Bacterial community succession during in situ uranium bioremediation: Spatial similarities along controlled flow paths

ISME Journal

Volumn 3, Issue 1, 2009, Pages 47-64

  Hwang, Chiachi ^a,b   Wu, Weimin ^b   Gentry, Terry J ^c   Carley, Jack ^d   Corbin, Gail A ^a   Carroll, Sue L ^d   Watson, David B ^d   Jardine, Phil M ^d   Zhou, Jizhong ^e,f   Criddle, Craig S ^b   Fields, Matthew W ^b,f  

^a MIAMI UNIVERSITY   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF OKLAHOMA   (United States)

^f Virtual Institute of Microbial Stress and Survival

Author keywords

Bacterial community dynamics; Uranium bioreduction; Uranium reducing populations

Indexed keywords

ALCOHOL; BACTERIAL DNA; BACTERIAL RNA; METAL; RIBOSOME DNA; RNA 16S; SULFATE; URANIUM;

ARTICLE; BACTERIUM; BIODIVERSITY; BIOREMEDIATION; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYLOGENY; RNA GENE; SEQUENCE HOMOLOGY;

BACTERIA; BIODEGRADATION, ENVIRONMENTAL; BIODIVERSITY; DNA, BACTERIAL; DNA, RIBOSOMAL; ENVIRONMENTAL MICROBIOLOGY; ETHANOL; GENES, RRNA; METALS; OXIDATION-REDUCTION; PHYLOGENY; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SULFATES; URANIUM;

BACTERIA (MICROORGANISMS);

EID: 58049123401     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2008.77     Document Type: Article

References (66)

