Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim Degradation

Carbendazim (CBZ) is a fungicide widely used on different crops, including soybeans, cereals, cotton, tobacco, peanuts, and sugar beet. Excessive use of this xenobiotic causes environmental deterioration and affects human health. Microbial metabolism is one of the most efficient ways of carbendazim...

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Main Authors: Roosivelt Solano-Rodríguez, Fortunata Santoyo-Tepole, Mario Figueroa, Voleta Larios-Serrato, Nora Ruiz-Ordaz, Abigail Pérez-Valdespino, Everardo Curiel-Quesada
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Language:English
Published: MDPI AG 2024-12-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/13/1/40
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author Roosivelt Solano-Rodríguez
Fortunata Santoyo-Tepole
Mario Figueroa
Voleta Larios-Serrato
Nora Ruiz-Ordaz
Abigail Pérez-Valdespino
Everardo Curiel-Quesada
author_facet Roosivelt Solano-Rodríguez
Fortunata Santoyo-Tepole
Mario Figueroa
Voleta Larios-Serrato
Nora Ruiz-Ordaz
Abigail Pérez-Valdespino
Everardo Curiel-Quesada
author_sort Roosivelt Solano-Rodríguez
collection DOAJ
description Carbendazim (CBZ) is a fungicide widely used on different crops, including soybeans, cereals, cotton, tobacco, peanuts, and sugar beet. Excessive use of this xenobiotic causes environmental deterioration and affects human health. Microbial metabolism is one of the most efficient ways of carbendazim elimination. In this work, <i>Rhodococcus qingshengii</i> RC1 and <i>Rhodococcus erythropolis</i> RC9 were isolated from a bacterial community growing in a biofilm reactor acclimated with microbiota from carbendazim-contaminated soil. Sequencing analysis of genomes of both strains revealed the presence of <i>cbm</i>A, the gene coding for the enzyme that hydrolyses carbendazim to produce 2-aminobenzimidazole (2-AB). The alternative gene for the first catabolic step (<i>mhe</i>I) was detected by PCR in strain RC9 but not in RC1. Metabolomic analysis by HPLC and LC-MS showed that both strains have the ability to metabolize carbendazim. <i>R. qingshengii</i> RC1 converts carbendazim to 2-AB, the first degradation intermediary, while <i>R. erythropolis</i> RC9 metabolizes the fungicide to its mineralization, probably because <i>R. qingshengii</i> RC1 lacks the <i>hdx</i> gene coding for 2-AB hydroxylase. HRESIMS-MS/MS results indicate that <i>R. erythropolis</i> RC9 metabolizes carbendazim by cleavage of the benzene ring and subsequent formation of 5-formyl-2-hydroxy-4,5-dihydro-1H-imidazole-4-carboxylic acid (X2 C<sub>5</sub>H<sub>6</sub>N<sub>2</sub>O<sub>4</sub>). The presence of carbendazim metabolites in culture supernatants of strains RC9 and RC1 suggests that both strains contribute to the efficient degradation of carbendazim in nature.
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spelling doaj-art-6ff0ef88ff264d6886b0fadf268d61e92025-01-24T13:42:24ZengMDPI AGMicroorganisms2076-26072024-12-011314010.3390/microorganisms13010040Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim DegradationRoosivelt Solano-Rodríguez0Fortunata Santoyo-Tepole1Mario Figueroa2Voleta Larios-Serrato3Nora Ruiz-Ordaz4Abigail Pérez-Valdespino5Everardo Curiel-Quesada6Departamento de Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala S/N, Col. Santo Tomás, Mexico City 11340, MexicoDepartamento de Investigación, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala S/N, Col. Santo Tomás, Mexico City 11340, MexicoDepartamento de Farmacia, Facultad de Química, Universidad Nacional Autónoma de México, Mexico City 04510, MexicoDepartamento de Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala S/N, Col. Santo Tomás, Mexico City 11340, MexicoDepartamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Av. Wilfrido Massieu, Unidad Adolfo López Mateos, Mexico City 07738, MexicoDepartamento de Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala S/N, Col. Santo Tomás, Mexico City 11340, MexicoDepartamento de Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala S/N, Col. Santo Tomás, Mexico City 11340, MexicoCarbendazim (CBZ) is a fungicide widely used on different crops, including soybeans, cereals, cotton, tobacco, peanuts, and sugar beet. Excessive use of this xenobiotic causes environmental deterioration and affects human health. Microbial metabolism is one of the most efficient ways of carbendazim elimination. In this work, <i>Rhodococcus qingshengii</i> RC1 and <i>Rhodococcus erythropolis</i> RC9 were isolated from a bacterial community growing in a biofilm reactor acclimated with microbiota from carbendazim-contaminated soil. Sequencing analysis of genomes of both strains revealed the presence of <i>cbm</i>A, the gene coding for the enzyme that hydrolyses carbendazim to produce 2-aminobenzimidazole (2-AB). The alternative gene for the first catabolic step (<i>mhe</i>I) was detected by PCR in strain RC9 but not in RC1. Metabolomic analysis by HPLC and LC-MS showed that both strains have the ability to metabolize carbendazim. <i>R. qingshengii</i> RC1 converts carbendazim to 2-AB, the first degradation intermediary, while <i>R. erythropolis</i> RC9 metabolizes the fungicide to its mineralization, probably because <i>R. qingshengii</i> RC1 lacks the <i>hdx</i> gene coding for 2-AB hydroxylase. HRESIMS-MS/MS results indicate that <i>R. erythropolis</i> RC9 metabolizes carbendazim by cleavage of the benzene ring and subsequent formation of 5-formyl-2-hydroxy-4,5-dihydro-1H-imidazole-4-carboxylic acid (X2 C<sub>5</sub>H<sub>6</sub>N<sub>2</sub>O<sub>4</sub>). The presence of carbendazim metabolites in culture supernatants of strains RC9 and RC1 suggests that both strains contribute to the efficient degradation of carbendazim in nature.https://www.mdpi.com/2076-2607/13/1/40carbendazimbiodegradation<i>Rhodococcus</i> spp.microbial cooperation
spellingShingle Roosivelt Solano-Rodríguez
Fortunata Santoyo-Tepole
Mario Figueroa
Voleta Larios-Serrato
Nora Ruiz-Ordaz
Abigail Pérez-Valdespino
Everardo Curiel-Quesada
Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim Degradation
Microorganisms
carbendazim
biodegradation
<i>Rhodococcus</i> spp.
microbial cooperation
title Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim Degradation
title_full Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim Degradation
title_fullStr Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim Degradation
title_full_unstemmed Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim Degradation
title_short Cooperation Between <i>Rhodococcus qinshengii</i> and <i>Rhodococcus erythropolis</i> for Carbendazim Degradation
title_sort cooperation between i rhodococcus qinshengii i and i rhodococcus erythropolis i for carbendazim degradation
topic carbendazim
biodegradation
<i>Rhodococcus</i> spp.
microbial cooperation
url https://www.mdpi.com/2076-2607/13/1/40
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