{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,13]],"date-time":"2026-09-13T03:13:21Z","timestamp":1789269201098,"version":"build-2803163510"},"reference-count":43,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2024,12,29]],"date-time":"2024-12-29T00:00:00Z","timestamp":1735430400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Secretaria de Investigaci\u00f3n y Posgrado del Instituto Polit\u00e9cnico Nacional","award":["20211300"],"award-info":[{"award-number":["20211300"]}]},{"name":"Secretaria de Investigaci\u00f3n y Posgrado del Instituto Polit\u00e9cnico Nacional","award":["20220895"],"award-info":[{"award-number":["20220895"]}]},{"name":"Secretaria de Investigaci\u00f3n y Posgrado del Instituto Polit\u00e9cnico Nacional","award":["20231290"],"award-info":[{"award-number":["20231290"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>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, Rhodococcus qingshengii RC1 and Rhodococcus erythropolis 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 cbmA, the gene coding for the enzyme that hydrolyses carbendazim to produce 2-aminobenzimidazole (2-AB). The alternative gene for the first catabolic step (mheI) 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. R. qingshengii RC1 converts carbendazim to 2-AB, the first degradation intermediary, while R. erythropolis RC9 metabolizes the fungicide to its mineralization, probably because R. qingshengii RC1 lacks the hdx gene coding for 2-AB hydroxylase. HRESIMS-MS\/MS results indicate that R. erythropolis 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 C5H6N2O4). 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.<\/jats:p>","DOI":"10.3390\/microorganisms13010040","type":"journal-article","created":{"date-parts":[[2024,12,31]],"date-time":"2024-12-31T13:26:25Z","timestamp":1735651585000},"page":"40","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Cooperation Between Rhodococcus qinshengii and Rhodococcus erythropolis for Carbendazim Degradation"],"prefix":"10.3390","volume":"13","author":[{"given":"Roosivelt","family":"Solano-Rodr\u00edguez","sequence":"first","affiliation":[{"name":"Departamento de Bioqu\u00edmica, Escuela Nacional de Ciencias Biol\u00f3gicas, Instituto Polit\u00e9cnico Nacional, Prolongaci\u00f3n de Carpio y Plan de Ayala S\/N, Col. Santo Tom\u00e1s, Mexico City 11340, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fortunata","family":"Santoyo-Tepole","sequence":"additional","affiliation":[{"name":"Departamento de Investigaci\u00f3n, Escuela Nacional de Ciencias Biol\u00f3gicas, Instituto Polit\u00e9cnico Nacional, Prolongaci\u00f3n de Carpio y Plan de Ayala S\/N, Col. Santo Tom\u00e1s, Mexico City 11340, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7004-0591","authenticated-orcid":false,"given":"Mario","family":"Figueroa","sequence":"additional","affiliation":[{"name":"Departamento de Farmacia, Facultad de Qu\u00edmica, Universidad Nacional Aut\u00f3noma de M\u00e9xico, Mexico City 04510, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0052-4376","authenticated-orcid":false,"given":"Voleta","family":"Larios-Serrato","sequence":"additional","affiliation":[{"name":"Departamento de Bioqu\u00edmica, Escuela Nacional de Ciencias Biol\u00f3gicas, Instituto Polit\u00e9cnico Nacional, Prolongaci\u00f3n de Carpio y Plan de Ayala S\/N, Col. Santo Tom\u00e1s, Mexico City 11340, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nora","family":"Ruiz-Ordaz","sequence":"additional","affiliation":[{"name":"Departamento de Ingenier\u00eda Bioqu\u00edmica, Escuela Nacional de Ciencias Biol\u00f3gicas, Instituto Polit\u00e9cnico Nacional, Av. Wilfrido Massieu, Unidad Adolfo L\u00f3pez Mateos, Mexico City 07738, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2885-592X","authenticated-orcid":false,"given":"Abigail","family":"P\u00e9rez-Valdespino","sequence":"additional","affiliation":[{"name":"Departamento de Bioqu\u00edmica, Escuela Nacional de Ciencias Biol\u00f3gicas, Instituto Polit\u00e9cnico Nacional, Prolongaci\u00f3n de Carpio y Plan de