.2016.09.024
BOURELLY, P. 1981. Les Algues d'eau douce: Initiation a la systematique. Tome III: Les Algues jaunes at brunes. Chrysophycées. Phéophycées. Xanthophycées et Diatomées. Societé Nouvelle des Editions Boubée, Paris.
BRAY, R. H. & L. T. KURTZ. 1945. Determination of total organic and available forms of phosphorus in soils. Soil Science 59: 39-45. http://dx.doi.org/10.1097/00010694-194501000-00006
BREMNER J. M. 1996. Nitrogen total. In: SPARKS L., A.L. PAGE, P.A. HELMKE, R.H. LOEPPERT, P. N. SOLTANPOUR, M. A. TABATABAI, C. T. JOHNSTON & M. E. SUMNER (eds). Methods of Soil Analysis. Part 3. Chemical Methods. pp. 1085-1121. Soil Science Society of America and American Society of Agronomy, Madison, USA. https://doi.org/10.2136/sssabookser5.3.c37
BUBRICK, P., M. GALUN & A. FRENSDORFF. 1984. Observations on free-living Trebouxia de Puymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th. Fr. Can be found free-living in nature. New Phytol. 97: 455-462. https://doi.org/10.1111/j.1469-8137.1984.tb03611.x
CHRIST, R. H., K. OBERHOLSER, N. SHANK & M. NGUYEN. 1980. Nature of bonding between metallic ions and algal cell walls. Environ. Sci. Technol. 15: 1212-1217.https://doi.org/10.1021/es00092a010
EPA, U. 2007. Brownfields Road Map to Understanding Options for Site Investigation and Cleanup. AGENCY U.S.E.P. Sixth Edition [online]. Disponible en: www.epa.gov/brownfields/brownfields-roadmap [Acceso: 5 Julio 2020].
ESSA, A. M. M. & S. S. M. MOSTAFA. 2011. Heavy metals biomineralization by some cyanobacterial isolates. Egypt. J. Bot. 11: 146-153.
FAO & ITPS. 2015. Status of the World’s Soil Resources (SWSR) - Main Report. Rome, Italy, Food and Agriculture Organization of the United Nations and Intergovernmental Technical Panel on Soils [online]. Disponible en: http://www.fao.org/3/a-i5199e.pdf [Acceso: 5 Julio 2020].
FOSTER, P. L. 1982. Metal resistance of Chlorophyta from rivers polluted by heavy metals. Freshwater Biol. 12: 41-61. https://doi.org/10.1111/j.1365-2427.1982.tb00602.x
FU, P. & F. SECUNDO. 2016. Algae and their bacterial consortia for soil bioremediation. Chem. Enginn. Trans. 49: 427-432. http://doi.org/10.3303/CET1649072
GARCÍA-MEZA, J. V., A. CARRILLO-CHAVEZ & O. MORTON-BERMEA. 2006. Sequential extractions on mine tailings samples after and before bioassays: implications on the speciation of metals during microbial re-colonization. Environ. Geol. 49: 437-448. https://doi.org/10.1007/s00254-005-0101-4
GORGAS J. & J. TASSILE. 2003. Recursos Naturales de la Provincia de Córdoba. Vol. 1. INTA, Córdoba, Argentina.
GUPTA, R. K., K. K. CHOUDHARY, M. KUMAR, A. NEGI & H. RAI. 2012. Bioremediation and cyanobacteria an overview. BioNano Frontiers 9: 190-196.
HALPERIN, D.R., M. I. MENDOZA & G. ZULPA DE CAIRE. 1973. Obtención de cultivos axénicos de algas azules (Cyanophyta). Physis 32: 67-84.
HIFNEY, A.F., A. A. ISSA, M. S. ADAM & A. A. AL-ABSSY. 2009. The influence of the heavy metals (Cd2+, Ni2+ and Pb2+) concentrations on the algal distribution as well as species composition in relation to soil types. Egypt. J. Bot. 38: 121-134.
