Longstanding industrial deposits of 1-chloro-4-[2,2,2-trichloro-1-(4-chlorophenyl)ethyl]benzene (DDT) impose environmental threat in Salamanca city, located in central Mexico. Native bacteria from this location were isolated and identified, and their potential utility for DDT biodegradation was examined. Twenty-five isolates were obtained, and cell lysates were analyzed by matrix-assisted laser desorption/ionization-time of flight mass spectrometry (MALDI-TOF MS) with BiotyperTR; twenty-one organisms were identified at species level, and the other four were assigned to genus. The most abundant species corresponded to Bacillus (44%) and Pseudomonas genera (20%). Eight bacteria could grow in the presence of 200 mg/L of DDT. Two-week exposure of Lysinibacillus fusiformis, Bacillus mycoides, Bacillus pumilus, and Bacillus cereus to DDT 50 mg/L and 200 mg/L, caused percentage pesticide degradation in the range 41-48% and 26-31%, respectively. Other four bacteria presented lower degradation rates. Gas chromatography-mass spectrometry (GC-MS) analysis of the spent media revealed that eight isolates assisted the conversion of DDT, DDD (1,1-dichloro-2,2-bis-(4-chlorophenyl)ethane), and DDE (1,1-dichloro-2,2-bis-(4-chlorophenyl)ethylene) to DDMU (1,1-(2-chloro-1,1-ethenediyl)-bis-(4-chlorobenzene)); however, DDNU (2,2-bis(4-chlorophenyl)ethylene), DBP (4,4'-dichlorobenzophenone(bis(4-chlorophenyl)methanone)) and DBH (bis(4-chlorophenyl)methanol) were found only for L. fusiformis, B. mycoides, B. cereus, B. marisflavi, and B. megaterium. Within the context of DDT biodegradation, the first three were the most promising isolates and further studies will be aimed at setting the experimental conditions for efficient mineralization of DDT congeners.

Chemistry Department Division of Natural and Exact Sciences University of Guanajuato L de Retana 5 36000 Guanajuato Mexico

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Ahmad KS (2020) Remedial potential of bacterial and fungal strains (Bacillus subtilis, Aspergillus niger, Aspergillus flavus and Penicillium chrysogenum) against organochlorine insecticide Endosulfan. Folia Microbiol https://doi.org/10.1007/s12223-020-00792-7

Aislabie JM, Richards NK, Boul HL (1997) Microbial degradation of DDT and its residues—a review. New Zealand J Agric Res 40(2):269–282

Avanzi IR, Gracioso LH, Baltazar MDGP, Karolski B, Perpetuo EA, do Nascimento CAO (2017) Rapid bacteria identification from environmental mining samples using MALDI-TOF MS analysis. Environ Sci Pollut Res 24:3717–3726

Betancur-Corredor B, Pino NJ, Cardona S, Peñuela GA (2015) Evaluation of biostimulation and Tween 80 addition for the bioremediation of long-term DDT-contaminated soil. J Environ Sci 28:101–109

Biesta-Peters EG, Reij MW, Joosten H, Gorris LG, Zwietering MH (2010) Comparison of two optical-density-based methods and a plate count method for estimation of growth parameters of Bacillus cereus. Appl Environ Microbiol 76:1399–1405 PubMed PMC

Cao F, Liu TX, Wu CY, Li FB, Li XM, Yu HY, Chen MJ (2012) Enhanced biotransformation of DDTs by an iron-and humic-reducing bacteria Aeromonas hydrophila HS01 upon addition of goethite and anthraquinone-2, 6-disulphonic disodium salt (AQDS). J Agric Food Chem 60:11238–11244 PubMed

Eganhouse RP, DiFilippo EL (2015) Determination of 1-chloro-4-[2, 2, 2-trichloro-1-(4-chlorophenyl) ethyl] benzene and related compounds in marine pore water by automated thermal desorption-gas chromatography/mass spectrometry using disposable optical fiber. J Chromatogr A 1415:38–47 PubMed

Eggen T, Majherczyk A (2006) Effects of zero-valent iron (Fe0) and temperature on the transformation of DDT and its metabolites in lake sediment. Chemosphere 62:1116–1125 PubMed

Fang H, Dong B, Yan H, Tang F, Yu Y (2010) Characterization of a bacterial strain capable of degrading DDT congeners and its use in bioremediation of contaminated soil. J Hazard Mater 184:281–289 PubMed

Focht DD, Alexander M (1970) Aerobic cometabolism of DDT analogues by Hydrogenomonas sp. Science 170:91–92 PubMed

Foght J, April T, Biggar K, Aislabie J (2001) Bioremediation of DDT-contaminated soils: a review. Biorernediation J 5:225–246

Grewal NJ, Bhattacharya A, Kumar S, Singh DK, Khare SK (2016) Biodegradation of 1, 1, 1-trichloro-2, 2-bis (4-chlorophenyl) ethane (DDT) by using Serratia marcescens NCIM 2919. J Environ Sci Health - Part B 51:809–816

