Detection of arsenic-binding siderophores in arsenic-tolerating Actinobacteria by a modified CAS assay

G. Retamal-Morales, M. Mehnert, R. Schwabe, D. Tischler, C. Zapata, R. Chávez, M. Schlömann, G. Levicán

Research output: Contribution to journalArticle

Abstract

The metalloid arsenic is highly toxic to all forms of life, and in many countries decontamination of water and soil is still required. Some bacteria have mechanisms to detoxify arsenic and can live in its presence. Actinobacteria are well known for their ability to produce a myriad of biologically-active compounds. In the present study, we isolated arsenic-tolerant Actinobacteria from contaminated water in Saxony, Germany, and determined their ability to produce siderophores able to bind arsenic. The binding capacity of different siderophore-like compounds was determined by a modified chrome azurol S (As-mCAS) assay with As(III) at high pH and using CAS decolorization as a readout. Arsenic-tolerant isolates from three actinobacterial genera were identified by 16 S rRNA gene sequence analysis: Rhodococcus, Arthrobacter and Kocuria. The isolated Actinobacteria showed a high As(III)-binding activity by siderophore-like compounds, resulting in 82–100% CAS decolorization, as compared to the results with EDTA. The interaction between As(III) and siderophore-like compounds was also detected at neutral pH. In summary, our results suggest that the isolated arsenic-tolerant Actinobacteria produce siderophores that bind arsenic, and open new perspectives on potential candidates for decontaminating environments with arsenic and for other biotechnological applications. © 2018 Elsevier Inc.
LanguageEnglish
Pages176-181
Number of pages6
JournalEcotoxicology and Environmental Safety
Volume157
DOIs
Publication statusPublished - 2018

Fingerprint

Siderophores
Actinobacteria
Arsenic
Assays
Metalloids
Arthrobacter
Rhodococcus
Decontamination
Water
Poisons
Ethylenediaminetetraacetic acid
rRNA Genes
Edetic Acid
Germany
Sequence Analysis
Bacteria
Soil
Genes
Soils

Keywords

  • Actinobacteria
  • Arsenic
  • As-mCAS assay
  • Bioremediation
  • CAS assay
  • Siderophore
  • Arthrobacter
  • Kocuria
  • Rhodococcus

Cite this

Detection of arsenic-binding siderophores in arsenic-tolerating Actinobacteria by a modified CAS assay. / Retamal-Morales, G.; Mehnert, M.; Schwabe, R.; Tischler, D.; Zapata, C.; Chávez, R.; Schlömann, M.; Levicán, G.

In: Ecotoxicology and Environmental Safety, Vol. 157, 2018, p. 176-181.

