Abstract
Mechanistic models of enteric bacteria fate and transport in surface waters are important tools for research and management. The existing modeling approach typically assumes that bacteria die in a first-order fashion, but a recent study suggests that bacteria can mutate relatively rapidly to a strain better adapted to the surface water environment. We built an agent-based model that simulates individual wild-type and mutant Escherichia coli cells. The bacteria die, grow on the natural assimilable organic carbon available to E. coli, divide and mutate. We apply the model to laboratory experiments (from the literature and new ones) and the Charles River in Boston. Laboratory applications include decay, growth, and competition (between wild-type and mutant) in various types of surface water. For decay experiments, the stochastic mutation process in the model can produce both first-order and biphasic decay patterns, which is consistent with observations in the literature. For the Charles River, the model can reproduce the main patterns observed in the field data. The model applications provide evidence in support of the mutation mechanism. However, the mutation model does not produce better predictions for the Charles River than a previous model based on labile and resistant subpopulations.
Similar content being viewed by others
References
Auer, M. T., & Niehaus, S. L. (1993). Modeling fecal coliform bacteria—I. Field and laboratory determination of loss kinetics. Water Research, 27, 693–701.
Blumberg, A. F., & Mellor, G. L. (1987). A description of a three-dimensional coastal ocean circulation model. In N. Heaps (Ed.), Three-dimensional coastal ocean models (pp. 1–16). Washington: American Geophysical Union.
Bucci, V., Vulić, M., Ruan, X., & Hellweger, F. L. (2011). Population dynamics of Escherichia coli in surface water. Journal of the American Water Resources Association. http://onlinelibrary.wiley.com/, doi:10.1111/j.1752-1688.2011.00528.x/abstract.
Camper, A. K., McFeters, G. A., Characklis, W. G., & Jones, W. L. (1991). Growth kinetics of coliform bacteria under conditions relevant to drinking water distributions systems. Applied and Environmental Microbiology, 57, 2233–2239.
Campos, P. R. A., & de Oliveria, V. M. (2003). Scale-free networks in evolution. Physica A, 325, 570–576.
Chandaran, A., & Hatha, A. A. M. (2005). Relative survival of Escherichia coli and Salmonella typhimurium in a tropical estuary. Water Research, 39(7), 1397–1403.
Chapra, S. C. (1997). Surface water-quality modeling. Boston, MA: McGraw-Hill.
Chapra, S. C., & Pelletier, G. J. (2003). QUAL2K: a modeling framework for simulating river and stream water quality: documentation and users manual. Medford, MA: Tufts University.
Collins, R., & Rutherford, K. (2004). Modelling bacterial water quality in streams draining pastoral land. Water Research, 38, 700–712.
Connolly, J. P., Coffin, R. B., & Landeck, R. E. (1992). Modeling carbon utilization by bacteria in natural water systems. In C. Hurst (Ed.), Modeling the metabolic and physiologic activities of microorganisms (pp. 249–276). New York: Wiley.
Di Toro, D. M., Fitzpatrick, J. J., & Thomann, R. V. (1983). Documentation for Water Quality Analysis Simulation Program (WASP) and Model Verification Program (MVP). New Jersey: Hydroscience.
Dutka, B. J., & Kwan, K. K. (1980). Bacterial die-off and stream transport studies. Water Research, 14, 909–915.
Easton, J. H., Gauthier, J. J., Lalor, M. M., & Pitt, R. E. (2005). Die-off of pathogenic E. coli O157:H7 in sewage contaminated waters. Journal of the American Water Resources Association, 41(5), 1187–1193.
EPA. (2005). Microbial source tracking guide document. EPA/600/R-05/064. Washington: Environmental Protection Agency.
EPA. (2009). National water quality inventory. Washington, DC: Environmental Protection Agency. http://www.epa.gov/305b/2000report/. Accessed 24 Feb 2009
Escobar, I. C., & Randall, A. A. (2001). Assimilable organic carbon (AOC) and biodegradable dissolved organic carbon (BDOC): complementary measurements. Water Research, 35(18), 4444–4454.
Finkel, S. (2006). Long-term survival during stationary phase: evolution and the GASP phenotype. Nature Reviews Microbiology, 2, 113–120.
