TY - JOUR
AU - Ramos Monroy, O
AB - Abstract By decolorization of azo dyes, caused by reductive cleavage of the azo linkage, toxic or recalcitrant amines are generated. The present study deals with the effect of the inflowing medium composition (C:N ratio) on the kinetic behavior of a bacterial biofilm-forming consortium, able to use as carbon, nitrogen and sulfur source, the molecule of 4-aminonaphthalene-1-sulfonic acid (4ANS), which is one of the most recalcitrant byproducts generated by decolorization of azo dyes. All the experiments were carried out at room temperature in a lab-scale packed-bed biofilm reactor. Because environmental conditions affect the bioreactor performance, two mineral salts media containing 4ANS, with distinct C:N ratios; 0.68 (carbon as the limiting nutrient) and 8.57 (nitrogen as the limiting nutrient) were used to evaluate their effect on 4ANS biodegradation. By HPLC and COD measurements, the 4ANS removal rates and removal efficiencies were determined. The cultivable bacterial strains that compose the consortium were identified by their 16S rDNA gene sequence. With the enrichment technique used, a microbial consortium able to use efficiently 4ANS as the sole carbon source and energy, nitrogen and sulfur, was selected. The bacterial strains that constitute the consortium were isolated and identified. They belong to the following genera: Bacillus, Arthrobacter, Microbacterium, Nocardioides, and Oleomonas. The results obtained with this consortium showed, under nitrogen limitation, a remarkable increase in the 4ANS removal efficiency ηANS, and in the 4ANS volumetric removal rates R V,4ANS, as compared to those obtained under carbon limitation. Differences observed in bioreactor performance after changing the nutrient limitation could be caused by changes in biofilm properties and structure. Introduction Aromatic amines are major industrial chemicals used to produce detergents, dispersing and wetting agents, synthetic dyes, and pharmaceuticals [39, 58]. Degradation of azo dyes is also an important generation source of these compounds. By reductive cleavage of the azo bond, aromatic amines are formed. Many of them have been reported as carcinogens and mutagens [7]; therefore, their removal from contaminated sources is of health and environmental concern. A group of these aromatic amines represented by aryl sulfonates (AS), aminobenzene (ABS), and amino naphthyl sulfonates (ANS). 4-aminonaphthalene-1-sulfonic acid (4ANS, 1-naphthylamine-4-sulfonic acid or naphthionic acid) is used as a diazo component in many azo dyes, e.g., Food Red 3, Food Red 7, Food Red 9, Acid Red 3, Acid Red 18, Acid Red 25, Acid Red 27, Acid Red 88, Fast Sulphon Black F (1-hydroxy-8-(2-hydroxy-1-naphthylazo)-2-(4-sulfo-1-naphthylazo)-naphthalene-3,6-disulfonic acid), and DI-SNADNS (3,6-bis(4-sulfo-1-naphtylazo)-4,5-dihydroxy-2,7-naphtalenedisulfonic acid) [10]. These derivatives can pose a health hazard and some have been designated as priority pollutants. Most are toxic or inhibitory to biological activities; and therefore could present a severe problem in conventional wastewater treatment systems [55]. The presence of a sulfonic group enhances the water-solubility of naphtylamines; therefore, during production processes, sulfonated aromatic amines could easily reach the aquatic environment through industrial wastewaters. Sulfonated aromatic amines have been found in rivers of Italy, Germany, and Spain [15, 28, 33, 65, 66]; also in Mediterranean coastal water [17]. This means that these compounds are not efficiently removed in wastewater treatment plants (WTP). Once hazardous pollutants enter a WTP, some alternatives to remove them could be the bioaugmentation of WTP’s biota with specialized microorganisms able to degrade these compounds, or the implementation of subsequent treatment processes. In the first case, the environmental conditions prevailing in a WTP are generally hostile toward exogenous microorganisms, which must compete with the biota from the wastewater sludge; thus, bioaugmentation is not always an effective solution. Babcock et al. [4] summarize several cases of wastewater treatment processes, showing either successful or unsuccessful persistence of the inoculated microorganisms. In the second case, physicochemical or biological post-treatment processes could be used to remove naphthalene sulfonic acids or to increase their biodegradability [55]. However, the removal of diluted compounds using chemical, photochemical, or electrochemical oxidation techniques could be uneconomical [44, 49, 59], and the use of non-destructive removal procedures, such as adsorption by activated carbon, acid or basic