Hay AG, Focht DD (1998) Cometabolism of 1,1-dichloro-2,2-bis(4-chlorophenyl)ethylene by Pseudomonas acidovorans M3GY grown on biphenyl. Appl Environ Microbiol 64:2141–2146 PubMed PMC

Hay AG, Focht DD (2000) Transformation of 1,1-dichloro-2,2-(4-chlorophenyl)ethane (DDD) by Ralstonia eutropha strain A5 FEMS. Microbiol Ecol 31:249–253

Huang H, Zhang Y, Chen W, Yuen DA, Ding Y, Chen Y, Mao Y, Qi S (2018) Sources and transformation pathways for dichlorodiphenyltrichloroethane (DDT) and metabolites in soils from Northwest Fujian, China. Environ Pollut 235:560–570 PubMed

ICH (2012) Harmonized Tripartite Guideline. Validation of analytical procedures: text and methodology (Q2/R1). hhtp://wwwish org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Quality/Q2_R1/Step4/Q2_R1_Guidelinepdf

Kamanavalli CM, Ninnekar HZ (2004) Biodegradation of DDT by a Pseudomonas species. Curr Microbiol 48:10–13 PubMed

Kantachote D, Singleton I, McClure N, Naidu R, Megharaj M, Harch BD (2003) DDT resistance and transformation by different microbial strains isolated from DDT-contaminated soils and compost materials. Compost Sci Util 11:300–310

Kopcakova A, Stramova Z, Kvasnova S, Godany A, Perhacova Z, Pristas P (2014) Need for database extension for reliable identification of bacteria from extreme environments using MALDI TOF mass spectrometry. Chem Papers 68:1435–1442

Kostrzewa M (2018) Application of the MALDI Biotyper to clinical microbiology: progress and potential. Expert Rev Proteomics 15:193–202 PubMed

Kuhad RC,  Johri AK,  Singh A,  Ward OP (2004) Bioremediation of pesticide-contaminated soils A Singh OP Ward Eds Applied Bioremediation and Phytoremediation 1. Springer Berlin 35-54

Liang Q, Lei M, Chen T, Yang J, Wan X, Yang S (2014) Application of sewage sludge and intermittent aeration strategy to the bioremediation of DDT-and HCH-contaminated soil. J Environ Sci 26:1673–1680

López-Carrillo L, Torres-Arreola L, Torres-Sánchez L, Espinosa-Torres F, Jiménez C, Cebrián M, Waliszewski S, Saldate O (1996) Is DDT use a public health problem in Mexico? Environ Health Perspect 104:584–588 PubMed PMC

Lovecka P, Pacovska I, Stursa P, Vrchotova B, Kochankova L, Demnerova K (2015) Organochlorinated pesticide degrading microorganisms isolated from contaminated soil. New Biotechnol 32:26–31

Maier T,  Klepel S,  Renner U,  Kostrzewa M (2006) Fast and reliable MALDI-TOF MS-based microorganism identification. Nat Methods 3:328

Mansouri A, Cregut M, Abbes C, Durand MJ, Landoulsi A, Thouand G (2017) The environmental issues of DDT pollution and bioremediation: a multidisciplinary review. Appl Biochem Biotechnol 181:309–339 PubMed

Mellmann A, Cloud J, Maier T, Keckevoet U, Ramminger I, Iwen P, Dunn J, Hall G, Wilson D, LaSala P, Kostrzewa M, Harmsen D (2008) Evaluation of matrix-assisted laser desorption ionization-time-of-flight mass spectrometry in comparison to 16S rRNA gene sequencing for species identification of nonfermenting bacteria. J Clin Microbiol 46:1946–1954 PubMed PMC

Mwangi K, Boga HI, Muigai AW, Kiiyukia C, Tsanuo MK (2010) Degradation of dichlorodiphenyltrichloroethane (DDT) by bacterial isolates from cultivated and uncultivated soil. Afr J Microbiol Res 4:185–196

Nagy E, Becker S, Kostrzewa M, Barta N, Urbán E (2012) The value of MALDI-TOF MS for the identification of clinically relevant anaerobic bacteria in routine laboratories. J Med Microbiol 61:1393–1400 PubMed

Odukkathil G, Vasudevan N (2015) Biodegradation of endosulfan isomers and its metabolite endosulfate by two biosurfactant producing bacterial strains of Bordetella petrii. J Environ Sci Health - Part B 50:81–89

Ortíz I, Velasco A, Le Borgne S, Revah S (2013) Biodegradation of DDT by stimulation of indigenous microbial populations in soil with cosubstrates. Biodegradation 24:215–225 PubMed

Pan X, Lin D, Zheng Y, Zhang Q,  Yin Y,  Cai X, Fang H, Yu Y (2016) Biodegradation of DDT by Stenotrophomonas sp. DDT-1: characterization and genome functional analysis. Sci Reports 6:21332