Garcia-Armisen, T., Thouvenin, B., & Servais, P. (2006). Modelling faecal coliforms dynamics in the Seine estuary, France. Water Science and Technology, 54(3), 177–184.
Garnier, J., Servais, P., Billen, G., Akopian, M., & Brion, N. (2001). Lower Seine River and Estuary (France) carbon and oxygen budgets during low flow. Estuaries, 24(6B), 964–976.
Grimm, V., Berger, U., DeAngelis, D. L., Polhill, J. G., Giske, J., & Railsback, S. F. (2010). The ODD protocol: a review and first update. Ecological Modelling, 221(23), 2760–2768.
Grover, J. P. (1990). Resource competition in a variable environment: phytoplankton growing according to Monod’s model. The American Naturalist, 136(6), 771–789.
Gunter, S. E., & Kohn, H. I. (1956). Effect of X-rays on the survival of bacteria and yeast II. Relation of cell concentration and endogenous respiration to sensitivity. Journal of Bacteriology, 72, 422–428.
Hammes, F. A., & Egli, T. (2005). New method for assimilable organic carbon determination using flow-cytometric enumeration and a natural microbial consortium as inoculum. Environmental Science & Technology, 39(9), 3289–3294.
Hellweger, F. L. (2008). Spatially explicit individual-based modeling using a fixed super-individual density. Computers & Geosciences, 34, 144–152.
Hellweger, F. L. (2010a). Resonating circadian clocks enhance fitness in cyanobacteria in silico. Ecological Modelling, 221, 1620–1629.
Hellweger, F. L. (2010b). Wildtype and mutant E. coli in the Charles River. YouTube video. http://youtu.be/yHyDySZ-kLU. Accessed 18 Sept 2011.
Hellweger, F. L. (2010c). E. coli age distribution at community boating (density). YouTube video. http://youtu.be/Wn4OHr28tsE. Accessed 18 Sept 2011.
Hellweger, F. L. (2010d). E. coli age distribution at community boating (fraction). YouTube video. http://youtu.be/JGzEbELOmXs. Accessed 18 Sept 2011.
Hellweger, F. L., & Bucci, V. (2009). A bunch of tiny individuals—individual-based modeling for microbes (review paper). Ecological Modelling, 220(1), 8–22.
Hellweger, F. L., & Kianirad, E. (2007a). Individual-based modeling of phytoplankton: evaluating approaches for applying the cell quota model. Journal of Theoretical Biology, 249, 554–565.
Hellweger, F. L., & Kianirad, E. (2007b). Accounting for intra-population variability in biogeochemical models using agent-based methods. Environmental Science & Technology, 41(8), 2855–2860.
Hellweger, F. L., & Masopust, P. (2008). Investigating the fate and transport of E. coli in the Charles River, Boston using high-resolution observation and modeling. Journal of the American Water Resources Association, 44(2), 509–522.
Hellweger, F. L., Bucci, V., Litman, M. R., Gu, A. Z., & Onnis-Hayden, A. (2009). Biphasic decay kinetics of fecal bacteria in surface water: not a density effect. ASCE Journal Environmental Engineering, 135, 372–376.
Hem, L. J., & Efraimsen, H. (2001). Assimilable organic carbon in molecular weight fractions of organic matter. Water Research, 35, 1106–1111.
Hipsey, M. R., Antenucci, J. P., & Brookes, J. D. (2008). A generic, process-based model of microbial pollution in aquatic systems. Water Resources Research, 44, W07048.
HydroQual (2002). A primer for ECOMSED, version 1.3, users manual. New Jersey: HydroQual.
HydroQual (2004). User’s guide for RCA (Release 3.0). New Jersey: HydroQual.
Jurtshuk, P., Jr., & McQuitty, D. N. (1976). Use of a quantitative oxidase test for characterizing oxidative metabolism in bacteria. Applied and Environmental Microbiology, 31, 668–679.
Kreft, J. U., Booth, G., & Wimpenny, J. W. T. (1998). BacSim, a simulator for individual-based modelling of bacterial colony growth. Microbiology, 144, 3275–3287.
LeChavelier, M. W., Shaw, N. E., Kaplan, L. A., & Bott, T. L. (1993). Development of a rapid assimilable organic carbon method for water. Applied and Environmental Microbiology, 59(5), 1526–1531.
