Comprehensive Assessment of Bacterial Communities and Analysis of PCB Congeners in PCB-Contaminated Sediment with Depth
Publication: Journal of Environmental Engineering
Volume 138, Issue 12
Abstract
The potential effectiveness and time scales for monitored natural attenuation of polychlorinated biphenyl (PCB)-contaminated sediments are difficult to predict. Little is known about the depth- and time-dependent dechlorination of PCBs and the microbial communities that give rise to dechlorination processes. The present work describes evaluation of a single sediment core from the Grasse River (Massena, New York) using a combination of molecular techniques to provide detailed insight of dechlorination potential. Primers specific for 16S rRNA genes from the bacterial domains, putative dechlorinating organisms in the phylum Chloroflexi, the Dehalococcoides genus, and two PCB degrading organism strains, o-17 and DF-1, were used to construct phylogenetic microbial community profiles using denaturing gradient gel electrophoresis (DGGE). Further, quantitative polymerase chain reaction (Q-PCR) was used to estimate population numbers of putative PCB-related organisms in the sediments along the depth of the core. PCB congener analysis was used in conjunction with Molar Dechlorination Product Ratio (MDPR, the sum of five PCB end products over total PCBs), chlorine content, chlorine per biphenyl (CPB), and PCB composition changes with depth in the core to evaluate the extent of dechlorination. All core samples contained populations of Chloroflexi, Dehalococcoides, and o-17/DF-1 related organisms, representing the first report of putative dechlorinating organisms with depth in PCB-contaminated sediment. A clear pattern of dechlorination was observed, with deeper (older) sediments showing more extensive dechlorination and middle sediments showing less dechlorination. The evaluation of putative dechlorinating bacterial populations in conjunction with congener shifts resulting from dechlorination enables a critical association that may lead to better prediction of successful natural attenuation of PCB-contaminated sediment.
Get full access to this article
View all available purchase options and get full access to this article.
Acknowledgments
The authors acknowledge the Strategic Environmental Research and Development Program (SERDP) for funding through the Environmental Restoration (ER) program (ER-1495). The authors are grateful to collaborators at The Aluminum Company of America (ALCOA) for their in kind support in provision of sediment and core samples from the Grasse River. Special thanks to Larry McShea, Program Manager, Remediation Work Group, and John Smith, Manager, Sustainable Production Technology.
References
Adrian, L., Dudkova, V., Demnerova, K., and Bedard, D. L. (2009). “Dehalococcoides sp strain CBDB1 extensively dechlorinates the commercial polychlorinated biphenyl mixture Aroclor 1260.” Appl. Environ. Microbiol., 75(13), 4516–4524.
ALCOA. (1999). “Comprehensive characterization of PCBs in the Lower Grasse River.”, New York.
ALCOA. (2009). “Aluminum Company of America New York.”, EPA Region 2, Congressional District(s):24, New York.
Alder, A. C., Haggblom, M. M., Oppenhelmer, S. R., and Young, L. Y. (1993). “Reductive dechlorination of polychlorinated-biphenyls in anaerobic sediments.” Environ. Sci. Technol., 27(3), 530–538.
Bedard, D. L. (2008). “A case study for microbial biodegradation: Anaerobic bacterial reductive dechlorination of polychlorinated biphenyles-from sediment to defined medium.” Ann. Rev. Microbiol., 62, 253–270.
Bedard, D. L., Bailey, J. J., Reiss, B. L., and Jerzak, G. V. (2006). “Development and characterization of stable sediment-free anaerobic bacterial enrichment cultures that dechlorinate Aroclor 1260.” Appl. Environ. Microbiol., 72(4), 2460–2470.
Bedard, D. L., and Quensen, J. F. III (1995). “Microbial reductive dechlorination of polychlorinated biphenyls.” Microbial transformation and degradation of toxic organic chemicals, Young, L. Y., and Cerniglia, G. E., eds., Wiley-Liss, New York, 127–216.
Brenner, R. C. et al. (2004). “Long-term recovery of PCB-contaminated surface sediments at the Sangamo-Weston/Twelvemile Creek/Lake Hartwell superfund site.” Environ. Sci. Technol., 38(8), 2328–2337.
