Skip to main content
SpringerLink
Log in

Effect of vegetative filter strips on the dynamics of E. coli biofilm-building potential and expression of virulence factors at Mau, Kenya

  • Original Article
  • Published:
Energy, Ecology and Environment Aims and scope Submit manuscript

Abstract

Escherichia coli (E. coli) populations could become tolerant to extreme environmental temperatures to become resident in soil and surface water habitats creating public health problems. The objective of this study was to understand the interaction between dynamics of E. coli genetic diversity, physiology, and vegetative filter strips (VFS) in overland flows and soil habitats. Pulse-field gel electrophoresis was used to establish the genetic diversity of the isolates (n = 4). Genotypic analysis showed that the runoff isolates do not form a single genetic strain, but that multiple genotype strains were capable of surviving and proliferating in these habitats. High overall unique genotypic diversity was observed in VFS II (38.5%) as compared to VFS III (9.5%) and VFS I (1.5%). Approximately 8.5% E. coli genotypes observed in the surface water and 5.5% observed in soil habitat were shared between different sampling sites, suggesting diffuse sources of E. coli in these habitats. Approximately 32.5% genotypic overlap and a limited sharing (72.5%) between soil and surface water habitats were observed. These findings inferred that certain E. coli strains might have the ability to colonize and adapt to soil and runoff surface water habitats through production of biofilms. Thus, these results confirm that biofilm formation confers competitive advantage to the E. coli environmental isolates including hardiness, versatility, higher resistance to ecological and physical impacts and higher resource availability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahmed W, Tucker J, Bettelheim KA, Neller R, Katouli M (2007) Detection of virulence genes in Escherichia coli of an existing metabolic fingerprint database to predict the sources of pathogenic E. coli in surface waters. Water Res 41:3785–3791. https://doi.org/10.1016/j.watres.2006.12.026

    Article  Google Scholar 

  • American Public Health Association (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, New York

    Google Scholar 

  • Anderson J, Bhandari R, Kumar JP (2005) A genetic screen identifies putative targets and binding partners of CREB-binding protein in the developing Drosophila eye. Genetics 171(4):1655–1672

    Article  Google Scholar 

  • Atlas RM (1984) Use of microbial diversity measurements to assess the environmental stress. In: Klug MJ, Reddy CA (eds) Current perspectives in microbiol ecology. American Society for Microbiology, Washington, DC

    Google Scholar 

  • Baertsch C, Paez-Rubio T, Viau E, Peccia J (2007) Source tracking aerosols released from land-applied class B bio solids during high-wind events. Appl Environ Microbiol 73:4522–4531

    Article  Google Scholar 

  • Beloin C, Roux A, Ghigo JM (2008) Escherichia coli biofilms. Curr Top Microbiol Immunol 322:249–289. https://doi.org/10.1007/978-3-540-75418-3-2

    Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  Google Scholar 

  • Blount ZD (2015) The unexhausted potential of E. coli. Elife 4:e06956. https://doi.org/10.7554/eLife.05826.001

    Article  Google Scholar 

  • Blount ZD, Barrick JE, Davidson CJ, Lenski RE (2012) Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489:513–518. https://doi.org/10.1038/nature11514

    Article  Google Scholar 

  • Bonetta S, Borelli E, Bonetta S, Conio O, Palumbo F, Carraro E (2011) Development of a PCR protocol for the detection of Escherichia coli O157:H7 and Salmonella spp. in surface water. Environ Monit Assess 177:493–503. https://doi.org/10.1007/s10661-010-1650-x

    Article  Google Scholar 

  • Brennan FP, Abram F, Chinalia FA, Richards KG, O’Flaherty V (2010) Characterization of environmentally persistent Escherichia coli population leached from an Irish soil. Appl Environ Microbiol 76(7):2175–2180

    Article  Google Scholar 

  • Byappanahalli MN, Fujioka RS (1998) Evidence that tropical soil environment can support the growth of Escherichia coli. Water Sci Technol 38(12):171–174

    Google Scholar 

  • Byappanahalli MN, Shively DA, Nevers MB, Sadowssky MJ, Whitman RL (2003a) Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). FEMS Microbiol Ecol 46:203–211

    Article  Google Scholar 

  • Byappanahalli M, Fowler M, Shively D, Whitman R (2003b) Ubiquity and persistence of Escherichia coli in a midwestern coastal stream. Appl Environ Microbiol 69:4549–4555