HOFFMAN, L. 1989. Algae of Terrestrial Habitats. Bot. Rev. 55: 77-105. https://doi.org/10.1007/BF02858529
HONEGGER, R. 1991. Functional aspects of the lichen symbiosis. Ann. Rev. Physiol Plant Mol. Biol. 42: 553-558. https://doi.org/10.1146/annurev.pp.42.060191.003005
HUBER-PESTALOZZI, G. 1961. Das Phytoplankton des Süsswasser, Chlorophyceae. In: THIENEMANN A. (ed). Die Binnengewasser, E. Schweizerbar t’sche Verlagsbuchhandlung, Stuttgart.
JACKSON, M. L. 1964. Análisis químico de suelos. 2nd Edn. Omega, Barcelona, España.
JOHANSEN, J. R. & L. E. SHUBERT. 2001. Algae in Soils. Nova Hedwigia 123: 297-306.
KOMÁREK J. & K. ANAGNOSTIDIS. 1998. Cyanoprokaryota 1. Chroococcales. In: ETTL, H., G. GÄRTNER, H. HEYNIG & D. MOLLENHAUER (eds.), Süßwasserflora von Mitteleuropa, Gustav Fischer, pp. 548, Jena-Stuttgart- Lübeck-Ulm.
KOMÁREK, J. & K. ANAGNOSTIDIS. 2005. Cyanoprokariota: Oscillatoriales. In: BÜDEL B., L. KRIENITZ, G. GÄRTNER & M. SCHAGERL (eds.), Süßwasserflora von Mitteleuropa, 1ra edición. pp. 759, Elsevier, München.
KOMÁREK, J., C. L. SANT´ANNA, M. BOHUNICKÁ, J. MAREŠ, G. S. HENTSCHKE, J. RIGONATO & M. F. FIORE. 2013. Phenotype diversity and phylogeny of selected Scytonema-species (Cyanoprokaryota) from SE Brazil. Fottea 13: 173-200. https://doi.org/10.5507/fot.2013.015
KOMÁREK, J., J. KAŠTOVSKÝ, J. MAREŠ & J. R. JOHANSEN. 2014. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) using a polyphasic approach. Preslia 86: 295-235.
KOMÁREK, J. & T. HAUER. 2013. CyanoDB.cz -On-line database of cyanobacterial genera. Word-wide electronic publication, Univ. of South Bohemia & Inst. of Botany, AS CR [online]. Disponible en: http://www.cyanodb.cz. [Acceso: 2 July 2020].
KULAL, D. K., C. L. PRAKASH, C. DCOSTA, S. SOME & P. K. KALAMBATE. 2020.
KUMAR, V. KUMAR SINGH & A. K. SHRIVASTAVA. Advances in Cyanobacterial Biology, pp. 291-300. Academic Press. https://doi.org/10.1016/B978-0-12-819311-2.00019-X
KUMAR, J. I. N., C. OOMMEN & R. N. KUMAR. 2009. Biosorption of heavy metals from aqueous solution by green marine macroalgae from Okha port, Gulf of Kutch, India. Am.-Eur. J. Agric. Environm. Sci. 6: 317-323.
KUMAR K., R. A. MELLELLA-HERRARA & J. W. GOLDEN. 2010. Cyanobacterial Heterocysts. Cold Spring Harb. Perspect. Biol. 2: a000315. https://doi: 10.1101/cshperspect.a000315
KUZYAKHMETOV, G. G. 1998. Algological evaluation of the toxicity of copper compounds in gray forest soil and leached chernozem. Eur. Soil Sci. 31: 877-882.
LA VOZ DEL INTERIOR. 2006. Más intoxicados con plomo en Bouwer [online]. Disponible en: http://archivo.lavoz.com.ar/nota.asp?nota_id=2144 [Acceso: 4 de noviembre 2020].
LA VOZ DEL INTERIOR. 2008. Bouwer sitiado por la contaminación [online]. Disponible en: http://archivo.lavoz.com.ar/08/02/10/secciones/grancordoba/nota.asp?nota_id=160954 [Acceso: 28 de diciembre 2020].
