Abstract
Autecological properties that are thought to be important for polycyclic aromatic hydrocarbon (PAH)-degradation by bacteria in contaminated soils include the ability to utilize a broad range of carbon sources, efficient biofilm formation, cell-surface hydrophobicity, surfactant production, motility, and chemotaxis. Sphingomonas species are common PAH-degraders, and a selection of PAH-degrading sphingomonad strains isolated from contaminated soils was therefore characterized in terms of these properties. All the sphingomonads tested were relatively hydrophilic and were able to grow as biofilms on a phenanthrene-coated surface, though biofilm formation under other conditions was variable. Sphingobium yanoikuyae B1 was able to utilize the greatest range of carbon sources, though it was not chemotaxic towards any of the substrates tested. Other sphingomonad strains were considerably less flexible in their catabolic range. None of the strains produced detectable surfactant and swimming motility varied between the strains. Examination of the total Sphingomonas community in the soils tested showed that one of the isolates studied was present at significant levels, suggesting that it can thrive under PAH-contaminated conditions despite the lack of many of the tested characteristics. We conclude that these properties are not essential for survival and persistence of Sphingomonas in PAH-contaminated soils.
Similar content being viewed by others
References
Arino S, Marchal R, Vandecasteele JP (1998) Involvement of a rhamnolipid-producing strain of Pseudomonas aeruginosa in the degradation of polycyclic aromatic hydrocarbons by a bacterial community. J Appl Microbiol 84:769–776
Bastiaens L, Springael D, Wattiau P, Harms H, deWachter R, Verachtert H, Diels L (2000) Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Environ Microbiol 66:1834–1843
Bodour AA, Miller-Maier RM (1998) Application of a modified drop-collapse technique for surfactant quantitation and screening of biosurfactant-producing microorganisms. J Microbiol Methods 32:273–280
Bosma TNP, Middeldorp PJM, Schraa G, Zehnder AJB (1997) Mass transfer limitation of biotransformation: quantifying bioavailability. Environ Sci Technol 31:248–252
Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A (1999) The Calgary Biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776
Cunliffe M, Kertesz MA (2005) Effect of Sphingobium yanoikuyae B1 inoculation on bacterial community dynamics and polycyclic aromatic hydrocarbon degradation in aged and freshly PAH-contaminated soils. Environ Pollut (in press) DOI 10.1016/j.envpol.2005.12.026
Gibson DT (1999) Beijerinckia sp strain B1: a strain by any other name. J Ind Microbiol Biotechnol 23:284–293
Grimm AC, Harwood CS (1997) Chemotaxis of Pseudomonas spp. to the polyaromatic hydrocarbon naphthalene. Appl Environ Microbiol 63:4111–4115
Harms H, Wilkes H, Sinnwell V, Wittich RM, Figge K, Francke W, Fortnagel P (1991) Transformation of 3-chlorodibenzofuran by Pseudomonas sp. HH69. FEMS Microbiol Lett 81:25–30
Holden PA, LaMontagne MG, Bruce AK, Miller WG, Lindow SE (2002) Assessing the role of Pseudomonas aeruginosa surface-active gene expression in hexadecane biodegradation in sand. Appl Environ Microbiol 68:2509–2518
Johnsen AR, Karlson U (2004) Evaluation of bacterial strategies to promote the bioavailability of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 63:452–459
Johnsen AR, Winding A, Karlson U, Roslev P (2002) Linking of microorganisms to phenanthrene metabolism in soil by analysis of C-13-labeled cell lipids. Appl Environ Microbiol 68:6106–6113
Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84
Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY (2005) Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol 39:4640–4646
Leys NM, Ryngaert A, Bastiaens L, Verstraete W, Top EM, Springael D (2004) Occurrence and phylogenetic diversity of Sphingomonas strains in soils contaminated with polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:1944–1955
Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, London
Marx RB, Aitken MD (2000) Bacterial chemotaxis enhances naphthalene degradation in a heterogeneous aqueous system. Environ Sci Technol 34:3379–3383
Mazumder R, Phelps TJ, Krieg NR, Benoit RE (1999) Determining chemotactic responses by two subsurface microaerophiles using a simplified capillary assay method. J Microbiol Methods 37:255–263
Mueller JG, Chapman PJ, Blattmann BO, Pritchard PH (1990) Isolation and characterization of a fluoranthene-utilizing strain of Pseudomonas paucimobilis. Appl Environ Microbiol 56:1079–1086
Muyzer G, De Waal ED, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Pang CM, Hong PY, Guo HL, Liu WT (2005) Biofilm formation characteristics of bacterial isolates retrieved from a reverse osmosis membrane. Environ Sci Technol 39:7541–7550
Parales RE, Harwood CS (2002) Bacterial chemotaxis to pollutants and plant-derived aromatic molecules. Curr Opin Microbiol 5:266–273
Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97:4885–4890
Rosenberg M, Rosenberg E (1981) Role of adherence in growth of Acinetobacter calcoaceticus RAG-1 on hexadecane. J Bacteriol 148:51–57
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. CSH, Cold Spring Harbor, NY
Semple KT, Doick KJ, Jones KC, Burauel P, Craven A, Harms H (2004) Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ Sci Technol 38:228A–231A
Singer AC, Thompson IP, Bailey MJ (2004) The tritrophic trinity: a source of pollutant-degrading enzymes and its implications for phytoremediation. Curr Opin Microbiol 7:239–244
Singer AC, van der Gast CJ, Thompson IP (2005) Perspectives and vision for strain selection in bioaugmentation. Trends Biotech 23:74–77
Stenstrom TA (1989) Bacterial hydrophobicity, an overall parameter for the measurement of adhesion potential to soil particles. Appl Environ Microbiol 55:142–147
Streger SH, Vainberg S, Dong HL, Hatzinger PB (2002) Enhancing transport of Hydrogenophaga flava ENV735 for bioaugmentation of aquifers contaminated with methyl tert-butyl ether. Appl Environ Microbiol 68:5571–5579
Thompson IP, van der Gast CJ, Ciric L, Singer AC (2005) Bioaugmentation for bioremediation: the challenge of strain selection. Environ Microbiol 7:909–915
Turnbull GA, Morgan JAW, Whipps JM, Saunders JR (2001) The role of motility in the in vitro attachment of Pseudomonas putida PaW8 to wheat roots. FEMS Microbiol Ecol 35:57–65
Van Broekhoven K, Ryngaert A, Bastiaens L, Wattiau P, Van Canneyt M, Swings J, De Mot R, Springael D (2004) Streptomycin as a selective agent to facilitate recovery and isolation of introduced and indigenous Sphingomonas from environmental samples. Environ Microbiol 6:1123–1136
Wick LY, de Munain AR, Springael D, Harms H (2002) Responses of Mycobacterium sp LB501T to the low bioavailability of solid anthracene. Appl Microbiol Biotechnol 58:378–385
Widada J, Nojiri H, Kasuga K, Yoshida T, Habe H, Omori T (2002) Molecular detection and diversity of polycyclic aromatic hydrocarbon-degrading bacteria isolated from geographically diverse sites. Appl Microbiol Biotechnol 58:202–209
Wittich R-M, Wilkes H, Sinnwell V, Francke W, Fortnagel P (1992) Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1. Appl Environ Microbiol 58:1005–1010
Acknowledgement
This work was supported by the Natural Environment Research Council (NERC).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cunliffe, M., Kertesz, M.A. Autecological properties of soil sphingomonads involved in the degradation of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 72, 1083–1089 (2006). https://doi.org/10.1007/s00253-006-0374-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-006-0374-x