    Article  Google Scholar 

  • Byappanahalli MN, Shively DA, Nevers MB, Sadowsky MJ, Whitman RL (2003c) Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). FEMS Microbiol Ecol 46:203–211

    Article  Google Scholar 

  • Byappanahalli MN, Whitman RL, Shively DA, Evert Ting WT, Tseng CC, Nevers MB (2006) Seasonal persistence and population characteristics of Escherichia coli and enterococci in deep backshore san of two freshwater beaches. J Water Health 04(3):313

    Article  Google Scholar 

  • Carson CA, Shear BL, Ellersieck MR, Asfaw A (2001) Identification of fecal Escherichia coli from humans and animals by ribotyping. Appl Environ Microbiol 67:1503–1507

    Article  Google Scholar 

  • Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558

    Article  Google Scholar 

  • Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 5:58–65

    Article  Google Scholar 

  • D’Elia CF, Steudler PA, Corwin N (1977) Determination of total nitrogen in aqueous samples using persulfate digestion. Limnol Ocean 22:760–764

    Article  Google Scholar 

  • Delbès C, Moletta R, Godon JJ (2000) Monitoring of activity dynamics of an anaerobic digester bacterial community using 16S rRNA polymerase chain reaction–single-strand conformation polymorphism analysis. Environ Microbiol 2:506–515

    Article  Google Scholar 

  • Dick LK, Stelzer EA, Bertke EE, Fong DL, Stoeckel DM (2010) Relative decay of Bacteroidales microbial source tracking markers and cultivated Escherichia coli in freshwater microcosms. Appl Environ Microbiol 76:3255–3262. https://doi.org/10.1128/AEM.02636-09

    Article  Google Scholar 

  • Dombek PE, Johnson LK, Zimmerley ST, Sadowsky MJ (2000) Use of repetitive DNA sequences and the PCR to differentiate Escherichia coli isolates from human and animal sources. Appl Environ Microbiol 66:2572–2577

    Article  Google Scholar 

  • Eaton AD, Clesceri LS, Rice EW, Greenberg AE (eds) (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Eisakhani M, Malakahmad A (2009) Water quality assessment of Bertam River and its tributaries in cameron highlands, Malaysia. J World Appl Sci 7(6):769–776

    Google Scholar 

  • Escherich T (1988) The intestinal bacteria of the neonate and breastfed infant (1885). Rev Infect Dis 10:1220–1225

    Article  Google Scholar 

  • Ferguson C, De Roda Husman A, Altavilla N, Deere D, Ashbolt N (2003a) Fate and transport of surface water pathogens in watersheds. Crit Rev Environ Sci Technol 33(3):299–361

    Article  Google Scholar 

  • Ferguson C, De Roda Husman A, Altavilla N, Deere D, Ashbolt N (2003b) Fate and transport of surface water pathogens in watersheds. Crit Rev Environ Sci Technol 33(3):299–361

    Article  Google Scholar 

  • Gerba CP, Smith JE (2004) Sources of pathogenic microorganisms and their fate during land application of wastes. J Environ Qual 34:42–48

    Google Scholar 

  • Gordon DM, Bauer S, Johnson JR (2002) The genetic structure of Escherichia coli populations in primary and secondary habitats. Microbiology 148:1513–1522

    Article  Google Scholar 

  • Gordon DM, Clermont O, Tolley H, Denamur E (2008) Assigning Escherichia coli strains to phylogenetic groups: multilocus sequence typing versus the PCR triplex method. Environ Microbiol 10:2484–2496

    Article  Google Scholar 

  • Gotelli NJ, Entsminger GL (2004) EcoSim 700; null models software for ecology, version 7. Acquired Intelligence Inc., and Kesey-Bear, Burlington, VT

  • Goto D, Yan T (2011) Effects of land uses on fecal indicator bacteria in the water and soil of a tropical watershed. Microbes Environ 26(3):254–260

    Article  Google Scholar 

  • Greenberg AF, Clesceri LS, Eaton AD (1992) Standard methods for examination of water and waste water, 18th edn. American Public Health Association, Washington, DC, USA

    Google Scholar 

  • Hagstrom A, Larsson U, Horstedt P, Normark S (1979) Frequency of dividing cells a new approach to the determination of bacterial growth rates in aquatic environment. Appl Environ Microbial 37:805–812