resins, requires the disposal or reactivation of the saturated adsorbent [21]. An efficient and cheaper alternative to physicochemical processes could be the use of specialized microorganisms and simple biological processes to remove these compounds [35]; however, some problems exist. Several studies have shown the biodegradation recalcitrance and toxicity of this kind of xenobiotic compounds, and the main difficulties to find microorganisms able to use them as the sole source of carbon. Several authors report that the polar nature of aminoarylsulfonates makes these compounds recalcitrant to biotransformation and hardly used by microorganisms as a nutrient source, requiring for their biodegradation specialized aerobic microbial consortia [38, 56]. By example, Aeromonas sp., is unable to degrade 4ANS, accumulating it after decolorization of the dye Bordeaux S [19]. Mixed microorganisms from various environmental samples can degrade several aminobenbenzene sulfonic acids, but not amino naphthalene sulfonic acids [61]. Shewanella decolorantius S12 was unable to degrade 1-aminonaphthyl-4-sulfonic acid, either in anaerobic or aerobic conditions [20]. Other authors report that naphthalene sulfonates are partially degraded by certain bacteria and algae, using them as a source of sulfur. Similarly, Pseudomonas sp., an Arthrobacter sp. and an unidentified bacterium isolated from sewage, desulfonate at least 16 aromatic compounds, although none of them served as the carbon source [68]. On the other hand, a recent study has shown that immobilized or free cells of Alcaligenes latus degrade the amino hydroxy naphthalene disulfonic acid [63]; however, the culture medium should be complemented with relatively expensive nutrients such as glucose and yeast extract. The use of biofilm-forming microbial consortia, selected in response to the continuous availability of amino naphthalene sulfonic acids, could help to their rapid and complete degradation. By several reasons, the use of fixed-bed reactors containing a mixed microbial biofilm is appropriate to remove compounds toxic to cells; because the exopolymeric matrix acts as a diffusion barrier to the chemicals, or interacts with the toxic substances acting as an ion exchanger that sequesters charged substances [22]. The biofilm matrix could also inhibit washout of enzymes, nutrients, or even signaling molecules that could then accumulate locally and create favorable microenvironments within the biofilm [6]. Additionally, mixed-culture biofilms provide an ideal environment for microbial residents to coordinate metabolic activities and share genetic elements encoding beneficial traits with each other [30]. The retention of attached active bacteria provides biofilm reactors with several advantages over conventional suspended-growth reactors, including faster conversion rates due to higher concentrations of active biomass, reduced bacterial washout at high-dilution rates, enhanced reactor stability, and rapid response to varying or adverse operating conditions [9]. However, it is well known that bacterial cell composition and physiology are affected by the carbon/nitrogen ratio of the nutrient supply [12, 64] and that change in biofilm structure and properties are caused by nutrient limitation [3, 51]. Therefore, it is expected that a change in the limiting nutrient affects the performance of a biofilm removal process. For the previous reasons, the aim of this work is the selection of a biofilm-forming microbial consortium able to use 4-amino naphthalene1-sulfonic acid as its sole source of carbon, nitrogen, and sulfur, and study its biodegradation kinetics in a laboratory-scale packed-bed-biofilm column under carbon or nitrogen limitations. Methods Chemicals 4-aminonaphthalene-1-sulfonic acid (1-naphthylamine-4-sulfonic acid, naphthionic acid), 97 % purity, was purchased from Chem-Service, PA, USA. The solvents used for high-performance liquid chromatography (HPLC) were purchased from J. T. Baker, USA. Culture media Two different mineral salts media (MS) were used. To probe the 4-aminonaphthalene-1-sulfonic acid as the sole carbon and energy source, the MS1 medium, containing the following components, in mg l−1, was used CaCl2, 20; MgSO4·7H2O, 100; (NH4)2SO4, 100; and K2HPO4, 200. 