Bzdusek, P. A., Christensen, E. R., Lee, C. M., Pakdeesusuk, U., and Freedman, D. L. (2006). “PCB congeners and dechlorination in sediments of Lake Hartwell, South Carolina, determined from cores collected in 1987 and 1998.” Environ. Sci. Technol., 40(1), 109–119.
Coffin, R. et al. (2008). “Analysis of methane and sulfate flux in methane-charged sediments from the Mississippi Canyon, Gulf of Mexico.” Mar. Petrol. Geol., 25(9), 977–987.
Cutter, L., Sowers, K. R., and May, H. D. (1998). “Microbial dechlorination of 2,3,5,6-tetrachlorobiphenyl under anaerobic conditions in the absence of soil or sediment.” Appl. Environ. Microbiol., 64(8), 2966–2969.
Cutter, L. A., Watts, J. E. M., Sowers, K. R., and May, H. D. (2001). “Identification of a microorganism that links its growth to the reductive dechlorination of 2,3,5,6-chlorobiphenyl.” Environ. Microbiol., 3(11), 699–709.
Duhamel, M., Mo, K., and Edwards, E. A. (2004). “Characterization of a highly enriched Dehalococcoides-containing culture that grows on vinyl chloride and trichloroethene.” Appl. Environ. Microbiol., 70(9), 5538–5545.
Edwards, U., Rogall, T., Blocker, H., Emde, M., and Bottger, E. C. (1989). “Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA.” Nucleic Acids Res., 17(19), 7843–7853.
EPA. (1994). Method 3541-Automatic Soxhlet extraction, U.S. EPA, Washington, DC.
EPA. (1996). Method 3660B-Sulfur cleanup, U.S. EPA, Washington, DC.
EPA. (1997). Phase II reassessment: Data evaluation and interpretation report for the Hudson River PCB superfund site, U.S. EPA, Washington, DC.
EPA. (2007a). Method 9056a-Determinaton of inorganic anions by ion chromatography, U.S. EPA, Washington, DC.
EPA. (2007b). Method 3620C-Florisil cleanup, U.S. EPA, Washington, DC.
Fagervold, S. K., May, H. D., and Sowers, K. R. (2007). “Microbial reductive dechlorination of Aroclor 1260 in Baltimore Harbor sediment microcosms is catalyzed by three phylotypes within the phylum Chloroflexi.” Appl. Environ. Microbiol., 73(9), 3009–3018.
Fagervold, S. K., Watts, J. E. M., May, H. D., and Sowers, K. R. (2005). “Sequential reductive dechlorination of meta-chlorinated polychlorinated biphenyl congeners in sediment microcosms by two different Chloroflexi phylotypes.” Appl. Environ. Microbiol., 71(12), 8085–8090.
Fennell, D. E., Nijenhuis, I., Wilson, S. F., Zinder, S. H., and Haggblom, M. M. (2004). “Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants.” Environ. Sci. Technol., 38(7), 2075–2081.
Frame, G. M., Cochran, J. W., and Bowadt, S. S. (1996). “Complete PCB congener distributions for 17 Aroclor mixtures determined by 3 HRGC systems optimized for comprehensive, quantitative, congener-specific analysis.” J. High Resolut. Chromatogr., 19(12), 657–668.
He, J. Z., Ritalahti, K. M., Aiello, M. R., and Loffler, F. E. (2003). “Complete detoxification of vinyl chloride by an anaerobic enrichment culture and identification of the reductively dechlorinating population as a Dehalococcoides species.” Appl. Environ. Microbiol., 69(2), 996–1003.
Hendrickson, E. R., Payne, J. A., Young, R. M., Starr, M. G., Perry, M. P., and Fahnestock, S. (2002). “Molecular analysis of Dehalococcoides 16S ribosomal DNA from chloroethene-contaminated sites throughout North America and Europe.” Appl. Environ. Microbiol., 68(2), 485–495.
Hiraishi, A. (2008). “Biodiversity of dehalorespiring bacteria with special emphasis on polychlorinated biphenyl/dioxin dechlorinators.” Microbes Environ., 23(1), 1–12.
Hiraishi, A., Sakamaki, N., Miyakoda, H., Maruyama, T., Kato, K., and Futamata, H. (2005). “Estimation of “Dehalococcoides” populations in lake sediment contaminated with low levels of polychlorinated dioxins.” Microbes Environ., 20(4), 216–226.