    Google Scholar 

  • Hammer ØD, Harper AT, Ryan PD (2005) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:4–9

    Google Scholar 

  • Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M (2011) Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis 15(4):1413–8670. https://doi.org/10.1590/S1413-86702011000400002

    Article  Google Scholar 

  • Hay V, Pittroff W, Tooman EE, Meyer D (2006) Effectiveness of vegetated filter strips in attenuating nutrient and sediment overland from irrigated pastures. J Agric Sci 144:349–360

    Article  Google Scholar 

  • Haydon S, Deletic A (2006) Development of a coupled pathogen-hydrologic catchment model. J Hydrol 328:467–480

    Article  Google Scholar 

  • Hood MA, Ness GE (1982) Survival of Vibrio cholerae and Escherichia coli in estuarine waters and sediments. Appl Environ Microbiol 43(3):578–584

    Google Scholar 

  • Ishii S, Ksoll WB, Hicks RE, Sadowsky MS (2006) Presence and growth of natural Escherichia coli in temperate soils from Lake Superior Watershed. Appl Environ Microbiol 72(1):612–621. https://doi.org/10.1128/AEM.72.1.612-621.2006

    Article  Google Scholar 

  • Ishii A, Kawasaki M, Matsumoto M, Tochinai S, Seya T (2007) Phylogenetic and expression analysis of amphibian Xenopus Toll-like receptors. Immunogenetics 59(4):281–293

    Article  Google Scholar 

  • Jamieson RC, Gordon RJ, Sharles KE, Stratton GW, Madani A (2002) Movement and persistence of fecal bacteria in agricultural soils and subsurface drainage water: a review. Can Biosyst Eng 44:1.1–1.9

    Google Scholar 

  • Kaper JB (2005) Pathogenic Escherichia coli. Int J Med Microbiol 295:355–356. https://doi.org/10.1016/j.ijmm.2005.06.008

    Article  Google Scholar 

  • Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140. https://doi.org/10.1038/nrmicro818

    Article  Google Scholar 

  • Karanis P, Kourenti C, Smith H (2007) Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health 5:1–38

    Article  Google Scholar 

  • Khaleel R, Foster GR, Reddy KR, Overcash MR, Westerman PW (1979) A non—point source model for land areas receiving animal waste: III. A conceptual model for sediment and manure transport. Trans Am Soc Agric Eng 22(6):1353–1361

    Article  Google Scholar 

  • Kim L (2001) Riddle of biofilm resistance. Antimic Ag Chemother 45(4):999–1007

    Article  Google Scholar 

  • Kingsley MT, Bohlool BB (1981) Release of Rhizobium spp. from tropical soils and recovery for immunofluorescence enumeration. Appl Environ Microbiol 42:241–248

    Google Scholar 

  • Kirk RE (1982) Experimental design: procedures for the behavioural sciences, 2nd edn. Brooks Cole Publishing Co, Belmont

    Google Scholar 

  • Kiruki S, Limo KM, Njagi ENM, Okemo PO (2011) Bacteriological quality and diarrhoeagenic pathogens on River Njoro and Nakuru Municipal water, Kenya. Int J Biotechnol Mol Biol Res 2(9):150–162

    Google Scholar 

  • Klein DA, Casida LE Jr (1967) Escherichia coli die-out from normal soil as related to nutrient availability and the indigenous micro flora. Can J Microbiol 13:1461–1470

    Article  Google Scholar 

  • Ksoll WB, Ishii S, Sadowsky MJ, Hicks RE (2007) Presence and sources of fecal coliform bacteria in epilithic periphyton communities of Lake Superior. Appl Environ Microbiol 73(12):3771–3778

    Article  Google Scholar 

  • Lalancette C et al (2014) Changes in Escherichia coli to Cryptosporidium ratios for various fecal pollution sources and drinking water intakes. Water Res 55:150–161. https://doi.org/10.1016/j.watres.2014.01.050

    Article  Google Scholar 

  • Lim TT, Edwards DR, Workman SR, Larson BT, Dunn L (1998) Vegetated filter strip removal of cattle manure constituents in overland. Trans ASAE 41:1375–1381