Research output: Contribution to journalArticle

Retamal-Morales, G. ; Mehnert, M. ; Schwabe, R. ; Tischler, D. ; Zapata, C. ; Chávez, R. ; Schlömann, M. ; Levicán, G. / Detection of arsenic-binding siderophores in arsenic-tolerating Actinobacteria by a modified CAS assay. In: Ecotoxicology and Environmental Safety. 2018 ; Vol. 157. pp. 176-181.
@article{e2d81174ca774e108ec2342b0d13c3a1,
title = "Detection of arsenic-binding siderophores in arsenic-tolerating Actinobacteria by a modified CAS assay",
abstract = "The metalloid arsenic is highly toxic to all forms of life, and in many countries decontamination of water and soil is still required. Some bacteria have mechanisms to detoxify arsenic and can live in its presence. Actinobacteria are well known for their ability to produce a myriad of biologically-active compounds. In the present study, we isolated arsenic-tolerant Actinobacteria from contaminated water in Saxony, Germany, and determined their ability to produce siderophores able to bind arsenic. The binding capacity of different siderophore-like compounds was determined by a modified chrome azurol S (As-mCAS) assay with As(III) at high pH and using CAS decolorization as a readout. Arsenic-tolerant isolates from three actinobacterial genera were identified by 16 S rRNA gene sequence analysis: Rhodococcus, Arthrobacter and Kocuria. The isolated Actinobacteria showed a high As(III)-binding activity by siderophore-like compounds, resulting in 82–100{\%} CAS decolorization, as compared to the results with EDTA. The interaction between As(III) and siderophore-like compounds was also detected at neutral pH. In summary, our results suggest that the isolated arsenic-tolerant Actinobacteria produce siderophores that bind arsenic, and open new perspectives on potential candidates for decontaminating environments with arsenic and for other biotechnological applications. {\circledC} 2018 Elsevier Inc.",
keywords = "Actinobacteria, Arsenic, As-mCAS assay, Bioremediation, CAS assay, Siderophore, Arthrobacter, Kocuria, Rhodococcus",
author = "G. Retamal-Morales and M. Mehnert and R. Schwabe and D. Tischler and C. Zapata and R. Ch{\'a}vez and M. Schl{\"o}mann and G. Levic{\'a}n",
note = "Export Date: 11 April 2018 CODEN: EESAD Correspondence Address: Levic{\'a}n, G.; Universidad de Santiago de Chile, Laboratorio de Microbiolog{\'i}a B{\'a}sica y Aplicada, Facultad de Qu{\'i}mica y Biolog{\'i}aChile; email: gloria.levican@usach.cl Funding details: 033R147, BMBF, Bundesministerium f{\"u}r Bildung und Frauen Funding details: CONICYT, Consejo Nacional de Innovaci{\'o}n, Ciencia y Tecnolog{\'i}a Funding text: This work was supported by Fondecyt Grant (1120746; 1170799) from the government of Chile, and Dicyt-Usach to G.L. G.R-M. was recipient of a Doctoral Fellowship from CONICYT, Chile. A stay of G.R-M. in Freiberg was funded by DAAD-IPID4all project Young GEOMATENUM International (57156629). M.M. and D.T. are funded by BMBF junior research group BakSolEx (033R147), and R.S. by a fellowship of the state of Saxony. References: Alexander, D.B., Zuberer, D.A., Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria (1991) Biol. Fertil. Soils, 12, pp. 39-45; Barka, E.A., Vatsa, P., Sanchez, L., Gaveau-Vaillant, N., Jacquard, C., Klenk, H.-P., Cl{\'e}ment, C., van Wezel, G.P., Taxonomy, physiology, and natural products of Actinobacteria (2016) Microbiol. Mol. Biol. Rev., 80, pp. 1-43; Bosello, M., Zeyadi, M., Kraas, F.I., Linne, U., Xie, X., Marahiel, M.A., Structural characterization of the heterobactin siderophores from Rhodococcus erythropolis PR4 and elucidation of their biosynthetic machinery (2013) J. Nat. Prod., 76, pp. 2282-2290; Braud, A., Geoffroy, V., Hoegy, F., Mislin, G.L.A., Schalk, I.J., Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance (2010) Environ. Microbiol. Rep., 2, pp. 