Imamoglu, I., Li, K., Christensen, E. R., and McMullin, J. K. (2004). “Sources and dechlorination of polychlorinated biphenyl congeners in the sediments of Fox River, Wisconsin.” Environ. Sci. Technol., 38(9), 2574–2583.
Iozza, S., Muller, C. E., Schmid, P., Bogdal, C., and Oehme, M. (2008). “Historical profiles of chlorinated paraffins and polychlorinated biphenyls in a dated sediment core from Lake Thun (Switzerland).” Environ. Sci. Technol., 42(4), 1045–1050.
Karcher, S. C., Small, M. J., and Vanbriesen, J. M. (2004). “Statistical method to evaluate the occurrence of PCB transformations in river sediments with application to Hudson River data.” Environ. Sci. Technol., 38(24), 6760–6766.
Kittelmann, S., and Friedrich, M. W. (2008). “Identification of novel perchloroethene-respiring microorganisms in anoxic river sediment by RNA-based stable isotope probing.” Envrion. Microbiol., 10(1), 31–46.
Kjellerup, B. V., Sun, X. L., Ghosh, U., May, H. D., and Sowers, K. R. (2008). “Site-specific microbial communities in three PCB-impacted sediments are associated with different in situ dechlorinating activities.” Envrion. Microbiol., 10(5), 1296–1309.
Krzmarzick, M. J. et al. (2012). “Natural niche for organohalide-respiring Chloroflexi.” Appl. Environ. Microbiol., 78(2), 393–401.
Lane, D. L. (1991). “16S/23S rRNA sequencing.” Nucleic acid techniques in bacterial systematics, Stackebrandt, E., and Goodfellow, M. N., eds., Wiley, Chichester, U.K., 115–147.
Lovley, D. R. et al. (1993). “Geobacter-metallireducens gen-nov sp-nov, a microorganism capable of coupling the complete oxidation of organic-compounds to the reduction of iron and other metals.” Arch. Microbiol., 159(4), 336–344.
Magar, V. S., Johnson, G. W., Brenner, R. C., Quensen, J. F., Foote, E. A., and Durell, G. (2005). “Long-term recovery of PCB-contaminated sediments at the Lake Hartwell superfund site: PCB dechlorination. 1. End-member characterization.” Environ. Sci. Technol., 39(10), 3538–3547.
May, H. D., Miller, G. S., Kjellerup, B. V., and Sowers, K. R. (2008). “Dehalorespiration with polychlorinated biphenyls by an anaerobic ultramicrobacterium.” Appl. Environ. Microbiol., 74(7), 2089–2094.
Mazumdar, A., Paropkari, A. L., Borole, D. V., Rao, B. R., Khadge, N. H., and Karisiddaiah, S. M. (2007). “Pore-water sulfate concentration profiles of sediment cores from Krishna-Godavari and Goa basins, India.” Geochem. J., 41(4), 259–269.
Muyzer, G., Dewaal, E. C., and Uitterlinden, A. G. (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(3), 695–700.
Page, R. D. M. (1996). “TreeView: An application to display phylogenetic trees on personal computers.” Comput. Appl. Biosci., 12(4), 357–358.
Pakdeesusuk, U., Lee, C. M., Coates, J. T., and Freedman, D. L. (2005). “Assessment of natural attenuation via in situ reductive dechlorination of polychlorinated bipheny is in sediments of the Twelve Mile Creek arm of Lake Hartwell, SC.” Environ. Sci. Technol., 39(4), 945–952.
Pulliam Holoman, T. R., Elberson, M. A., Cutter, L. A., May, H. D., and Sowers, K. R. (1998). “Characterization of a defined 2,3,5,6-tetrachlorobiphenyl-ortho-dechlorinating microbial community by comparative sequence analysis of genes coding for 16S rRNA.” Appl. Environ. Microbiol., 64(9), 3359–3367.
Quensen, J. F., Boyd, S. A., and Tiedje, J. M. (1990). “Dechlorination of four commercial polychlorinated biphenyl mixtures (Aroclors) by anaerobic microorganisms from sediments.” Appl. Environ. Microbiol., 56(8), 2360–2369.