Loferer-Krößbacher, M., Klima, J., & Psenner, R. (1998). Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Applied and Environmental Microbiology, 64(2), 688–694.
Martin, J. L., & Wool, T. (2002). A dynamic one dimensional model of hydrodynamics and water quality EPD-RIV1, version 1.0. User’s manual. Athens, GA: AScI Cooperation.
Medema, G. J., Bahar, M., & Schets, F. M. (1997). Survival of Cryptosporidium parvum, Escherichia coli, faecal enterococci and Clostridium perfringens in river water: influence of temperature and autochthonous microorganisms. Water Science and Technology, 35(11), 249–252.
Miller, M. P., McKnight, D. M., Chapra, S. C., & Williams, M. W. (2009). A model of degradation and production of three pools of dissolved organic matter in an alpine lake. Limnology and Oceanography, 54(6), 2213–2227.
Munro, P. M., Flatau, G. N., Clément, R. L., & Gauthier, M. J. (1995). Influence of the RpoS (KatF) sigma factor on maintenance of viability and culturability of Escherichia coli and Salmonella typhimurium in seawater. Applied and Environmental Microbiology, 61(5), 1853–1858.
Roszak, D. B., & Colwell, R. R. (1987). Survival strategies of bacteria in the natural environment. Microbiology Reviews, 51(3), 365–379.
Servais, P., Anzil, A., & Ventresque, C. (1989). A simple method for the determination of biodegradable dissolved organic carbon in water. Applied and Environmental Microbiology, 55, 2732–2734.
Servais, P., Billen, G., Goncalves, A., & Garcia-Armisen, T. (2007). Modelling microbiological water quality in the Seine river drainage network: past, present and future situations. Hydrology and Earth System Science, 11, 1581–1592.
Søndergaard, M., & Middleboe, M. (1995). A cross-system analysis of labile dissolved organic carbon. Marine Ecological Progress Series, 118, 283–294.
Stearns & Wheler Engineers. (1979). Onondaga lake storms impact study. Cazenovia, NY: Stearns and Wheler.
Steets, B. M., & Holden, P. A. (2003). A mechanistic model of runoff-associated fecal coliform fate and transport through a coastal lagoon. Water Research, 37, 589–608.
Thomann, R. V., & Mueller, J. A. (1987). Principles of surface water quality modeling and control. New York: HarperCollins.
Vital, M., Füchslin, H. P., Hammes, F., & Egli, T. (2007). Growth of Vibrio cholerae O1 Ogawa Eltor in freshwater. Microbiology, 153, 1993–2001.
Vital, M., Hammes, F., & Egli, T. (2008). Escherichia coli O157 can grow in natural freshwater at low carbon concentrations. Environmental Microbiology, 10(9), 2387–2396.
Vulić, M., & Kolter, R. (2001). Evolutionary cheating in Escherichia coli stationary phase cultures. Genetics, 158, 519–526.
Wang, Y., Hammes, F., Boon, N., & Egli, T. (2007). Quantification of the filterability of freshwater bacteria through 0.45, 0.22, and 0.1 micron pore size filters and shape-dependent enrichment of filterable bacterial communities. Environmental Science & Technology, 41(20), 7080–7086.
Wetzel, R. G. (2001). Limnology. Lake and river ecosystems (3rd ed.). San Diego: Academic.
WHO, 2011. http://www.who.int/water_sanitation_health/facts_figures/en/index.html. Accessed 30 March 2011.
Zambrano, M. M., Siegele, D. A., Almiron, M., Tormo, A., & Kolter, R. (1993). Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science, 259(5102), 1757–1760.
Acknowledgments
This study was supported by the National Science Foundation. Two anonymous reviewers provided constructive criticism.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Materials
Below is the link to the electronic supplementary material.
ESM 1
PDF 150 kb
Rights and permissions
About this article
Cite this article
Bucci, V., Hoover, S. & Hellweger, F.L. Modeling Adaptive Mutation of Enteric Bacteria in Surface Water Using Agent-Based Methods. Water Air Soil Pollut 223, 2035–2049 (2012). https://doi.org/10.1007/s11270-011-1003-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11270-011-1003-6