LICURSI, M. & N. GÓMEZ. 2013. Short-term toxicity of hexavalent-chromium to epipsammic diatoms of a microtidal estuary (Río de la Plata): Responses from the individual cell to the community structure. Aquat. Toxicol. 134-135: 82-91. https://doi.org/10.1016/j.aquatox.2013.03.007
LUKEŠOVÁ, A. 2001. Soil algae in brown coal and lignite post-mining areas in central Europe (Czech Republic and Germany). Restor. Ecol. 9: 341-350. https://doi.org/10.1046/j.1526-100X.2001.94002.x
LUKEŠOVÁ, A. & L. HOFFMANN. 1996. Soil algae from acid impacted forest areas of the Krušné Hory Mts. 1. Algal communities. Vegetatio 125: 123-136. https://doi.org/10.1007/BF00044646
MAGDALENO, A., L. DE CABO, S. ARREGHINI & S. SALINAS. 2014. Assessment of heavy metal contamination and water quality in an urban river from argentina. Braz. J. Aquat. Sci. Technol. 18: 113-120. https://doi.org/10.14210/bjast.v18n1.p113-120
MAHMOOD, Q., N. MIRZA & S. SHAHEEN. 2015. Phytoremediation using algae and macrophytes: I. In: ANSARI, A., S. GILL, R. GILL, G. LANZA & L. NEWMAN (eds.). Phytoremediation Springer, Cham., pp. 265-289. https://doi.org/10.1007/978-3-319-10969-5_22
MAXWELL, C. D. 1991. Floristic changes in soil algae and cyanobacteria in reclaimed metal-contaminated land at Sudbury, Canada. Water Air Soil Pollut. 60: 381-393. https://doi.org/10.1007/BF00282633
METTING, B. 1981. The systematics and ecology of soil algae. Bot. Rev. 47: 195-312. https://doi.org/10.1007/BF02868854
MULLER, G. 1969. Index of geoaccumulation in sediments of the Rhine River. GeoJournal 2: 108-118.
MURIALDO, R. C., M.C. FERNÁNDEZ BELMONTE, I. C. DAGA, C. GONZÁLEZ & H. E. MURIALDO. 2019. Contribución al estudio de cianobacterias edáficas en un suelo con manejo agrícola de Córdoba-Argentina. Ciencia del Suelo 37: 383-387.
NALEWAIKO, C. & M. M. OLAVESON. 1995. Differential responses of growth, photosynthesis, respiration phosphate uptake to copper in copper-tolerant and copper-in-tolerant strains of Scenedesmus aqutus (Chlorophyceae). Can. J. Bot. 73: 1295-1303. https://doi.org/10.1139/b95-141
NOVAKOVSKAYA, I. V. & E. N. PATOVA. 2007. Changes in soil algal communities in spruce phytocenoses under the influence of aerotechnogenic pollution. Eur. Soil Sci. 40: 576-582. https://doi.org/10.1134/S1064229307050146
OKSANEN, J. 2015. Vegan: an introduction to ordination. Disponible en: http://cran.r-project.org.