    Article  Google Scholar 

  • Liu YJ, Zhang CM, Wang XC (2009) Simultaneous detection of enteric bacteria from surface waters by QPCR in comparison with conventional bacterial indicators. Environ Monit Assess 158:535–544. https://doi.org/10.1007/s10661-008-0602-1

    Article  Google Scholar 

  • Maciolek JA (1962) Limnological organic analyses by quantitative dichromate oxidation. In: Wetzel RG, Likens GE (eds) Limnological analyses. Springer, New York, p 391

    Google Scholar 

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902

    Article  Google Scholar 

  • Mavura WJ, Ngari MS, Matofari JW, Muliro PS, Perry J, Harden A, Carter M (2006) How safe is the water we drink? Determination of chemical and bacteriological quality of various water sources in Njoro, Nakuru District, Kenya. Egerton J Sci Technol 4:17–28

    Google Scholar 

  • Moreira CG, Palmer K, Whiteley M, Sireili MP, Trabulsi LR, Castro AFP, Sperandio V (2006) Bundle—forming pili and EspA are involved in biofilm formation by enteropathogenic Escherichia coli. Bacteriol 188(11):3952–3961. https://doi.org/10.1128/JB.00177-06

    Article  Google Scholar 

  • Muia AW, Bretschko G, Herndl GJ (2011) An overview of the structure and function of microbial biofilms, with special emphasis on heterotrophic aquatic microbial communities. Afr J Aquat Sci 36(1):1–10

    Article  Google Scholar 

  • Muirhead RW, Collins RP, Bremer PJ (2006) Interaction of Escherichia coli and soil particles in overland. Appl Environ Microbiol 72(5):3406–3411

    Article  Google Scholar 

  • Nesse LL, Sekse C, Berg K, Johannesen KC, Solheim H, Vestby LK, Urdahl AM (2014) Potentially pathogenic Escherichia coli can form a biofilm under conditions relevant to the food production chain. Appl Environ Microbiol 80:2042–2049. https://doi.org/10.1128/AEM.03331-13

    Article  Google Scholar 

  • Noble RT, Weisberg SB (2005) A review of technologies for rapid detection of bacteria in recreational waters. J Water Health 3:381–392

    Article  Google Scholar 

  • Noor R, Islam Z, Munshi SK, Rahman F (2013) Influence of temperature on E. coli growth in different culture media. J. Pure Appl Microbiol 7(2):899–904

    Google Scholar 

  • Odonkor ST, Ampofo JK (2013) Escherichia coli as an indicator of bacteriological quality of water. Microbiol Res 4:5–11

    Article  Google Scholar 

  • Olilo CO, Muia AW, Moturi WN, Onyando JO, Amber FR (2016a) The current state of knowledge on the interaction of E. coli within vegetative filter strips as a sustainable best management practice to reduce fecal pathogen loading into surface waters. Energ Ecol Environ 1(4):248–266. https://doi.org/10.1007/s40974-016-0026-7

    Article  Google Scholar 

  • Olilo CO, Onyando JO, Moturi WN, Muia AW, Amber FR, Ogari ZF, Ombui PN, Shivoga WA (2016b) Composition and design of vegetative filter strips instrumental in improving water quality by mass reduction of suspended sediment, nutrients and Escherichia coli in overland flows in eastern escarpment of Mau Forest, Njoro River Watershed, Kenya. Energ Ecol Environ 1(6):386–407. https://doi.org/10.1007/s40974-016-00329

    Article  Google Scholar 

  • Olilo CO, Onyando JO, Moturi WN, Muia AW, Ombui P, Shivoga WA, Roegner AF (2016c) Effect of vegetated filter strips on transport and deposition rates of Escherichia coli in overland flow in the eastern escarpments of the Mau Forest, Njoro River Watershed, Kenya. Energ Ecol Environ 1(3):157–182. https://doi.org/10.1007/s40974-016-006-y

    Article  Google Scholar 

  • Olilo CO, Muia WA, Onyando JO, Moturi WN, Ombui PN, Shivoga WA (2017) Effect of vegetated filter strips on infiltration and survival rates of E. coli in soil matrix at Mau, Njoro River Watershed, Kenya. Energ Ecol Environ 2(2):125–142. https://doi.org/10.1007/s40974-016-0049-0