4ANS was added to obtain a concentration of 50 mg l−1. The C/N and C/S proportions in MS1 were 0.68 and 0.29, respectively; thus, with this medium, the microbial growth was limited by the carbon source. To probe the 4-aminonaphthalene-1-sulfonic acid as the sole carbon, energy, nitrogen, and sulfur source, the MS2 medium was used. It contains the following components, in mg l−1: CaCl2, 20; MgCl2, 80; and K2HPO4, 200. The 4ANS was added to obtain a concentration of 50 mg l−1. This medium was formulated considering the C/N and C/S ratios of the 4ANS molecule (8.57 and 3.74, respectively). With MS2 medium, the microbial growth was limited by the nitrogen source. Selection of the microbial community able to grow on 4ANS Soil samples collected nearby a textile industry were inoculated in 250-ml flasks containing 50 ml of MS1 plus 4ANS as the sole source of carbon and energy. The flasks were incubated at 30 °C in a rotatory shaker for 48 h. The consumption of the 4ANS was spectrophotometrically estimated. Aliquots of the culture medium were transferred to flasks containing new mineral salts medium, and the procedure was repeated. After 12 successive transfers, a microbial community that uses the 4ANS as the carbon and energy source was obtained. This community was maintained on agar slants containing MS1 medium. Packed-bed column reactor All experiments were carried out at room temperature in a lab-scale packed-bed column reactor, which, at the bottom, has a sintered glass plate diffuser with pore diameter 40–100 μm (Heraeus Quarzglas GmbH & Co., Germany). The body of the glass column has lateral ports for liquid input and air/liquid outflow. It also has a glass cover with ports for inoculation, sampling, and air venting (Fig. 1). The supply of air to the bubbling column was kept constant at 0.67 l min−1. Air and liquid were concurrently supplied through the column, which was packed with small fragments of a porous volcanic stone named tezontle; material widely distributed in central Mexico. Fig. 1 Open in new tabDownload slide Packed-bed column reactor The particle volume was calculated and used to estimate the equivalent diameter d p of the volcanic stone particles considering porous fragments as ellipsoidal bodies, with three characteristic radii [16]. The average d p value was 7.4 ± 2.7 mm. The column was packed with 998 g of porous stone fragments. The liquid contained in the interparticle space corresponds to a circulating liquid volume, or drained volume, V L of 560 ml. With this value, the volumetric loading (B V,ANS = F C ANS-R /V L) and removal (R V,ANS = F(C ANS-R − C ANS-OUT)/V L) rates of 4ANS in the PBR operating in steady-state continuous regime were estimated. In these equations, F is the medium flow rate, C ANS-R and C ANS-OUT, are the concentrations of 4ANS entering or leaving the PBR. The corresponding volumetric loading and removal rates of the compound were also expressed in terms of the chemical oxygen demand (B V,COD, and R V,COD) entering or leaving the reactor. The general performance of the bioreactor was evaluated through these volumetric removal rates, and the biodegradation capabilities of the bacterial consortium were estimated through the values of removal efficiencies ηANS = R V,ANS /B V,ANS, ηCOD = R V,COD /B V,COD. Start-up of the bioreactor Before the continuous operation, the column was packed with the porous support, sterilized (121 °C for 30 min), and saturated with the 4ANS by supplying MS1 medium containing 50 mg l−1 of 4ANS. It was considered that the support was saturated when the 4ANS concentration of the outflowing medium, spectrophotometrically measured at λ238, was equal to that of the inflowing medium. The reactor was then inoculated with 25 ml of suspended cells of the selected bacterial consortium, previously cultivated in MS1 medium. The reactor was operated in batch mode for 48 h in aerobic conditions to allow the microbial colonization of the porous support. When operated in continuous regime, a constant flow of MS1 medium (carbon limited) was maintained until no change in 4ANS, COD, and TOC concentrations could be observed (about four hydraulic retention times HRT = V L/F). In this condition, it was considered that a steady-state was reached. Several flow rates of MS1 (16 to 400 ml h−1), corresponding to 4ANS loading rates B VANS ranging from 1.43 to 35.7 mg l−1 h−1, were probed. When a consistent decay in 4ANS removal efficiencies was evident, the medium was changed to MS2 medium (nitrogen limited). The new flow rates were varied from 30 to 825 ml h−1, with corresponding B VANS values ranging from 2.68 to 73.66 mg l−1 h−1. Analytical methods 4ANS determination Two methods were used. For a rapid estimation, the absorbance of the samples was measured at λ238 in a Beckman DU-620 spectrophotometer, and by HPLC, using a Shimadzu 10AT system with an UV detector. The column used was a Merck LiChrospher 100, C18 (250 mm × 4 mm i.d., particle size 5 μm). The mobile phase was a 60:40, v/v mixture of 0.3 % phosphoric acid solution, and acetonitrile 100 %. Chemical oxygen demand (COD) Another form to evaluate the removal of 4ANS, and particularly of some degradation byproducts that cannot be measured by HPLC, was the determination of the chemical oxygen demand in all samples using a closed reflux method 8000 [18]. The reactive kit used could determine COD levels from 3 to 150 mg l−1. Estimation of bacterial diversity in the biofilm and the PBR outflowing liquid The presence or predominance of bacterial strains in the biofilm and in the PBR outflowing liquid was determined by thermal gradient gel electrophoresis (TGGE) of 16S rDNA fragments PCR-amplified (Gene Amp PCR System 2400, USA) using U968 and L1401 primers [13]. The equipment used was a TGGE System (Biometra, Göttingen, Germany), using a thermal gradient of 39–55 °C. Isolation and identification of the cultivable bacteria constituting the microbial community Once finished, the PBR’s last run under nitrogen limitation and the cultivable microorganisms present in the microbial consortium were isolated. Decimal dilutions of a sample of suspended cells were prepared. Aliquots of 200 μl were distributed in nutrient agar plates and incubated at 30 °C. Daily observations were made. The number of different cultivable bacteria present in the microbial community was estimated by observing differences in colonial morphology. Bacterial isolates were cryopreserved in glycerol at −70 °C. Each isolate was propagated in Luria–Bertani medium, and DNA from harvested cells were extracted and purified. By PCR amplification of 16S rDNA with 8FPL (5′ AGT TTG ATC CTG GCT CAG 3′) and 13B (5′ AGG CCC GGG AAC GTA TTC AC 3′) oligonucleotides [45, 46], amplicons of about 1,400 bp were obtained and purified. Purity of bacterial strains was verified by gel electrophoresis of their 16S rDNA fragments. Amplicons were sequenced and compared with known sequences of bacterial 16S rDNA at NCBI GeneBank. Reported species showing the higher similarities were regarded as the isolated species. Results Selection of a microbial consortium able to degrade 4ANS As described in the Methods section, an aliquot of soil suspension was inoculated and incubated in MS1 medium. After successive transfers, the cell population was enriched with microorganisms able to use 4ANS as the sole carbon and energy source. At the eleventh transfer, after incubating the flaks for 24 h, the 4ANS (spectrophotometrically measured at λ238) showed a diminution of 95 %. This microbial community was seeded in agar slants containing MS1 medium. The biomass harvested from the slants was suspended in liquid MS1 medium. Part of the cell suspension was used to isolate the constituents of the microbial consortium. The other part was used as inoculum for the bioreactor start-up. Following the procedure described in the Methods section, the bacterial isolates were identified (Table 1). Identification of the bacterial strains constituting the microbial consortium, which degrades 4ANS Microorganism . Similarity (%) . NCBI accession number . Oleomonas (sagarenensis) 98 D45202 Arthrobacter (chlorophenolicus) 97 CP001341 Arthrobacter sp. 97 FJ449635 Bacillus sp 97 FJ601659 Nocardioides sp 95 AB373748 Microbacterium (oxydans) 92 FJ009389 Microorganism . Similarity (%) . NCBI accession number . Oleomonas (sagarenensis) 98 D45202 Arthrobacter (chlorophenolicus) 97 CP001341 Arthrobacter sp. 97 FJ449635 Bacillus sp 97 FJ601659 Nocardioides sp 95 AB373748 Microbacterium (oxydans) 92 FJ009389 Open in new tab Identification of the bacterial strains constituting the microbial consortium, which degrades 4ANS Microorganism . Similarity (%) . NCBI accession number . Oleomonas (sagarenensis) 98 D45202 Arthrobacter (chlorophenolicus) 97 CP001341 Arthrobacter sp. 97 FJ449635 Bacillus sp 97 FJ601659 Nocardioides sp 95 AB373748 Microbacterium (oxydans) 92 FJ009389 Microorganism . Similarity (%) . NCBI accession number . Oleomonas (sagarenensis) 98 D45202 Arthrobacter (chlorophenolicus) 97 CP001341 Arthrobacter sp. 97 FJ449635 Bacillus sp 97 FJ601659 Nocardioides sp 95 AB373748 Microbacterium (oxydans) 92 FJ009389 Open in new tab Degradation of 4ANS in the packed-bed column reactor operating in steady-state continuous regime Carbon-limited continuous culture Using the MS1 medium, 4ANS volumetric removal rate was evaluated at eight dilution rates D, 0.029–0.714 h−1, corresponding to hydraulic retention times HRT varying from 35.0 to 1.4 h, and 4ANS volumetric loading rates B V,ANS from 1.43 to 35.7 mg l−1 h−1. The results are shown in Fig. 2a. At B V,ANS values lesser than 14.7 mg l−1 h−1, the 4ANS removal efficiencies ηANS, measured by HPLC, rounded the 100 %. At higher B V,ANS values, a gradual decay in ηANS was observed. In