Relman, D. (1993). “Universal bacterial 16S rDNA amplification and sequencing.” Diagnostic medical microbiology: Principles and applications, Persing, D. H., Smith, T. F., Tenover, F. C., and White, T. J., eds., American Society for Microbiology, Washington, DC.
Rhee, G. Y., Sokol, R. C., Bethoney, C. M., and Bush, B. (1993). “Dechlorination of polychlorinated-biphenyls by Hudson River sediment organisms—specificity to the chlorination pattern of congeners.” Environ. Sci. Technol., 27(6), 1190–1192.
Rysavy, J. P., Yan, T., and Novak, P. J. (2005). “Enrichment of anaerobic polychlorinated biphenyl dechlorinators from sediment with iron as a hydrogen source.” Water Res., 39(4), 569–578.
Snoeyenbos-West, O., Van Praagh, C. G., and Lovley, D. R. (2001). “Trichlorobacter thiogenes should be renamed as a Geobacter species.” Appl. Environ. Microbiol., 67(2), 1020–1021.
Sokol, R. C., Kwon, O. S., Bethoney, C. M., and Rhee, G. Y. (1994). “Reductive dechlorination of polychlorinated-biphenyls in St-Lawrence-River sediments and variations in dechlorination characteristics.” Environ. Sci. Technol., 28(12), 2054–2064.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). “The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools.” Nucleic Acids Res., 25(24), 4876–4882.
Tiedje, J. M., Iii, J. F. Q., Chee-Sanford, J., Schimel, J. P., and Boyd, S. A. (1993). “Microbial reductive dechlorination of PCBs.” Biodegradation, 4(4), 231–240.
Watts, J. E. M., Fagervold, S. K., May, H. D., and Sowers, K. R. (2005). “A PCR-based specific assay reveals a population of bacteria within the Chloroflexi associated with the reductive dehalogenation of polychlorinated biphenyls.” Microbiology, 151(Pt. 6), 2039–2046.
Watts, J. E. M., Wu, Q. Z., Schreier, S. B., May, H. D., and Sowers, K. R. (2001). “Comparative analysis of polychlorinated biphenyl-dechlorinating communities in enrichment cultures using three different molecular screening techniques.” Environ. Microbiol., 3(11), 710–719.
Wiegel, J., and Wu, Q. Z. (2000). “Microbial reductive dehalogenation of polychlorinated biphenyls.” Fems Microbiol. Ecol., 32(1), 1–15.
Wu, Q. Z., Bedard, D. L., and Wiegel, J. (1997). “Temperature determines the pattern of anaerobic microbial dechlorination of Aroclor 1260 primed by 2,3,4,6-tetrachlorobiphenyl in Woods Pond sediment.” Appl. Environ. Microbiol., 63(12), 4818–4825.
Wu, Q. Z., Sowers, K. R., and May, H. D. (2000). “Establishment of a polychlorinated biphenyl-dechlorinating microbial consortium, specific for doubly flanked chlorines, in a defined, sediment-free medium.” Appl. Environ. Microbiol., 66(1), 49–53.
Wu, Q. Z., Watts, J. E. M., Sowers, K. R., and May, H. D. (2002). “Identification of a bacterium that specifically catalyzes the reductive dechlorination of polychlorinated biphenyls with doubly flanked chlorines.” Appl. Environ. Microbiol., 68(2), 807–812.
Yan, T., LaPara, T. M., and Novak, P. J. (2006). “The effect of varying levels of sodium bicarbonate on polychlorinated biphenyl dechlorination in Hudson River sediment cultures.” Environ. Microbiol., 8(7), 1288–1298.
Yu, Y., Lee, C., Kim, J., and Hwang, S. (2005). “Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction.” Biotechnol. Bioeng., 89(6), 670–679.
Information & Authors
Information
Published In
Journal of Environmental Engineering
Volume 138 • Issue 12 • December 2012
Pages: 1167 - 1178
Copyright
© 2012 American Society of Civil Engineers.
History
Received: Dec 18, 2011
Accepted: May 24, 2012
Published online: Nov 15, 2012
Published in print: Dec 1, 2012
Authors
Metrics & Citations
Metrics
Citations
Download citation
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.