    Article  Google Scholar 

  • Pachepsky YA, Sadeghi AM, Bradford SA, Shelton DR, Guber AK, Dao T (2006) Transport and fate of manure-borne pathogens: modeling perspective. Agric Water Manag 86(1–2):81–92. https://doi.org/10.1016/j.agwat.2006.06.010

    Article  Google Scholar 

  • Ponciano JM, La HJ, Joyce P, Forney LJ (2009) Evolution of diversity in spatially structured Escherichia coli populations. Appl Environ Microbiol 75:6047–6054. https://doi.org/10.1128/AEM.00063-09

    Article  Google Scholar 

  • Quero GM, Fasolato L, Vignaroli C, Luna GM (2015) Understanding the association of Escherichia coli with diverse macroalgae in the lagoon of Venice. Sci Rep 5:10969. https://doi.org/10.1038/srep10969

    Article  Google Scholar 

  • Ram S, Vajpayee P, Dwivedi PD, Shanker R (2011) Culture-free detection and enumeration of STEC in water. Ecotoxicol Environ Saf 74:551–557. https://doi.org/10.1016/j.ecoenv.2011.01.019

    Article  Google Scholar 

  • Rauch EM, Bar-Yam Y (2004) Theory predicts the uneven distribution of genetic diversity within species. Nature 431:449–452. https://doi.org/10.1038/nature02745

    Article  Google Scholar 

  • Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, Barrett TJ (2006) Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodbourne Path Dis 3:59–67

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Samson RW, Swiatnicki SA, Osinga VL, Supita JL, McDermott CM, Kleinheinz GT (2006) Effects of temperature and sand on E. coli survival in a northern lake water microcosm. J Water Health 04(3):389–393

    Article  Google Scholar 

  • Savichtcheva O, Okabe S (2006) Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res 40:2463–2476. https://doi.org/10.1016/j.watres.2006.04.040

    Article  Google Scholar 

  • Sharpley AN (1993) An innovative approach to estimate bio available phosphorus in agricultural overland using iron-impregnated paper. J Environ Qual 22:597–601

    Article  Google Scholar 

  • Shelton DR et al (2006) Impact of microbial diversity on rapid detection of enterohemorrhagic Escherichia coli in surface waters. FEMS Microbiol Lett 261:95–101. https://doi.org/10.1111/j.1574-6968.2006.00334.x

    Article  Google Scholar 

  • Shih CM et al (2015) Paper-based ELISA to rapidly detect Escherichia coli. Talanta 145:2–5. https://doi.org/10.1016/j.talanta.2015.07.051

    Article  Google Scholar 

  • Shivoga W, Moturi WN (2009) Geophaga as a risk factor for diarrhoea. J Infect Dev Ctries 3(2):94–98

    Google Scholar 

  • Shulman ST, Friedman HC, Sims RH (2007) Theodor Escherich: the first pediatric infectious diseases physician? Clin Infect Dis 45:1025–1029. https://doi.org/10.1086/521946

    Article  Google Scholar 

  • Snedecor WG, Cochran WG (1980) Statistical methods, 7th edn. Iowa State University Press, Ames

    MATH  Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of sea water analysis. 2nd Ed. Bull Fish Res Bio Can 167:310

    Google Scholar 

  • Suh SJ, Suh LS, Woods DE, Hassett DJ, West SHE, Ohman DE (1999) Effect of rpoS Mutation on the stress Response and Expression of Virulence Factors in Pseudomonas aeruginosa. J Bacteriol 181(13):3890–3897

    Google Scholar 

  • SYSTAT Software, Inc., 2007. SYSTAT 12, Statistics I, II, III, IV. pp. 2200, Chicago

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software, version 4.0. Mol Biol Evol 24:1596–1599

    Article  Google Scholar 

  • Tate KW, Atwill ER, Bartolome JW, Nader G (2006) Significant Escherichia coli attenuation by vegetated buffers on annual grasslands. J Environ Qual 35:795–805

    Article  Google Scholar 

  • Tran NH, Gin KY, Ngo HH (2015) Fecal pollution source tracking toolbox for identification, evaluation and characterization of fecal contamination in receiving urban surface waters and groundwater. Sci Total Environ 538:38–57. https://doi.org/10.1016/j.scitotenv.2015.07.155

