Abstract
Delftia acidovorans MC1071 can productively degrade R-2-(2,4-dichlorophenoxy)propionate (R-2,4-DP) but not 2,4-dichlorophenoxyacetate (2,4-D) herbicides. This work demonstrates adaptation of MC1071 to degrade 2,4-D in a model two-dimensional porous medium (referred to here as a micromodel). Adaptation for 2,4-D degradation in the 2 cm-long micromodel occurred within 35 days of exposure to 2,4-D, as documented by substrate removal. The amount of 2,4-D degradation in the adapted cultures in two replicate micromodels (~10 and 20 % over 142 days) was higher than a theoretical maximum (4 %) predicted using published numerical simulation methods, assuming instantaneous biodegradation and a transverse dispersion coefficient obtained for the same pore structure without biomass present. This suggests that the presence of biomass enhances substrate mixing. Additional evidence for adaptation was provided by operation without R-2,4-DP, where degradation of 2,4-D slowly decreased over 20 days, but was restored almost immediately when R-2,4-DP was again provided. Compared to suspended growth systems, the micromodel system retained the ability to degrade 2,4-D longer in the absence of R-2,4-DP, suggesting slower responses and greater resilience to fluctuations in substrates might be expected in the soil environment than in a chemostat.
Similar content being viewed by others
References
Acharya RC, Valocchi AJ, Werth CJ, Willingham TW (2007) Pore-scale simulation of dispersion and reaction along a transverse mixing zone in two-dimensional porous media. Water Resour Res 43:W10435
Chomsurin C, Werth CJ (2003) Analysis of pore-scale nonaqueous phase liquid dissolution in etched silicon pore networks. Water Resour Res 39(9):1265–1276
Dorn JG, Brusseau ML, Maier RM (2005) Real-time, in situ monitoring of bioactive zone dynamics in heterogeneous systems. Environ Sci Technol 39(22):8898–8905
Esener AA, Roels JA, Kossen NWF, Roozenburg JWH (1981) Description of microbial growth behaviour during wash-out phase: determination of the specific maximum growth rate. J Appl Microbiol Biotechnol 13:141–144
Habets MGJL, Rozen DE, Hoekstra RF, de Visser JAGM (2006) The effect of population structure on the adaptive radiation of microbial populations evolving in spatially structured environments. Ecol Lett 9:1041–1048
Kerr B, Riley MA, Feldman MW, Bohannan BJM (2002) Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418:171–174
Korona R, Nakatsu CH, Forney LJ, Lenski RE (1994) Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. Proc Nat Acad Sci USA 91:9037–9041
Leibeling S, Schmidt F, Jehmlich N, von Bergen M, Müller RH, Harms H (2010) The declining capacity of starving Delftia acidovorans MC1 to degrade phenoxypropionate herbicides correlates with oxidative modification of the initial enzyme. Environ Sci Technol 44(10):3793–3799
Leibeling S, Maeß MB, Centler F, Kleinsteuber S, von Bergen M, Thullner M, Harms H, Müller RH (2013) Posttranslational oxidative modification of (R)-2,4-dichlorophenoxypropionate/α-ketoglutarate-dioxygenase (RdpA) leads to improved degradation of 2,4-dichlorophenoxyacetate (2,4-D). Eng Life Sci 13:278–291
Long T, Ford RM (2009) Enhanced transverse migration of bacteria by chemotaxis in a porous T-sensor. Environ Sci Technol 43(5):1546–1552
Müller RH (2007) Activity and reaction mechanism of the initial enzymatic step specifying the microbial degradation of 2,4-dichlorophenoxyacetate. Eng Life Sci 7(4):1–12
Müller RH, Babel W (1996) Measurement of growth at very low rates (μ ≥ 0), an approach to study the energy requirement for the survival of Alcaligenes eutrophus JMP134. Appl Environ Microbiol 62:147–151
Müller RH, Babel W (2000) A theoretical study on the metabolic requirements resulting from α-ketoglutarate-dependent cleavage of phenoxyalkanoates. Appl Environ Microbiol 66(1):339–344
Müller RH, Babel W (2001) Pseudo-recalcitrance of chlorophenoxyalkanoate herbicides—correlation to the availability of α-ketoglutarate. Acta Biotechnol 21(3):227–242
Müller RH, Hoffmann D (2006) Uptake kinetics of 2,4-dichlorophenoxyacetate by Delftia acidovorans MC1 and derivative strains: complex characteristics in response to pH and growth substrate. Biosci Biotech Biochem 70(7):1642–1654
Müller RH, Jorks S, Kleinsteuber S, Babel W (1999) Comamonas acidovorans strain MC1: a new isolate capable of degrading the chiral herbicides dichlorprop and mecoprop and the herbicides 2,4-D and MCPA. Microbiol Res 154:241–246
