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Redalyc.Efects of Metal Ions (Cd2+, Cu2+, Zn2+) on the Growth And

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Redalyc.Efects of Metal Ions (Cd2+, Cu2+, Zn2+) on the Growth And Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela Machuca, Ángela; Navias, David; Milagres, Adriane M. F.; Chávez, Daniel; Guillén, Yudith Efects of metal ions (Cd2+, Cu2+, Zn2+) on the growth and chelating-compound production of three ectomycorrhizal fungi Interciencia, vol. 39, núm. 4, abril, 2014, pp. 221-227 Asociación Interciencia Caracas, Venezuela Available in: http://www.redalyc.org/articulo.oa?id=33930412002 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative EffECTS OF METAL IONS (Cd2+, Cu2+, Zn2+) ON THE GROWTH anD CHELATIng-COMPOUND PRODUCTION OF THREE ECTOMYCORRHIzaL FUngI ÁngELA MacHUca, DaVID NAVIAS, ADRIanE M. F. MILagRES, DanIEL CHÁVEZ and YUDITH GUILLÉN SUMMARY Several studies have shown that ecotypes of ectomycorrhizal inter- and intraspecific variation in the fungal responses at low fungi from metal-contaminated sites present a high metal toler- and high metal concentrations. Some ecotypes of Rhizopogon ro- ance under in vitro conditions, but it is not clear whether fungi seolus and Suillus luteus were the most tolerant at 1mM Cu and from non-contaminated sites can also develop ecotypes with high 10mM Zn. S. luteus SRS showed tolerance to the three metals. metal tolerance. Tolerance to Cd2+, Cu2+ and Zn2+ ions, and pro- The addition of Cu and Cd stimulated CAS-detected metal-che- duction of chelating compounds as a detoxification mechanism lating compounds and dark pigmentation production in all iso- were evaluated in ectomycorrhizal fungi collected from three un- lates. In the presence of Cd the lowest pH values of the culture contaminated sites (SIS, SRS and ESC). The fungi were grown in media were detected. Hydroxamates and catecholates were de- solid medium with 5 and 20μmol·l-1 Cd, 0.1 and 1mmol·l-1 Cu, and tected only in some isolates, and the catecholates were stimulat- 1 and 10mmol·l-1 Zn, and the tolerance index was determined. ed by Cd in S. luteus and S. bellinii. Among fungi collected from The metal-chelating compounds were determined by Chrome uncontaminated sites it was possible to found ecotypes tolerant Azurol S (CAS) assay, and the chemical nature (hydroxamate or to high metal concentrations and also producers of siderophore- catecholate) of the compounds was analyzed. There was a clear type chelating compounds. tudies have demonstrated dez et al., 2000a; Jentschke and Goldbold, portant that the screening of native ecotypes the importance of ectomy- 2000; Urban, 2011). Metal-tolerant ecotypes of ectomycorrhizal fungi be site/host specif- corrhizal fungi for the may play a crucial role in the establishment ic, ecologically adapted to particular tree plant species with which they form symbi- of mycorrhizal tree seedlings in contaminat- species and edaphoclimatic conditions of the otic associations, since under certain condi- ed soils for the restoration or remediation of region where the mycorrhizal seedlings will tions these fungi may develop ecotypes industrial and metalliferous sites (Godbold be introduced (Ray et al., 2005; Carrillo- with tolerance or resistance to high metal et al., 1998; Schützendübel and Polle, 2002; Gon zález and González-Chávez, 2012). concentrations and thus can protect their Urban 2011). Nevertheless, when the selec- The mechanisms of metal host plants when they grow in metal con- tion of fungal ecotypes is done for the tolerance described in fungi include extra- taminated soils (Hartley et al., 1997; Blau- aforementioned applications, it is very im- cellular chelation through organic com- KEYWORDS / Catecholates / Fungi / Metals / Radial Growth Rate / Rhizopogon roseolus / Suillus bellinii / Suillus luteus / Received: 01/29/2014. Modified: 03/31/2014. Accepted: 03/04/2014. Ángela Machuca. Biochemist, Universidad de Concepción (UdeC), Chile. M.S. and Ph.D. in Biochemistry, Universidade Estadual de Campinas (Unicamp), Brasil. Professor, Universidad de Concepción, Chile. Address: Labo- ratorio de Biotecnología de Hongos, Departamento de Ciencias y Tecnología Vegetal, Escuela de Ciencias y Tecnología, UdeC, Campus Los Ángeles, Chile. e-mail: [email protected] David Navias. Forestry Excecution Engineer, UdeC, Chile. Functionary, Servicio Agrícola Ga- nadero (SAG), Chile. e-mail: [email protected] Adriane M. F. Milagres. Food Engineer, Universidade de Viçosa, Brazil, Doctor en Ciencia con mención en Bioquímica, Unicamp, Brasil. Professor, Universidade de São Paulo, Brasil. e-mail: [email protected] Daniel Chávez. Forestry Excecution Engineer, UdeC, Chile. Forestry Engineer, Universidad Arturo Prat, Chile. Doctoral Candidate, UdeC, Chile. e-mail: [email protected] Yudith Guillén. Forestry Engineer and M.S. in Forest Products Technology, Universidad de Los Andes, Venezuela. Doctor in Forestry Sciences, UEDC, Chile. Professor, Universidad Nacional Experimental de Guayana, Ve- nezuela. e-mail: [email protected] APR 2014, VOL. 