Ayala S\/N, Col. Santo Tom\u00e1s, Mexico City 11340, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9508-5518","authenticated-orcid":false,"given":"Everardo","family":"Curiel-Quesada","sequence":"additional","affiliation":[{"name":"Departamento de Bioqu\u00edmica, Escuela Nacional de Ciencias Biol\u00f3gicas, Instituto Polit\u00e9cnico Nacional, Prolongaci\u00f3n de Carpio y Plan de Ayala S\/N, Col. Santo Tom\u00e1s, Mexico City 11340, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,12,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Singh, R., Singh, P., Tripathi, S., Chandra, K.K., and Bhadouria, R. (2023). The Effects of Xenobiotics on Soil and Human Health. Xenobiotics in Urban Ecosystems, Springer International Publishing.","DOI":"10.1007\/978-3-031-35775-6"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"126384","DOI":"10.1016\/j.jhazmat.2021.126384","article-title":"Mechanistic Insights into the Success of Xenobiotic Degraders Resolved from Metagenomes of Microbial Enrichment Cultures","volume":"418","author":"Li","year":"2021","journal-title":"J. Hazard. Mater."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1126\/science.aat1168","article-title":"Emergent Simplicity in Microbial Community Assembly","volume":"361","author":"Goldford","year":"2018","journal-title":"Science"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2085","DOI":"10.1038\/ismej.2016.22","article-title":"Beyond the Black Queen Hypothesis","volume":"10","author":"Mas","year":"2016","journal-title":"ISME J."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e00036-12","DOI":"10.1128\/mBio.00036-12","article-title":"The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss","volume":"3","author":"Morris","year":"2012","journal-title":"mBio"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Agrios, G.N. (2005). Control of plant diseases. Plant Pathology, Elsevier.","DOI":"10.1016\/B978-0-08-047378-9.50015-4"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Singh, S., Kumar, V., Singh, S., and Singh, J. (2019). Influence of Humic Acid, Iron and Copper on Microbial Degradation of Fungicide Carbendazim. Biocatal. Agric. Biotechnol., 20.","DOI":"10.1016\/j.bcab.2019.101196"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"137723","DOI":"10.1016\/j.chemosphere.2022.137723","article-title":"Carbendazim: Ecological Risks, Toxicities, Degradation Pathways and Potential Risks to Human Health","volume":"314","author":"Zhou","year":"2023","journal-title":"Chemosphere"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"S16","DOI":"10.1016\/j.chemosphere.2014.03.049","article-title":"Commercially Available Chemicals as Immunizing Haptens for the Development of a Polyclonal Antibody Recognizing Carbendazim and Other Benzimidazole-Type Fungicides","volume":"119","author":"Zikos","year":"2015","journal-title":"Chemosphere"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2047","DOI":"10.1099\/ijs.0.057935-0","article-title":"Nocardioides soli sp. Nov., a Carbendazim-Degrading Bacterium Isolated from Soil under the Long-Term Application of Carbendazim","volume":"64","author":"Sun","year":"2014","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1016\/j.scitotenv.2017.03.025","article-title":"Rhamnolipid-Aided Biodegradation of Carbendazim by Rhodococcus Sp. D-1: Characteristics, Products, and Phytotoxicity","volume":"590\u2013591","author":"Bai","year":"2017","journal-title":"Sci. Total Environ."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Zhang, X., Huang, Y., Harvey, P.R., Li, H., Ren, Y., Li, J., Wang, J., and Yang, H. (2013). Isolation and Characterization of Carbendazim-Degrading Rhodococcus erythropolis Djl-11. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0074810"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1016\/j.chemosphere.2010.08.040","article-title":"Biodegradation of Carbendazim by a Novel Actinobacterium Rhodococcus jialingiae Djl-6-2","volume":"81","author":"Wang","year":"2010","journal-title":"Chemosphere"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1353\/bae.2018.0010","article-title":"Biodegradation of Carbendazim by Rhodococcus erythropolis and Its Plant Growth-Promoting Traits","volume":"118B","author":"Abraham","year":"2018","journal-title":"Biol. Environ."