Patowary K,  Patowary R ,Kalita MC, Deka S (2016) Development of an efficient bacterial consortium for the potential remediation of hydrocarbons from contaminated sites. Front Microbiol 7:1092

Purnomo AS, Mori T, Kamei I, Kondo R (2011) Basic studies and applications on bioremediation of DDT: a review. Int Biodeter Biodegr 65:921–930

Qu J, Xu Y, Ai GM, Liu Y, Liu ZP (2015) Novel Chryseobacterium sp. PYR2 degrades various organochlorine pesticides (OCPs) and achieves enhancing removal and complete degradation of DDT in highly contaminated soil. J Environ Management 161:350–357

Ryzhov V, Fenselau C (2001) Characterization of the protein subset desorbed by MALDI from whole bacterial cells. Anal Chem 73:746–750 PubMed

Sandrin TR, Goldstein JE, Schumaker S (2013) MALDI TOF MS profiling of bacteria at the strain level: a review. Mass Spectrom Rev 32:188–217 PubMed

Sari SA, Tachibana S, Kazutaka I (2012) Determination of co-metabolism for 1,1,1-trichloro-2,2-bis(4-chlorophenyl) ethane (DDT) degradation with enzymes from Trametes versicolor U97. J Biosci Bioeng 114:176–181 PubMed

Sariwati A, Purnomo AS, Kamei I (2017) Abilities of co-cultures of brown-rot fungus Fomitopsis pinicola and Bacillus subtilis on biodegradation of DDT. Curr Microbiol 74:1068–1075 PubMed

Sauget M, Valot B, Bertrand X, Hocquet D (2017) Can MALDI-TOF mass spectrometry reasonably type bacteria? Trends Microbiol 25:447–455 PubMed

Sharma SK, Sadasivam KV, Dave JM (1987) DDT degradation by bacteria from activated sludge. Environ Int 13:183–190

Silva-Jiménez H, Araujo-Palomares CL, Macías-Zamora JV, Ramírez-Álvarez N, García-Lara B, Corrales-Escobosa AR (2018) Identification by MALDI-TOF MS of environmental bacteria with high potential to degrade pyrene. J Mex Chem Soc 62:214–225

Sudharshan S, Naidu R, Mallavarapu M, Bolan N (2012) DDT remediation in contaminated soils: a review of recent studies. Biodegradation 22:851–863

Timperio AM, Gorrasi S,  Zolla L,  Fenice M (2017) Evaluation of MALDI-TOF mass spectrometry and MALDI BioTyper in comparison to 16S rDNA sequencing for the identification of bacteria isolated from Arctic sea water. PLoS One 12:e0181860

Topić N, Popović SP, Kazazić I, Strunjak-Perović R, Čož-Rakovac (2017) Differentiation of environmental aquatic bacterial isolates by MALDI-TOF MS. Environ Res 152:7–16

Trejo-Acevedo A, Díaz-Barriga F, Carrizales L, Domínguez G, Costilla R, Ize-Lema I, Pérez-Maldonado IN (2009) Exposure assessment of persistent organic pollutants and metals in Mexican children. Chemosphere 74:974–980 PubMed

US EPA Method D (2018) Determinative chromatographic separations. https://www.epa.gov/sites/production/files/2015-12/documents/8000d.pdf

Velasco A, Aburto-Medina A, Shahsavari E, Revah S, Ortiz I (2017) Degradation mechanisms of DDX induced by the addition of toluene and glycerol as cosubstrates in a zero-valent iron pretreated soil. J Hazard Mater 321:681–689 PubMed

Wang B, Liu W, Liu X, Franks AE, Teng Y, Luo Y (2017) Comparative analysis of microbial communities during enrichment and isolation of DDT-degrading bacteria by culture-dependent and-independent methods. Sci Tot Environ 590:297–303

Wang GL, Bi M, Liang B, Jiang JD, Li SP (2011) Pseudoxanthomonas jiangsuensis sp. Nov., a DDT-degrading bacterium isolated from a long-term DDT-polluted soil. Curr Microbiol 62:1760–1766 PubMed

Wetterauer B, Ricking M, Otte JC, Hallare AV, Rastall A, Erdinger L, Schwarzbauer J, Braunbeck T, Hollert H (2012) Toxicity, dioxin-like activities, and endocrine effects of DDT metabolites—DDA, DDMU, DDMS, and DDCN. Environ Sci Pollut Res 19:403–415

Xiao P, Mori T, Kamei I, Kondo R (2011) A novel metabolic pathway for biodegradation of DDT by the white rot fungi, Phlebia lindtneri and Phlebia brevispora. Biodegradation 22:859–867 PubMed

Xie H, Zhu L, Xu Q, Wang J, Liu W, Jiang J, Meng YX (2011) Isolation and degradation ability of the DDT-degrading bacterial strain KK. Environ Earth Sci 62:93–99