39 Nº 4 0378-1844/14/04/221-07 $ 3.00/0 221 pounds released by the fungal hyphae, such Table I as organic acids and siderophores. These Location and soil characteristics of the ectomycorrhizal metal-chelating compounds play a very im- fungi collection sites portant role in metal acquisition by plants, Characteristics fungi and bacteria from their environments Origin Sites Metal content* (mg·kg-1 dry soil) Isolates (Guerinot, 1994; Winkelmann, 2002) and their participation in processes of metal de- San Isidro (SIS) Rhizopogon roseolus SIS Bio Bio Province Sandy loam soil, pH 5.9 Suillus luteus SIS toxification has been also demonstrated 36º55’0”S; 72º0’21”O Fe: 9.4, Zn: 0.1, Cu: 0.2 Suillus bellinii SIS (White et al., 1997; Jentschke and Godbold, Santa Rosa (SRS) Rhizopogon roseolus SRS 2000; Machuca, 2011). Organic acids such Bio Bio Province Sandy soil, pH 6.1 Suillus luteus SRS as oxalic and citric acids are excreted by 37º14’19”S; 72º24’46”O Fe: 4.8, Zn: 0.2, Cu: 0.1 Suillus bellinii SRS mycorrhizal fungi or plant roots into the Escuadron (ESC)** rhizosphere, where they may both mobilize Concepcion Province Clay soil, pH 4.1 Rhizopogon roseolus ESC metal ions from insoluble sources or immo- 73º09’12.76”S; 36º58’55.21”O Fe: 27.2, Zn: 1.1, Cu: 4.1 Suillus luteus ESC bilize them through precipitation (Meharg, 2003; Bellion et al., 2006). Siderophores are *Metal content as total concentration. **During the period when the fruiting bodies were collect- highly specific ferric iron (Fe3+) chelators ed, the S. bellinii species was not found at the ESC site. produced by many fungi and bacteria in re- sponse to Fe deficiency, but they are also ecotypes to be applied in future investiga- 1987; Santiago-Martínez et al., 2003). capable of forming stable complexes with tions on the mycorrhization of forest spe- Each fungal isolate was inoculated in trip- many other metal ions in addition to Fe. cies, assessing the effect of the fungi when licate, with and without metal, and the These compounds can be classed into two the plants are introduced in disturbed soils, means of the values reported. The toler- major groups according to their chemical poor in essential nutrients and/or contami- ance of each isolate was expressed as the structure: hydroxamates and catecholates nated with metals. Tolerance Index (% TI) calculated com- (Hider, 1984; Renshaw et al., 2002). Al- pared to the growth of control culture though siderophores have been associated Material and Methods (without metal). Some morphological with metal detoxification and tolerance in changes in the fungal colonies were visu- bacteria and fungi (Rogers et al., 2001; Il- Fungal isolates and collection sites ally evaluated during the incubation peri- lmer and Buttinger, 2006; Braud et al., od. At the end of the incubation period the 2010; Rajkumar et al. 2010), production of Fruiting bodies of ecto- changes in pH were evaluated in the solid siderophores by ectomycorrhizal fungi mycorrhizal fungi Rhizopogon roseolus Fr., media, with and without metal ions, using growing in the presence of metal ions other Suillus bellinii (Inz.) Kuntze and Suillus lu- a surface pH electrode. than Fe and their possible relation with the teus L. Gray associated with young Pinus tolerance has not been described in the lit- radiata D. Don plantations were collected Detection of metal-chelating compounds in erature to date. from three forest sites located in the central- fungal extracts Several studies have southern region of Chile, where the soils shown that fungal ecotypes from contami- had different chemical and physical charac- At the end of the incuba- nated sites present a higher metal tolerance teristics (Table I). Pure cultures of different tion period (40 days), the content of each than isolates from non-contaminated sites, isolates were obtained from carpophores dish, including mycelium plus MMN me- and in some cases the tolerance displayed and identified at the Fungi Biotechnology dium, with and without metals (Cd, Cu or by the ecotypes is metal-specific to the site Laboratory, Universidad de Concepcion, Zn), was extracted with 20ml of deionised (Adriaensen et al., 2005; Colpaert, 2008; Chile. The stock of fungal cultures was cold water for 20min under agitation. The Colpaert et al., 2011; Urban, 2011). Howev- maintained and cultivated regularly on extracts were filtered through a 0.45μm er, in many cases metal-sensitive ecotypes plates containing solid modified Melin- Millipore membrane and the presence of have also been isolated from contaminated Norkrans(MMN) medium with pH adjusted metal-chelating compounds in the filtrates sites and it is not clear whether fungi found to 5.8 (Marx, 1969) and incubated in the was determined. To do this, 1ml of the fil- in uncontaminated sites can also present dark at 24 ±1°C for 25-30 days. tered fungal extract was mixed with 1ml tolerant ecotypes under in vitro conditions. of Chrome Azurol S (CAS; Schwyn and The aim of this work was to evaluate the Effects of metal ions on fungal growth Neilands 1987).
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