419-425; Braud, A., Hannauer, M., Mislin, G.L.A., Schalk, I.J., The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity (2009) J. Bacteriol., 191, pp. 3517-3525; Braud, A., Hoegy, F., Jezequel, K., Lebeau, T., Schalk, I.J., New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway (2009) Environ. Microbiol., 11, pp. 1079-1091; Braud, A., J{\'e}z{\'e}quel, K., Bazot, S., Lebeau, T., Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria (2009) Chemosphere, 74, pp. 280-286; Cullen, W.R., Reimer, K.J., Arsenic speciation in the environment (1989) Chem. Rev., 89, pp. 713-764; Del Olmo, A., Caramelo, C., SanJose, C., Fluorescent complex of pyoverdin with aluminum (2003) J. Inorg. Biochem., 97, pp. 384-387; Dimkpa, C.O., Merten, D., Svatoš, A., B{\"u}chel, G., Kothe, E., Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus) (2009) J. Appl. Microbiol., 107, pp. 1687-1696; Dimkpa, C., Svatoš, A., Merten, D., B{\"u}chel, G., Kothe, E., Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress (2008) Can. J. Microbiol., 54, pp. 163-172; Drewniak, L., Styczek, A., Majder-Lopatka, M., Sklodowska, A., Bacteria, hypertolerant to arsenic in the rocks of an ancient gold mine, and their potential role in dissemination of arsenic pollution (2008) Environ. Pollut., 156, pp. 1069-1074; Ehinger, S., Seifert, J., Kassahun, A., Schmalz, L., Hoth, N., Schl{\"o}mann, M., Predominance of Methanolobus spp. and Methanoculleus spp. in the archaeal communities of saline gas field formation fluids (2009) Geomicrobiol. J., 26, pp. 326-338; Emmanuel, E.S.C., Ananthi, T., Anandkumar, B., Maruthamuthu, S., Accumulation of rare earth elements by siderophore-forming Arthrobacter luteolus isolated from rare earth environment of Chavara, India (2012) J. Biosci., 37, pp. 25-31; Ess{\'e}n, S.A., Johnsson, A., Bylund, D., Pedersen, K., Lundstr{\"o}m, U.S., Siderophore production by Pseudomonas stutzeri under aerobic and anaerobic conditions (2007) Appl. Environ. Microbiol., 73, pp. 5857-5864; Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap (1985) Evolution, 39 (4), pp. 783-791; Flora, S.J.S., Pachauri, V., Chelation in metal intoxication (2010) Int. J. Environ. Res. Public Health, 7, pp. 2745-2788; Ghosh, P., Rathinasabapathi, B., Teplitski, M., Ma, L.Q., Bacterial ability in AsIII oxidation and AsV reduction: relation to arsenic tolerance, P uptake, and siderophore production (2015) Chemosphere, 138, pp. 995-1000; Gorchev, H.G., Ozolins, G., WHO Guidelines for Drinking-Water Quality (2011) WHO Chronicle; Huang, J.H., Elzinga, E.J., Brechbuehl, Y., Voegelin, A., Kretzschmar, R., Impacts of Shewanella putrefaciens strain CN-32 cells and extracellular polymeric substances on the sorption of As(V) and As(III) on Fe(III)-(hydr)oxides (2011) Environ. Sci. Technol., 45, pp. 2804-2810; Jomova, K., Jenisova, Z., Feszterova, M., Baros, S., Liska, J., Hudecova, D., Rhodes, C.J., Valko, M., Arsenic: toxicity, oxidative stress and human disease (2011) J. Appl. Toxicol., 31, pp. 95-107; Kraemer, S.M., Iron oxide dissolution and solubility in the presence of siderophores (2004) Aquat. Sci., 66, pp. 3-18; Lee, C.Y., Fluorescence spectroscopy (2009) Curr. Protoc. Essent. Lab. Tech., pp. 1-29; Liu, Z., Shen, J., Carbrey, J.M., Mukhopadhyay, R., Agre, P., Rosen, B.P., Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9 (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 6053-6058; Lukasz, D., Liwia, R., Aleksandra, M., Aleksandra, S., Dissolution of arsenic minerals mediated by dissimilatory arsenate reducing bacteria: estimation of the physiological potential for arsenic mobilization (2014) Biomed. Res. Int., p. 2014; Mandal, B.K., Suzuki, K.T., Arsenic round the world: a review (2002) Talanta, 58, pp. 201-235; Marchesi, J.R., Sato, T., Weightman, A.J., Martin, T.A., Fry, J.C., Hiom, S.J., Wade, W.G., Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA (1998) Appl. Environ. Microbiol., 64, pp. 