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.jhazmat.2017.02.007","article-title":"Identification of the Key Amino Acid Sites of the Carbendazim Hydrolase (MheI) from a Novel Carbendazim-Degrading Strain Mycobacterium sp. SD-4","volume":"331","author":"Zhang","year":"2017","journal-title":"J. Hazard. Mater."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2940","DOI":"10.1128\/AEM.02990-09","article-title":"Cloning and Biochemical Characterization of a Novel Carbendazim (Methyl-1H-Benzimidazol-2-Ylcarbamate)-Hydrolyzing Esterase from the Newly Isolated Nocardioides Sp. Strain SG-4G and Its Potential for Use in Enzymatic Bioremediation","volume":"76","author":"Pandey","year":"2010","journal-title":"Appl. Environ. Microbiol"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4803","DOI":"10.1111\/1462-2920.16139","article-title":"Functional Analysis, Diversity, and Distribution of Carbendazim Hydrolases MheI and CbmA, Responsible for the Initial Step in Carbendazim Degradation","volume":"24","author":"Zhang","year":"2022","journal-title":"Environ. Microbiol."},{"key":"ref_18","first-page":"939","article-title":"Isolation and Characterization of Pseudomonas sp","volume":"21","author":"Fang","year":"2010","journal-title":"CBW Capab. Degrad. Carbendazim. Biodegrad."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"142137","DOI":"10.1016\/j.scitotenv.2020.142137","article-title":"Characterization of a Novel Carbendazim-Degrading Strain Rhodococcus sp. CX-1 Revealed by Genome and Transcriptome Analyses","volume":"754","author":"Long","year":"2021","journal-title":"Sci. Total Environ."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1016\/j.mimet.2003.08.009","article-title":"Review and Re-Analysis of Domain-Specific 16S Primers","volume":"55","author":"Baker","year":"2003","journal-title":"J. Microbiol. Methods"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1118","DOI":"10.1002\/ps.739","article-title":"Rapid Mineralisation of the Herbicide Isoproturon in Soil from a Previously Treated Danish Agricultural Field","volume":"59","author":"Aamand","year":"2003","journal-title":"Pest Manag. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3137","DOI":"10.1093\/bioinformatics\/btx373","article-title":"FQC Dashboard: Integrates FastQC Results into a Web-Based, Interactive, and Extensible FASTQ Quality Control Tool","volume":"33","author":"Brown","year":"2017","journal-title":"Bioinformatics"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A Flexible Trimmer for Illumina Sequence Data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Prjibelski, A., Antipov, D., Meleshko, D., Lapidus, A., and Korobeynikov, A. (2020). Using SPAdes De Novo Assembler. Curr. Protoc. Bioinform., 70.","DOI":"10.1002\/cpbi.102"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1093\/bioinformatics\/btt086","article-title":"QUAST: Quality Assessment Tool for Genome Assemblies","volume":"29","author":"Gurevich","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1394","DOI":"10.1101\/gr.2289704","article-title":"Mauve: Multiple Alignment of Conserved Genomic Sequence with Rearrangements","volume":"14","author":"Darling","year":"2004","journal-title":"Genome Res."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., Formsma, K., Gerdes, S., Glass, E.M., and Kubal, M. (2008). The RAST Server: Rapid Annotations Using Subsystems Technology. BMC Genom., 9.","DOI":"10.1186\/1471-2164-9-75"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"W484","DOI":"10.1093\/nar\/gkad326","article-title":"Proksee: In-Depth Characterization and Visualization of Bacterial Genomes","volume":"51","author":"Grant","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1089\/10665270050081478","article-title":"A Greedy Algorithm for Aligning DNA Sequences","volume":"7","author":"Zhang","year":"2000","journal-title":"J. Comput. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"5101","DOI":"10.1111\/j.1742-4658.2005.04945.x","article-title":"Protein Database Searches Using Compositionally Adjusted Substitution Matrices","volume":"272","author":"Altschul","year":"2005","journal-title":"FEBS J."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Mu\u00f1oz-Ram\u00edrez, Z.Y., Mendez-Tenorio, A., Kato, I., Bravo, M.M., Rizzato, C., Thorell, K., Torres, R., Aviles-Jimenez, F., Camorlinga, M., and Canzian, F. (2017). Whole Genome Sequence and Phylogenetic Analysis Show Helicobacter pylori Strains from Latin America Have Followed a Unique Evolution Pathway. Front. Cell. Infect. Microbiol., 7.","DOI":"10.3389\/fcimb.2017.00050"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2731","DOI":"10.1093\/molbev\/msr121","article-title":"MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods","volume":"28","author":"Tamura","year":"2011","journal-title":"Mol. Biol. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Telles, G.P., Ara\u00fajo, G.S., Walter, M.E.M.T., Brigido, M.M., and Almeida, N.F. (2018). Live Neighbor-Joining. BMC Bioinform., 19.","DOI":"10.1186\/s12859-018-2162-x"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"117","DOI":"10.4056\/sigs.531120","article-title":"Digital DNA-DNA Hybridization for Microbial Species Delineation by Means of Genome-to-Genome Sequence Comparison","volume":"2","author":"Auch","year":"2010","journal-title":"Stand. Genom. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1007\/s10482-017-0844-4","article-title":"A Large-Scale Evaluation of Algorithms to Calculate Average Nucleotide Identity","volume":"110","author":"Yoon","year":"2017","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.jgg.2015.04.004","article-title":"Pyrimidine Metabolism: Dynamic and Versatile Pathways in Pathogens and Cellular Development","volume":"42","author":"Garavito","year":"2015","journal-title":"J. Genet. Genom."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e0018","DOI":"10.1199\/tab.0018","article-title":"Purine and Pyrimidine Nucleotide Synthesis and Metabolism","volume":"1","author":"Moffatt","year":"2002","journal-title":"Arab. Book"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1007\/s00449-016-1717-3","article-title":"Kinetics of Carbendazim Degradation in a Horizontal Tubular Biofilm Reactor","volume":"40","year":"2017","journal-title":"Bioprocess Biosyst. Eng."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"De Carvalho, C.C.C.R., Costa, S.S., Fernandes, P., Couto, I., and Viveiros, M. (2014). Membrane Transport Systems and the Biodegradation Potential and Pathogenicity of Genus Rhodococcus. Front. Physiol., 5.","DOI":"10.3389\/fphys.2014.00133"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1134\/S0026261723604062","article-title":"Rhodococcus qingshengii GlMm1 as the Basis for a Biosensor for Determination of the Fungicide Carbendazim","volume":"93","author":"Kuvichkina","year":"2024","journal-title":"Microbiology"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Ivshina, I., Bazhutin, G., and Tyumina, E. (2022). Rhodococcus strains as a Good Biotool for Neutralizing Pharmaceutical Pollutants and Obtaining Therapeutically Valuable Products: Through the Past into the Future. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.967127"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"P\u00e1tek, M., Grulich, M., and Ne\u0161vera, J. (2021). Stress Response in Rhodococcus strains. Biotechnol. Adv., 53.","DOI":"10.1016\/j.biotechadv.2021.107698"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/1\/40\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:56:00Z","timestamp":1760115360000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/1\/40"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,29]]},"references-count":43,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1]]}},"alternative-id":["microorganisms13010040"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13010040","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,29]]}}}