carbon limited conditions, at the highest loading rate probed (B V,ANS = 35.7 mg l−1 h−1) ηANS diminished in 63 % (Fig. 3a). Fig. 2 Open in new tabDownload slide Volumetric removal rate of 4ANS (R V,ANS) in the PBR operating in steady-state continuous regime. a Under carbon-limiting conditions. b Under nitrogen-limiting conditions Fig. 3 Open in new tabDownload slide Removal efficiency of 4ANS (ηANS) in the PBR operating in steady-state continuous regime. a Under carbon-limiting conditions. b Under nitrogen-limiting conditions When the xenobiotic removal was measured by the diminution in the chemical oxygen demand COD, a similar trend in R V,COD was observed (Fig. 4a), although with smaller values, rendering ηCOD values as low as 49 % (Fig. 5a). Fig. 4 Open in new tabDownload slide Volumetric removal rate of 4ANS, measured as COD (R V,COD) in the PBR operating in steady-state continuous regime. a Under carbon-limiting conditions. b Under nitrogen-limiting conditions Fig. 5 Open in new tabDownload slide Removal efficiency of 4ANS, measured as COD (ηCOD) in the PBR operating in steady-state continuous regime. a Under carbon-limiting conditions. b Under nitrogen-limiting conditions Accumulation of aromatic byproducts, detected by HPLC, was less than 0.7 %; thus, the difference in the 4ANS removal efficiencies could not be explained by this fact. Thus, accumulation of non-aromatic intermediaries could be responsible of the low values of ηCOD obtained at the smallest loading rates probed in carbon-limited continuous culture. Nitrogen-limited continuous culture The bioreactor was fed with MS2 medium containing 4ANS (50 mg l−1) as the sole source of carbon, nitrogen, and sulfur. In this case, the nitrogen contained in the 4ANS molecule limited the cell growth. Sulfur and carbon were in excess. The R V,ANS was evaluated at dilution rates ranging from 0.0054 to 1.43 h−1, corresponding to HRT values varying from 18.6 to 0.7 h and 4ANS loading rates B V,ANS from 2.6 to 73 mg l−1 h−1. In Figs. 2b and 4b, it can be appreciated that when the microbial consortium was limited by nitrogen (carbon excess), the bioreactor supported much higher 4ANS loading rates than when cell growth was limited by the carbon source. Under nitrogen limitation, it was determined that at B V,ANS values less than 38 mg l−1 h−1, the 4ANS removal efficiencies, measured by HPLC rounded the 100 % (Fig. 3b), and 93 % when measured by COD (Fig. 5b). At higher B V,ANS values, the 4ANS removal rates and efficiencies diminished noticeably. Identification of the isolated bacteria constituting the microbial community The bacterial isolates were identified by 16S rDNA amplification, sequencing, and comparison with known sequences of bacterial 16S rDNA at NCBI GeneBank. The results are presented in Table 1. Estimation of bacterial diversity in the biofilm and in the PBR outflowing liquid TGGE profiles of 16S rDNA fragments of the bacterial consortium grown on 4ANS under carbon or nitrogen limiting conditions (carbon-excess conditions) are shown in Fig. 6. A shift in the microbial diversity corresponding to the change in substrate limiting conditions was observed. Assuming that one DNA band correspond to one bacterial strain, a higher abundance of some bacterial strains in the consortium that grew under nitrogen limitation could be observed. In this case, six well-defined DNA bands in the biofilm and in the PBR-outflowing liquid are evidenced. In contrast, only four sharp DNA bands appear under carbon limitation. It was evident that the consortium structure was altered by the environmental changes that occurred in the bioreactor. Fig. 6 Open in new tabDownload slide Thermal gradient gel electrophoresis of amplicons obtained from 16SrDNA of planktonic cells (LI) and sessile cells (IN) of the microbial community that degrades 4ANS Discussion Differences observed in bioreactor behavior after changing the nutrient limitation could be explained by changes in biofilm structure [3], and in the viscoelastic properties of the biofilm, that difficult its detachment caused by shear stress [27, 48]. From an evolutionary viewpoint, microorganisms have acquired a high degree of plasticity in their physiological responses to changes in environmental conditions; thus, changes in the growth environment can result in a wide variation in morphology, composition, and enzyme activities [31]. Cells growing under carbon excess or carbon limitation could present important differences in gene expression and physiological differences; thus, biofilms formed in carbon-excess conditions (e.g., C/N = 8.57) could show reduced shear removal and minor susceptibility to sloughing due to a more cohesive