O’FARRELL I., R. J. LOMBARDO, P. DE TEZANOS PINTO & C. LOEZ. 2002. The assessment of water quality in the Lower Luján River (Buenos Aires, Argentina): phytoplankton and algal bioassays. Environ. Pollution 120: 207-218. https://doi.org/10.1016/S0269-7491(02)00136-7
PAWLIK-SKOWRONSKA, B. 2000. Relationships between acid–soluble thiol peptides and accumulated Pb in the green alga Stichococcus bacillaris. Aquat. Toxicol. 50: 221-230. https://doi.org/10.1016/S0166-445X(99)00102-2
PAWLIK-SKOWRONSKA, B 2002. Correlations between toxic Pb effects and production of Pb-induced thiol peptides in the microalga Stichococcus bacillaris. Environ. Pollut. 119: 119-227. https://doi.org/10.1016/S0269-7491(01)00280-9
PEPPER, I. L., C. P. GERBA, D. T. NEWBY & C. W. RICE. 2009. Soil: a public health threat or savior? Crit. Rev. Environ. Sci. Tech. 39: 416-432. https://doi.org/10.1080/10643380701664748
RAUNGSOMBOON, S., A. CHIDTHAISONG, B. BUNNAG, D. INTHORN & N. W. HARVEY. 2008. Removal of lead (Pb2+) by the Cyanobacterium Gloeocapsa sp. Biores. Tech. 99: 5650-5658. https://doi.org/10.1016/j.biortech.2007.10.056
R CORE TEAM. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Disponible en: https://www.R-project.org.
RIPPKA, R., J. DERUELLES, J. B. WATERBURY, M. HERDMAN & R. Y. STANIER. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111: 1-61. https://doi.org/10.1099/00221287-111-1-1
RODRÍGUEZ, C., I. ROCCHETTA, A. JUAREZ, A. TOLIVIA & V. CONFORTI. 2008. Toxicidad de los metales pesados sobre las microalgas: efectos bioquímicos, fisiológicos y morfológicos. En: RIAL A., A. VOLPEDO & L. FERNÁNDEZ REYES (eds.), Efecto de los cambios globales sobre la biodiversidad RED CYTED, Buenos Aires, Argentina, pp. 261-280.
ROY, S., A. N. GHOSH & A. R. THAKUR. 2008. Uptake of Pb2 by a cyanobacterium belonging to the genus Synechocystis, isolated from East Kolkata Wetlands. Biometals 21: 515-524. https://doi.org/10.1007/s10534-008-9138-7
SALAZAR, M. J. & M. L. PIGNATA. 2014. Lead accumulation in plants grown in polluted soils. Screening of native species for phytoremediation. J. Geochem. Explor. 137:29-36. https://doi.org/10.1016/j.gexplo.2013.11.003
SALAZAR, M. J., J. H. RODRIGUEZ, G. L. NIETO, & M. L. PIGNATA. 2012. Effects of heavy metal concentrations (Cd, Zn and Pb) in agricultural soils near different emission sources on quality, accumulation and food safety in soybean [Glycine max (L.) Merrill]. J. Hazard. Mat. 233-234: 244-253. https://doi.org/10.1016/j.jhazmat.2012.07.026
SALAZAR, M. J., E. MENOYO, V. FAGGIOLI, J. GEML, M. CABELLO, J. RODRIGUEZ, N. MARRO, A. PARDO, M. L. PIGNATA & A. G. BECERRA. 2018. Pb accumulation in spores of arbuscular mycorrhizal fungi. Sci. Total Environ. 643: 238-246. https://doi.org/10.1016/j.scitotenv.2018.06.199
SALGADO, S. G., M. A. Q. NIETO & N. M. B. SIMON. 2006. Optimisation of sample treatment for arsenic speciation in alga samples by focussed sonication and ultrafiltration. Talanta 68: 1522-1527. https://doi.org/10.1016/j.talanta.2005.08.004
SATHICQ, M. B. & N. GÓMEZ. 2018. Effects of hexavalent chromium on phytoplankton and bacterioplankton of the Río de la Plata estuary: an ex-situ assay. Environ. Monit. Assess. 190: 229. https://doi.org/10.1007/s10661-018-6619-1
SARAVANAN, A., V. BRINDHA & S. KRISHNAN. 2011. Characteristic study of the marine algae Sargassum sp. on metal adsorption. Am. J. Appl. Sci. 8: 691-694. https://doi.org/10.3844/ajassp.2011.691.694
SCHINQUEL, V., R. MURIALDO & C. DAGA. 2018. Cianobacterias edáficas en un relicto de monte nativo de la Provincia de Córdoba. Rev. Fac. Cs. Ex. Fis. Nat. 5: 59-67.