795-799; Marshall, G., Ferreccio, C., Yuan, Y., Bates, M.N., Steinmaus, C., Selvin, S., Liaw, J., Smith, A.H., Fifty-year study of lung and bladder cancer mortality in Chile related to arsenic in drinking water (2007) J. Natl. Cancer Inst., 99, pp. 920-928; Miethke, M., Marahiel, M.A., Siderophore-based iron acquisition and pathogen control (2007) Microbiol. Mol. Biol. Rev., 71, pp. 413-451; Mueller, J.H., Hinton, J., A protein-free medium for primary isolation of the Gonococcus and Meningococcus (1941) Exp. Biol. Med., 48, pp. 330-333; Nair, A., Juwarkar, A.A., Singh, S.K., Production and characterization of siderophores and its application in arsenic removal from contaminated soil (2007) Water Air Soil Pollut., 180, pp. 199-212; Oremland, R.S., Stolz, J.F., The ecology of arsenic (2003) Science, 80 (300), pp. 939-944; Pandey, N., Bhatt, R., Arsenic resistance and accumulation by two bacteria isolated from a natural arsenic contaminated site (2015) J. Basic Microbiol., 55, pp. 1275-1286; Reddy, G.S.N., Aggarwal, R.K., Matsumoto, G.I., Shivaji, S., Arthrobacter flavus sp. nov., a psychrophilic bacterium isolated from a pond in McMurdo Dry Valley, Antarctica (2000) Int. J. Syst. Evol. Microbiol., 50, pp. 1553-1561; Renshaw, J.C., Robson, G.D., Trinci, A.P.J., Wiebe, M.G., Livens, F.R., Collison, D., Taylor, R.J., Fungal siderophores: structures, functions and applications (2002) Mycol. Res., 106, pp. 1123-1142; Schalk, I.J., Hannauer, M., Braud, A., New roles for bacterial siderophores in metal transport and tolerance (2011) Environ. Microbiol., 13, pp. 2811-2854; Schwyn, B., Neilands, J.B., Universal chemical assay for the detection and determination of siderophores (1987) Anal. Biochem., 160, pp. 47-56; Shenker, M., Chen, Y., Hadar, Y., Rapid method for accurate determination of colorless siderophores and synthetic chelates (1995) Soil Sci. Soc. Am. J., 59, p. 1612; Shi, H., Shi, X., Liu, K.J., Oxidative mechanism of arsenic toxicity and carcinogenesis (2004) Mol. Cell. Biochem., 255, pp. 67-78; Slyemi, D., Bonnefoy, V., How prokaryotes deal with arsenic (2012) Environ. Microbiol. Rep., 4, pp. 571-586; Smith, A.H., Ercumen, A., Yuan, Y., Steinmaus, C.M., Increased lung cancer risks are similar whether arsenic is ingested or inhaled (2009) J. Expo. Sci. Environ. Epidemiol., 19, pp. 343-348; Smith, A.H., Hopenhayn-Rich, C., Bates, M.N., Goeden, H.M., Hertz-Picciotto, I., Duggan, H.M., Wood, R., Smith, M.T., Cancer risks from arsenic in drinking water (1992) Environ. Health Perspect., 97, pp. 259-267; Solecka, J., Zajko, J., Postek, M., Rajnisz, A., Biologically active secondary metabolites from Actinomycetes (2012) Open Life Sci., p. 7; Sultana, M., Vogler, S., Zargar, K., Schmidt, A.C., Saltikov, C., Seifert, J., Schl{\"o}mann, M., New clusters of arsenite oxidase and unusual bacterial groups in enrichments from arsenic-contaminated soil (2012) Arch. Microbiol., 194, pp. 623-635; Tamaki, S., Frankenberger, W., Jr, Environmental biochemistry of arsenic (1992) Rev. Environ. Contam. Toxicol. S., 124. , (1.71); Thomas, W., Bellenger, J.P., Morel, F.M.M., Kraepiel, A.M.L., Role of the siderophore azotobactin in the bacterial acquisition of nitrogenase metal cofactors (2009) Environ. Sci. Technol., 43, pp. 7218-7224; Vala, A.K., Vaidya, S.Y., Dube, H.C., Siderophore production by facultative marine fungi (2000) Indian J. Mar. Sci., 29, pp. 339-340; WHO, Environmental Health Criteria 224: Arsenic And Arsenic Compunds (2001), Second edition World Heal. Organ Geneva (doi:NLM Classification: QV 294); Wiegand, I., Hilpert, K., Hancock, R.E.W., Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances (2008) Nat. Protoc., 3, pp. 163-175",
year = "2018",
doi = "10.1016/j.ecoenv.2018.03.087",
language = "English",
volume = "157",
pages = "176--181",
journal = "Ecotoxicology and Environmental Safety",
issn = "0147-6513",
publisher = "Caister Academic Press",