    Article  Google Scholar 

  • Tyerman JG, Ponciano JM, Joyce P, Forney LJ, Harmon LJ (2013) The evolution of antibiotic susceptibility and resistance during the formation of Escherichia coli biofilms in the absence of antibiotics. BMC Evol Biol 13:22. https://doi.org/10.1186/1471-2148-13-22

    Article  Google Scholar 

  • Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831

    Article  Google Scholar 

  • Vogeleer P, Tremblay YD, Mafu AA, Jacques M, Harel J (2014) Life on the outside: role of biofilms in environmental persistence of Shiga toxin producing Escherichia coli. Front Microbiol 5:317. https://doi.org/10.3389/fmicb.2014.00317

    Article  Google Scholar 

  • Wang X, Rochon M, Lamprokostopoulou H, Lunsdorf H, Nimitz M, Romling U (2006) Impact of biofilm matrix components of commensal Escherichia coli with the gastrointestinal cell lineHT-29. Cell Mol Life Sci 63:2352–2363. https://doi.org/10.1007/s00018-oo6-6222-4t

    Article  Google Scholar 

  • Whitman RL, Nevers MB (2003) Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan Beach. Appl Environ Microbiol 69(9):5555–5562. https://doi.org/10.1128/AEM.69.9.555-5562.2003

    Article  Google Scholar 

  • Winfield MD, Groisman EA (2003) Role of non-host environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 69:3687–3694

    Article  Google Scholar 

  • Yamahara KM, Layton BA, Santoro AE, Boehm AB (2007) Beach sands along the California coast are diffuse sources of fecal bacteria to coastal waters. Environ Sci Technol 41:5415–5421

    Article  Google Scholar 

  • Yao Q, Lu Q, Wan X, Song F, Xu Y, Hu M, Zamyatina A, Liu X, Huang N, Xhu P, Shao F (2014) A structural mechanism for bacterial autotransporter glycosylation by a dodecameric heptosytransferase family. Biophics Struct Biol Microbiol Infect Dis eLife Digest. https://doi.org/10.7554/eLife.03714.001

    Google Scholar 

  • Zar JH (1996) Multiple Comparisons; Comparing simple linear regression equations. Biostatistical Analysis. 212. 353–369. 3rd ed. Englewood Cliffs, N.J. Printice Hall, New York USA

  • Zimmer C (2008) Microcosm. Pantheon Books; USA, New York

    Google Scholar 

Download references

Acknowledgements

This study was designed by among others Eng. Professor Japheth O. Onyando, the chairperson, Department of Agricultural Engineering and Technology; Dr. Anastasia W. Muia, the Department of Biological Sciences; and Dr. Wilkister N. Moturi, Department of Environmental Science. Our deepest appreciation goes to the Dean Faculty of Agriculture for granting us the permission to work in field 18 of Tatton Agriculture Park (TAP). We appreciate The Nakuru County Laboratory for the use of their facility for microbial analyses. We wish to thank The Department of Water and Civil Engineering of Egerton University provided the Meteorological data from Egerton University weather station. The Director, Kenya Marine and Fisheries Research Institute (KMFRI), Prof James M. Njiru who granted me the study grant under Egerton University (EU)_KMFRI Memorandum of Understanding (MOU) Study Programme is highly appreciated. This study was funded by The Kenya National Commission of Science and Technology, the Science, Technology and Innovation Ph.D. research Grant, under Grant nos: NCST/ST and I/RCD/4th Call PhD/181.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Egerton University, P.O. Box 536, Egerton, 20115, Kenya

    Anastasia Wairimu Muia

  2. Department of Agricultural Engineering and Technology, Egerton University, P.O. Box 536, Egerton, 20115, Kenya

    Japheth Ogalo Onyando

  3. Department of Environmental Science, Egerton University, P.O. Box 536, Egerton, 20115, Kenya

    Casianes Owino Olilo & Wilkister Nyaora Moturi

Authors
  1. Casianes Owino Olilo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anastasia Wairimu Muia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Japheth Ogalo Onyando
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wilkister Nyaora Moturi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Casianes Owino Olilo.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Olilo, C.O., Muia, A.W., Onyando, J.O. et al. Effect of vegetative filter strips on the dynamics of E. coli biofilm-building potential and expression of virulence factors at Mau, Kenya. Energ. Ecol. Environ. 3, 110–125 (2018). https://doi.org/10.1007/s40974-018-0081-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40974-018-0081-3

Keywords

Search

Navigation