SHTINA, E. A. & M. M. GOLLERBAKH. 1976. Ecology of Soil Algae. Science Publishing House, Moscow, pp. 143.
SHUBERT, L. E., A-M RUSU, K. BARTOK & C. B. MONCRIEFF. 2001. Distribution and abundance of edaphic algae adapted to highly acidic, metal rich soil. In: ELSTER J. & O. LHOTSKY (eds), Algae and extreme environments, Nova Hedwigia, Beiheft 123: 411-425.
SINGH, J. S., A. KUMAR, A. N. RAI & D. P. SINGH. 2016. Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front. Microbiol. 7: 529. https://doi.org/10.3389/fmicb.2016.00529
SINGH, R., P. PARIHAR, M. SINGH, A. BAJGUZ, J. KUMAR & S. SINGH. 2017. Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front. Microbiol. 8: 515. https://doi.org/10.3389/fmicb.2017.00515
SKOWRONSKI T., J. A. DE KNECHT, J. SIMONS & J. A. C. VERKLEIJ. 1998. Phytochelatin synthesis in response to cadmium uptake in Vaucheria (Xanthophyceae). Eur. J. Phycol. 33: 87-91. https://doi.org/10.1017/S0967026298001516
SUBASHCHANDRABOSE, S. R., B. RAMAKRISHNAN, M. MEGHARAJ, K. VENKATESWARLU & R. NAIDU. 2013. Mixotrophic Cyanobacteria and Microalgae as Distinctive Biological Agents for Organic Pollutant Degradation. Environ. Inter. 51: 59-72. https://doi.org/10.1016/j.envint.2012.10.007
SURESH, B. & G. A. RAVISHANKAR. 2004. Phytoremediation-a novel and promising approach for environmental clean-up. Crit. Rev. Biotech. 24: 97-124. https://doi.org/10.1080/07388550490493627
TELL, G. 1976. Algas del suelo de los alrededores de Buenos Aires (República Argentina). Darwiniana 20: 491-548.
TEMRALEEVA, A. D., D. L. PINSKII, E. N. PATOVA & E. V. SPIRINA. 2011. The use of algae–Cyanobacterial communities for the assessment of lead pollution of gray forest soils. Eur. Soil Sci. 44: 326-331. https://doi.org/10.1134/S1064229311030136
TREVORS, J. T. 1984. Effect of substrate concentration, inorganic nitrogen, O2 concentration, temperature and pH on dehydrogenase activity in soil. Plant Soil 77: 285-93. https://doi.org/10.1007/BF02182931
TRZCIŇSKA, M. & B. PAWLIK-SKOWROŇSKA. 2008. Soil algal communities inhabiting zinc and lead mine spoils. J. Appl. Phycol. 20: 341-348. https://doi.org/10.1007/s10811-007-9259-3
WALKLEY, A. J. & I. A. BLACK. 1934. Estimation of soil organic carbon by the chromic acid titration method. Soil Sci. 37: 29-38.
WATANABE, A. 1961. Collection and cultivation of nitrogen fixing blue-green algae and their effect on the growth and crop yield of rice plants. Stud. Tokugawa Inst. Tokyo 9: 162-166.
WEISSENHORN, L. & C. LEYVAL. 1995. Root colonization of maize by a Cd-sensitive and Cd-tolerant Glomus mosseae and cadmium uptake in sand culture. Plant Soil 175: 233-238.
WHO. 2013. Contaminated sites and health. Copenhagen, Denmark. [online]. Disponible en: http://www.euro.who.int/__data/assets/pdf_file/0003/186240/e96843e.pdf [Acceso: 5 July 2020].
YOON, H. S., C. CINIGLIA, M. WU, J. COMERON, G. PINTO, A. POLLIO & D. BHATTACHARYA. 2006. Establishment of endolithic populations of extremophilic Cyanidiales (Rhodophyta). BMC Evol. Biol. 6: 78. https://doi.org/10.1186/1471-2148-6-78
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