}

TY - JOUR

T1 - Detection of arsenic-binding siderophores in arsenic-tolerating Actinobacteria by a modified CAS assay

AU - Retamal-Morales, G.

AU - Mehnert, M.

AU - Schwabe, R.

AU - Tischler, D.

AU - Zapata, C.

AU - Chávez, R.

AU - Schlömann, M.

AU - Levicán, G.

N1 - Export Date: 11 April 2018 CODEN: EESAD Correspondence Address: Levicán, G.; Universidad de Santiago de Chile, Laboratorio de Microbiología Básica y Aplicada, Facultad de Química y BiologíaChile; email: gloria.levican@usach.cl Funding details: 033R147, BMBF, Bundesministerium für Bildung und Frauen Funding details: CONICYT, Consejo Nacional de Innovación, Ciencia y Tecnología Funding text: This work was supported by Fondecyt Grant (1120746; 1170799) from the government of Chile, and Dicyt-Usach to G.L. G.R-M. was recipient of a Doctoral Fellowship from CONICYT, Chile. A stay of G.R-M. in Freiberg was funded by DAAD-IPID4all project Young GEOMATENUM International (57156629). M.M. and D.T. are funded by BMBF junior research group BakSolEx (033R147), and R.S. by a fellowship of the state of Saxony. References: Alexander, D.B., Zuberer, D.A., Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria (1991) Biol. Fertil. Soils, 12, pp. 39-45; Barka, E.A., Vatsa, P., Sanchez, L., Gaveau-Vaillant, N., Jacquard, C., Klenk, H.-P., Clément, C., van Wezel, G.P., Taxonomy, physiology, and natural products of Actinobacteria (2016) Microbiol. Mol. Biol. Rev., 80, pp. 1-43; Bosello, M., Zeyadi, M., Kraas, F.I., Linne, U., Xie, X., Marahiel, M.A., Structural characterization of the heterobactin siderophores from Rhodococcus erythropolis PR4 and elucidation of their biosynthetic machinery (2013) J. Nat. Prod., 76, pp. 2282-2290; Braud, A., Geoffroy, V., Hoegy, F., Mislin, G.L.A., Schalk, I.J., Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance (2010) Environ. Microbiol. Rep., 2, pp. 419-425; Braud, A., Hannauer, M., Mislin, G.L.A., Schalk, I.J., The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity (2009) J. Bacteriol., 191, pp. 3517-3525; Braud, A., Hoegy, F., Jezequel, K., Lebeau, T., Schalk, I.J., New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway (2009) Environ. Microbiol., 11, pp. 1079-1091; Braud, A., Jézéquel, K., Bazot, S., Lebeau, T., Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria (2009) Chemosphere, 74, pp. 280-286; Cullen, W.R., Reimer, K.J., Arsenic speciation in the environment (1989) Chem. Rev., 89, pp. 713-764; Del Olmo, A., Caramelo, C., SanJose, C., Fluorescent complex of pyoverdin with aluminum (2003) J. Inorg. Biochem., 97, pp. 384-387; Dimkpa, C.O., Merten, D., Svatoš, A., Büchel, G., Kothe, E., Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus) (2009) J. Appl. Microbiol., 107, pp. 1687-1696; Dimkpa, C., Svatoš, A., Merten, D., Büchel, G., Kothe, E., Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress (2008) Can. J. Microbiol., 54, pp. 163-172; Drewniak, L., Styczek, A., Majder-Lopatka, M., Sklodowska, A., Bacteria, hypertolerant to arsenic in the rocks of an ancient gold mine, and their potential role in dissemination of arsenic pollution (2008) Environ. Pollut., 156, pp. 1069-1074; Ehinger, S., Seifert, J., Kassahun, A., Schmalz, L., Hoth, N., Schlömann, M., Predominance of Methanolobus spp. and Methanoculleus spp. in the archaeal communities of saline gas field formation fluids (2009) Geomicrobiol. J., 26, pp. 326-338; Emmanuel, E.S.C., Ananthi, T., Anandkumar, B., Maruthamuthu, S., Accumulation of rare earth elements by siderophore-forming Arthrobacter luteolus isolated from rare earth environment of Chavara, India (2012) J. Biosci., 37, pp. 25-31; Essén, S.A., Johnsson, A., Bylund, D., Pedersen, K., Lundström, U.S., Siderophore production by Pseudomonas stutzeri under aerobic and anaerobic conditions (2007) Appl. Environ. Microbiol., 73, pp. 5857-5864; Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap (1985) Evolution, 39 (4), pp. 783-791; Flora, S.J.S., Pachauri, V., Chelation in metal intoxication (2010) Int. J. Environ. Res. Public Health, 7, pp. 2745-2788; Ghosh, P., Rathinasabapathi, B., Teplitski, M., Ma, L.Q., Bacterial ability in AsIII oxidation and AsV reduction: relation to arsenic tolerance, P uptake, and siderophore production (2015) Chemosphere, 138, pp. 995-1000; Gorchev, H.G., Ozolins, G., WHO Guidelines for Drinking-Water Quality (2011) WHO Chronicle; Huang, J.H., Elzinga, E.J., Brechbuehl, Y., Voegelin, A., Kretzschmar, R., Impacts of Shewanella putrefaciens strain CN-32 cells and extracellular polymeric substances on the sorption of As(V) and As(III) on Fe(III)-(hydr)oxides (2011) Environ. Sci. Technol., 45, pp. 2804-2810; Jomova, K., Jenisova, Z., Feszterova, M., Baros, S., Liska, J., Hudecova, D., Rhodes, C.J., Valko, M., Arsenic: toxicity, oxidative stress and human disease (2011) J. Appl. Toxicol., 31, pp. 95-107; Kraemer, S.M., Iron oxide dissolution and solubility in the presence of siderophores (2004) Aquat. Sci., 66, pp. 3-18; Lee, C.Y., Fluorescence spectroscopy (2009) Curr. Protoc. Essent. Lab. Tech., pp. 1-29; Liu, Z., Shen, J., Carbrey, J.M., Mukhopadhyay, R., Agre, P., Rosen, B.P., Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9 (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 6053-6058; Lukasz, D., Liwia, R., Aleksandra, M., Aleksandra, S., Dissolution of arsenic minerals mediated by dissimilatory arsenate reducing bacteria: estimation of the physiological potential for arsenic mobilization (2014) Biomed. Res. Int., p. 2014; Mandal, B.K., Suzuki, K.T., Arsenic round the world: a review (2002) Talanta, 58, pp. 201-235; Marchesi, J.R., Sato, T., Weightman, A.J., Martin, T.A., Fry, J.C., Hiom, S.J., Wade, W.G., Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA (1998) Appl. Environ. Microbiol., 64, pp. 795-799; Marshall, G., Ferreccio, C., Yuan, Y., Bates, M.N., Steinmaus, C., Selvin, S., Liaw, J., Smith, A.H., Fifty-year study of lung and bladder cancer mortality in Chile related to arsenic in drinking water (2007) J. Natl. Cancer Inst., 99, pp. 920-928; Miethke, M., Marahiel, M.A., Siderophore-based iron acquisition and pathogen control (2007) Microbiol. Mol. Biol. Rev., 71, pp. 413-451; Mueller, J.H., Hinton, J., A protein-free medium for primary isolation of the Gonococcus and Meningococcus (1941) Exp. Biol. Med., 48, pp. 330-333; Nair, A., Juwarkar, A.A., Singh, S.K., Production and characterization of siderophores and its application in arsenic removal from contaminated soil (2007) Water Air Soil Pollut., 180, pp. 199-212; Oremland, R.S., Stolz, J.F., The ecology of arsenic (2003) Science, 80 (300), pp. 939-944; Pandey, N., Bhatt, R., Arsenic resistance and accumulation by two bacteria isolated from a natural arsenic contaminated site (2015) J. Basic Microbiol., 55, pp. 1275-1286; Reddy, G.S.N., Aggarwal, R.K., Matsumoto, G.I., Shivaji, S., Arthrobacter flavus sp. nov., a psychrophilic bacterium isolated from a pond in McMurdo Dry Valley, Antarctica (2000) Int. J. Syst. Evol. Microbiol., 50, pp. 1553-1561; Renshaw, J.C., Robson, G.D., Trinci, A.P.J., Wiebe, M.G., Livens, F.R., Collison, D., Taylor, R.J., Fungal siderophores: structures, functions and applications (2002) Mycol. Res., 106, pp. 1123-1142; Schalk, I.J., Hannauer, M., Braud, A., New roles for bacterial siderophores in metal transport and tolerance (2011) Environ. Microbiol., 13, pp. 2811-2854; Schwyn, B., Neilands, J.B., Universal chemical assay for the detection and determination of siderophores (1987) Anal. Biochem., 160, pp. 47-56; Shenker, M., Chen, Y., Hadar, Y., Rapid method for accurate determination of colorless siderophores and synthetic chelates (1995) Soil Sci. Soc. Am. J., 59, p. 1612; Shi, H., Shi, X., Liu, K.J., Oxidative mechanism of arsenic toxicity and carcinogenesis (2004) Mol. Cell. Biochem., 255, pp. 67-78; Slyemi, D., Bonnefoy, V., How prokaryotes deal with arsenic (2012) Environ. Microbiol. Rep., 4, pp. 571-586; Smith, A.H., Ercumen, A., Yuan, Y., Steinmaus, C.M., Increased lung cancer risks are similar whether arsenic is ingested or inhaled (2009) J. Expo. Sci. Environ. Epidemiol., 19, pp. 343-348; Smith, A.H., Hopenhayn-Rich, C., Bates, M.N., Goeden, H.M., Hertz-Picciotto, I., Duggan, H.M., Wood, R., Smith, M.T., Cancer risks from arsenic in drinking water (1992) Environ. Health Perspect., 97, pp. 259-267; Solecka, J., Zajko, J., Postek, M., Rajnisz, A., Biologically active secondary metabolites from Actinomycetes (2012) Open Life Sci., p. 7; Sultana, M., Vogler, S., Zargar, K., Schmidt, A.C., Saltikov, C., Seifert, J., Schlömann, M., New clusters of arsenite oxidase and unusual bacterial groups in enrichments from arsenic-contaminated soil (2012) Arch. Microbiol., 194, pp. 623-635; Tamaki, S., Frankenberger, W., Jr, Environmental biochemistry of arsenic (1992) Rev. Environ. Contam. Toxicol. S., 124. , (1.71); Thomas, W., Bellenger, J.P., Morel, F.M.M., Kraepiel, A.M.L., Role of the siderophore azotobactin in the bacterial acquisition of nitrogenase metal cofactors (2009) Environ. Sci. Technol., 43, pp. 7218-7224; Vala, A.K., Vaidya, S.Y., Dube, H.C., Siderophore production by facultative marine fungi (2000) Indian J. Mar. Sci., 29, pp. 339-340; WHO, Environmental Health Criteria 224: Arsenic And Arsenic Compunds (2001), Second edition World Heal. Organ Geneva (doi:NLM Classification: QV 294); Wiegand, I., Hilpert, K., Hancock, R.E.W., Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances (2008) Nat. Protoc., 3, pp. 163-175