Nambi IM, Werth CJ, Sanford RA, Valocchi AJ (2003) Pore-scale analysis of anaerobic halorespiring bacterial growth along the transverse mixing zone of an etched silicon pore network. Environ Sci Technol 37(24):5617–5624
Paulsen JE, Ekrann S, Oppen E (1999) Visualisation of bacterial degradation and mobilisation of oil in a porous medium. Environ Geol 38(3):204–208
Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394:69–72
Roush CJ, Lastoskie CM, Worden RM (2006) Denitrification and chemotaxis of Pseudomonas stutzeri KC in porous media. J Environ Sci Health Part A 41(6):967–983
Singh R, Olson MS (2011) Transverse mixing enhancement due to bacterial random motility in porous microfluidic devices. Environ Sci Technol 45(20):8780–8787. doi:10.1021/es201706w
Singh R, Olson MS (2012) Transverse chemotactic migration of bacteria from high to low permeability regions in a dual permeability microfluidic device. Environ Sci Technol 46(6):3188–3195. doi:10.1021/es203614y
Stewart TL, Fogler HS (2002) Pore-scale investigation of biomass plug development and propagation in porous media. Biotechnol Bioeng 77(5):577–588
Thullner M, Mauclaire L, Schroth MH, Kinzelbach W, Zeyer J (2002) Interaction between water flow and spatial distribution of microbial growth in a two-dimensional flow field in saturated porous media. J Contam Hydrol 58(3–4):169–189
Vayenas DV, Michalopoulou E, Constantinides GN, Pavlou S, Payatakes AC (2002) Visualization experiments of biodegradation in porous media and calculation of the biodegradation rate. Adv Water Resour 25:203–219
Werth CJ, Cirpka OA, Grathwohl P (2006) Enhanced mixing and reaction through flow focusing in heterogeneous porous media. Water Resour Res 42(12):W12414
Werth CJ, Zhang C, Brusseau ML, Oostrom M, Baumann T (2010) A review of non-invasive imaging methods and applications in contaminant hydrogeology research. J Contam Hydrol 113:1–24
Westendorf A, Müller RH, Babel W (2003) Purification and characterisation of the enantiospecific dioxygenases from Delftia acidovorans MC1 initiating the degradation of phenoxypropionate and phenoxyacetate herbicides. Acta Biotechnol 23(1):3–17
Westendorf A, Benndorf D, Pribyl T, Harms H, Müller RH (2006) Kinetic traits and enzyme form patterns of (R)-2-(2,4-dichlorophenoxy)propionate/α-ketoglutarate dioxygenase (RdpA) after expression in different bacterial strains. Eng Life Sci 6(6):552–559
Willingham T, Werth CJ, Valocchi AJ (2008) Evaluation of the effects of porous media structure on mixing-controlled reactions using pore-scale modeling and micromodel experiments. Environ Sci Technol 42(9):3185–3193
Willingham T, Zhang C, Werth CJ, Valocchi AJ, Oostrom M, Wietsma TW (2010) Using dispersivity values to quantify the effects of pore-scale flow focusing on enhanced reaction along a transverse mixing zone. Adv Water Resour 33(4):525–535
Yoon H, Valocchi AJ, Werth CJ, Dewers T (2012) Pore-scale simulation of mixing-induced calcium carbonate precipitation and dissolution in a microfluidic pore network. Water Resour Res 48:W02524
Zhang C, Kang Q, Wang X, Zilles JL, Müller RH, Werth CJ (2010) Effects of pore-scale heterogeneity and transverse mixing on bacterial growth in porous media. Environ Sci Technol 44(8):3085–3092
Acknowledgments
This work was supported by the National Research Initiative Grant 2007-35107-17817 from the United States Department of Agriculture National Institute of Food and Agriculture and a German Academic Exchange Service (DAAD) fellowship to SL. Sandia National Laboratories is a multi-program laboratory managed and operated by Sandia Corporation, a wholly owned subsidiary of Lockheed Martin Corporation, for the U.S. Department of Energy’s National Nuclear Security Administration under contract DE-AC04-94AL85000. CYZ also acknowledges financial support from the U.S. Department of Energy Office of Biological and Environmental Research, Subsurface Biogeochemistry Research Program Scientific Focus Area at the Pacific Northwest National Laboratory.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yoon, H., Leibeling, S., Zhang, C. et al. Adaptation of Delftia acidovorans for degradation of 2,4-dichlorophenoxyacetate in a microfluidic porous medium. Biodegradation 25, 595–604 (2014). https://doi.org/10.1007/s10532-014-9684-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-014-9684-3