structure supported on its greater exopolysaccharides (EPS) production. Oxygen and nutrient limitation may be key factors that trigger enhanced resistance mechanisms of sessile communities to hydrodynamic shear forces [52]. This phenomenon was observed when the effects of carbon and oxygen limitations on Pseudomonas putida biofilm removal processes were studied [3]. Additionally, the viscoelastic properties of bacterial biofilms produced in carbon excess conditions allow the biofilm deformation, resisting its detachment due to increased fluid shear, while remaining attached to a surface [48]. Other authors, studying the effects of growth conditions on the production of Xanthomonas campestris exopolysaccharides [60], or on biofilm formation of a P. putida strain [47] also observed that high C:N and C:P ratios in the medium were associated with high levels of polymer production. Additionally, it is a commonly accepted observation that due to the concerted activity of a multimember consortium, often the biodegradation rate of a compound is faster in nature than in pure cultures or in cultures with microbial communities constituted by few members [57]. The concerted metabolic activity of a higher number of bacterial strains could have contributed to the remarkable increase in the biodegradation rate of 4ANS determined under carbon-excess conditions (nitrogen-limiting conditions). Cultivable constituents identified in the bacterial consortium Searching for the characteristics of the species that compose the bacterial biofilm it can be observed that with the exception of Oleomonas, all the bacterial genera found in the microbial consortium have been reported as xenobiotic degraders; however, some strains of this genus could be involved in the initial stages of the biofilm formation. For example, Fernández et al. [14] reports that the initial community involved in biofilm formation is mainly comprised by Oleomonas sagaranensis, an α-proteobacteria [25] that produces extracellular polymers, facilitating its adhesion to the surface of the support material. Few reports exist about the degradation capabilities of Oleomonas, one of them reports that O. sagarensis is involved in the biodegradation of alophanate [24]. Strains of the genus Arthrobacter degrade several organophosphorous pesticides such as Malathion [5], parathion [34], glyphosate [40, 41], monochrotophos [8], and fenitrothion [36]. Bacillus is a bacterial genus with broad metabolic capabilities, able to degrade several xenobiotic compounds. Parathion [34], methyl parathion [54], monocrotophos [43], glyphosate [42], chlorpyrifos [2], pentachlorophenol [26], azo dyes [37, 50], p-aminobenzene [67], and p-nitrophenol [23]. Additionally, it has been reported that the surfactines produced by Bacillus subtilis enhance the biodegradation of hydrocarbon in wastewater bioremediation [32]. Species of the genus Microbacterium have been reported as keratinolytic bacteria [62], as degraders of the pesticides lindane [1], and fenamiphos [11], and able to carry out the desulfurization of dibenzothiophene and other organic sulfur compounds [29], and finally, some species of Nocardioides have been reported as novel crude-oil-degrading bacteria [53]. Conclusions With the enrichment technique used, a microbial community of six bacterial strains, able to use efficiently 4ANS as the sole carbon source and energy, nitrogen and sulfur, was selected. The N-limited system used for the biodegradation of the compound yielded removal rates and efficiencies, measured by HPLC and COD, much higher than those obtained in a C-limited system at comparable 4ANS loading rates and HRT values. The concerted metabolic activity of a higher number of bacterial strains could have contributed to the remarkable increase in the biodegradation rate of 4ANS determined under carbon-excess conditions (nitrogen-limiting conditions). Acknowledgments The authors thank the Secretaría de Investigación y Posgrado, Instituto Politécnico Nacional (SIP-IPN), and Comisión de Fomento de las Actividades Académicas (COFAA-IPN) for fellowships to C. Juárez-Ramírez, N. Ruiz-Ordaz, and J. Galíndez-Mayer, to SIP-IPN for financial support of R. 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TI - Degradation kinetics of 4-amino naphthalene-1-sulfonic acid by a biofilm-forming bacterial consortium under carbon and nitrogen limitations
JF - Journal of Industrial Microbiology and Biotechnology
DO - 10.1007/s10295-012-1123-z
DA - 2012-08-01
UR - https://www.deepdyve.com/lp/oxford-university-press/degradation-kinetics-of-4-amino-naphthalene-1-sulfonic-acid-by-a-oonMfrAcVe
SP - 1169
EP - 1177
VL - 39
IS - 8
DP - DeepDyve
ER -