PY - 2018

Y1 - 2018

N2 - The metalloid arsenic is highly toxic to all forms of life, and in many countries decontamination of water and soil is still required. Some bacteria have mechanisms to detoxify arsenic and can live in its presence. Actinobacteria are well known for their ability to produce a myriad of biologically-active compounds. In the present study, we isolated arsenic-tolerant Actinobacteria from contaminated water in Saxony, Germany, and determined their ability to produce siderophores able to bind arsenic. The binding capacity of different siderophore-like compounds was determined by a modified chrome azurol S (As-mCAS) assay with As(III) at high pH and using CAS decolorization as a readout. Arsenic-tolerant isolates from three actinobacterial genera were identified by 16 S rRNA gene sequence analysis: Rhodococcus, Arthrobacter and Kocuria. The isolated Actinobacteria showed a high As(III)-binding activity by siderophore-like compounds, resulting in 82–100% CAS decolorization, as compared to the results with EDTA. The interaction between As(III) and siderophore-like compounds was also detected at neutral pH. In summary, our results suggest that the isolated arsenic-tolerant Actinobacteria produce siderophores that bind arsenic, and open new perspectives on potential candidates for decontaminating environments with arsenic and for other biotechnological applications. © 2018 Elsevier Inc.

AB - The metalloid arsenic is highly toxic to all forms of life, and in many countries decontamination of water and soil is still required. Some bacteria have mechanisms to detoxify arsenic and can live in its presence. Actinobacteria are well known for their ability to produce a myriad of biologically-active compounds. In the present study, we isolated arsenic-tolerant Actinobacteria from contaminated water in Saxony, Germany, and determined their ability to produce siderophores able to bind arsenic. The binding capacity of different siderophore-like compounds was determined by a modified chrome azurol S (As-mCAS) assay with As(III) at high pH and using CAS decolorization as a readout. Arsenic-tolerant isolates from three actinobacterial genera were identified by 16 S rRNA gene sequence analysis: Rhodococcus, Arthrobacter and Kocuria. The isolated Actinobacteria showed a high As(III)-binding activity by siderophore-like compounds, resulting in 82–100% CAS decolorization, as compared to the results with EDTA. The interaction between As(III) and siderophore-like compounds was also detected at neutral pH. In summary, our results suggest that the isolated arsenic-tolerant Actinobacteria produce siderophores that bind arsenic, and open new perspectives on potential candidates for decontaminating environments with arsenic and for other biotechnological applications. © 2018 Elsevier Inc.

KW - Actinobacteria

KW - Arsenic

KW - As-mCAS assay

KW - Bioremediation

KW - CAS assay

KW - Siderophore

KW - Arthrobacter

KW - Kocuria

KW - Rhodococcus

U2 - 10.1016/j.ecoenv.2018.03.087

DO - 10.1016/j.ecoenv.2018.03.087

M3 - Article

VL - 157

SP - 176

EP - 181

JO - Ecotoxicology and Environmental Safety

T2 - Ecotoxicology and Environmental Safety

JF - Ecotoxicology and Environmental Safety

SN - 0147-6513

ER -