1. Abdelouas A, Lutze W, Gong W, Nuttall EH, Strietelmeier BA, Travis BJ. (2000). Biological reduction of uranium in groundwater and subsurface soil. Sci Total Environ 250: 21-35.
2. Abed RM, Safi NM, Köster J, de Beer D, El-Nahhal Y, Rullkötter J et al. (2002). Microbial diversity of a heavily polluted microbial mat and its community changes following degradation of petroleum compounds. Appl Environ Microbiol 68: 1674-1683.
3. Akob DM, Mills HJ, Kostka JE. (2007). Metabolically active microbial communities in uranium-contaminated subsurface sediments. FEMS Microbiol Ecol 59: 95-107.
4. Allen JP, Atekwana EA, Atekwana EA, Duris JW, Werkema DD, Rossbach S. (2007). The microbial community structure in petroleum-contaminated sediments correspond to geophysical signatures. Appl Environ Microbiol 73: 2860-2870.
5. Anderson CR, Pedersen K. (2003). In situ growth of Gallionella biofilms and partitioning of lanthanides and actinides between biological material and ferric oxyhidroxides. Geobiology 1: 169-178.
6. Anderson MJ, Gribble NA. (1998). Partitioning the variation among spatial, temporal and environmental components in a multivariate data set. Austral Ecol 23: 158-167.
7. Anderson MJ, Willis TJ. (2003). Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511-525.
8. Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Long PE, Dayvault R et al. (2003). Stimulating the in situ activity of Geobactey species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl Environ Microbiol 69: 5884-5891.
9. Barns SM, Cain EC, Sommerville L, Kuske CR. (2007). Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73: 3113-3116.
10. Brown MV, Bowman JP. (2001). A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol Ecol 35: 267-275.
11. Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personné JC. (2006). Diversity of microorganisms in Fe-As-rich acid mine drainage waters of Carnoulès, France. Appl Environ Microbiol 72: 551-556.
12. Cao Y, Cherr GN, Córdova-Kreylos AL, Fan TW, Green PG, Higashi RM et al. (2006). Relationships between sediment microbial communities and pollutants in two California salt marshes. Microb Ecol 52: 619-633.
13. Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry T et al. (2008). Microbial communities in contaminated sediments after bioremediation to submicromolar levels. Appl Environ Microbiol 74: 3718-3729.
14. Chang YJ, Long PE, Geyer R, Peacock AD, Resch CT, Sublette K et al. (2005). Microbial incorporation of 13C-labeled acetate at the field scale: detection of microbes responsible for reduction of U(VI). Environ Sci Technol 39: 9039-9048.
15. Chang YJ, Peacock AD, Long PE, Stephen JR, McKinley JP, Macnaughton SJ et al. (2001). Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. Appl Environ Microbiol 67: 3149-3160.
16. Coates JD, Ellis DJ, Gaw CV, Lovley DR. (1999). Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Bacterial 49: 1615-1622.
17. Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA et al. (2003). The ribosomal database project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31: 442-443.
18. Cordova-Kreylos AL, Cao Y, Green PG, Hwang HM, Kuivila KM, Lamontagne MG et al. (2006). Diversity, composition, and geographical distribution of microbial communities in California salt marsh sediments. Appl Environ Microbiol 72: 3357-3366.
19. Craft ES, Abu-Qare AW, Flaherty MM, Garofolo MC, Rincavage HL, Abou-Donia MB. (2004). Depleted and natural uranium: chemistry and toxicological effects. J Toxicol Environ Health B Grit Rev 7: 297-317.
20. Cummings DE, Snoeyenbos-West OL, Newby DT, Niggemyer AM, Lovley DR, Achenbach LA et al. (2003). Diversity of Geobacteraceae species inhabiting metalpolluted freshwater lake sediments ascertained by 16S rDNA analyses. Microb Ecol 46: 257-269.
21. Elias DA, Krumholz LR, Wong D, Long PE, Suflita JM. (2003). Characterization of microbial activities and U reduction in a shallow aquifer contaminated by uranium mill tailings. Microb Ecol 46: 83-91.
22. Fields MW, Bagwell CE, Carroll SL, Yan T, Liu X, Watson DB et al. (2006). Phylogenetic and functional biomarkers as indicators of bacterial community responses to mixed-waste contamination. Environ Sci Technol 40: 2601-2607.
23. Fields MW, Yan T, Rhee SK, Carroll SL, Jardine PM, Watson DB et al. (2005). Impacts on microbial communities and cultivable isolates from groundwater contaminated with high levels of nitric acid-uranium waste. FEMS Microbiol Ecol 53: 417-428.
24. Fite A, Macfarlane GT, Cummings JH, Hopkins MJ, Kong SC, Furrie E et al. (2004). Identification and quantitation of mucosal and faecal Desulfovibrios using real-time polymerase chain reaction. Gut 53: 523-529.
25. Francis AJ, Dodge CJ, Lu F, Halada GP, Clayton CR. (1994). XPS and XANES studies of uranium reduction by Clostridia sp. Environ Sci Tehcnol 28: 636-639.
26. Geets J, Vanbroekhoven K, Borremans B, Vangronsveld J, Diels L, van der Lelie D. (2006). Column experiments to assess the effects of electron donors on the efficiency of in situ precipitation of Zn, Cd, Co and Ni in contaminated groundwater applying the biological sulfate removal technology. Environ Sci Pollut Res Int 13: 362-378.
27. Gremion F, Chatzinotas A, Harms H. (2003). Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5: 896-907.
28. Hallberg KB, Coupland K, Kimura S, Johnson DB. (2006). Macroscopic streamer growths in acidic, metal-rich mine waters in north Wales consist of novel and remarkably simple bacterial communities. Appl Environ Microbiol 72: 2022-2030.
29. Holmes DE, Finneran KT, O'Neil RA, Lovley DR. (2002). Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Appl Environ Microbiol 68: 2300-2306.
30. Huber T, Faulkner G, Hugenholtz P. (2004). Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
31. Huston MA, DeAngelis DL. (1994). Competition and coexistence: the effects of resource transport and supply rates. Am Nat 144: 954-977.
32. Hwang C, Wu WM, Gentry TJ, Carley J, Carroll SL, Schadt C et al. (2006). Changes in bacterial community structure correlate with initial operating conditions of a field-scale denitrifying fluidized bed reactor. Appl Microbiol Biotechnol 71: 748-760.
33. Iwamoto T, Nasu M. (2001). Current bioremediation practice and perspective. J Biosci Bioeng 92: 1-8.
34. Kassen R, Rainey PB. (2004). The ecology and genetics of microbial diversity. Ann Rev Microbiol 58: 207-231.
35. Kent AD, Yannarell AC, Rusak J A, Triplett EW, McMahon KD. (2007). Synchrony in aquatic microbial community dynamics. ISME J 1: 38-47.
36. Kim JJ, Kim SJ, Tazaki K. (2002). Mineralogical characterization of microbial ferrihydrite and schwertmannite and non-biogenic Al-sulfate precipitates from acidmine drainage in the Donghae mine area, Korea. Environ Geol 42: 19-31.
37. Lawton JH, Naeem S, Thompson LJ, Hector A, Crawley MJ. (1998). Biodiversity and ecosystem function: getting the Ecotron experiment in its correct context. Fund Ecol 12: 848-852.
38. Lloyd JR. (2003). Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27: 411-425.
39. Lozupone CA, Hamady M, Kelley ST, Knight R. (2007). Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73: 1576-1585.
40. Luo J, Wu W, Fienen MN, Jardine PM, Mehlhom TL, Watson DB et al. (2006). A nested-cell approach for in situ remediation. Ground Water 44: 266-274.
41. Luo J, Wu WM, Carley J, Ruan C, Gu B, Jardine PM et al. (2007). Hydraulic performance analysis of a multiple injection-extraction well system. J Hydrol 336: 294-302.
42. Madden AS, Smith AC, Balkwill DL, Fagan LA, Phelps TJ. (2007). Microbial uranium immobilization independent of nitrate reduction. Environ Microbiol 9: 2321-2330.
43. Michalsen MM, Peacock AD, Spain AM, Smithgal AN, White DC, Sanchez-Rosario Y et al. (2007). Changes in microbial community composition and geochemistry during uranium and technetium bioimmobilization. Appl Environ Microbiol 73: 5885-5896.
44. Muylaert K, Sabbe K, Vyverman W. (2000). Spatial and temporal dynamics of phytoplankton communities in a freshwater tidal estuary (Schelde, Belgium). Estuar Coast Shelf Sci 50: 673-678.
45. Nevin KP, Finneran KT, Lovley DR. (2003). Microorganisms associated with uranium bioremediation in a high-salinity subsurface sediment. Appl Environ Microbiol 69: 3672-3675.
46. North NN, Dollhopf SL, Petrie L, Istok JD, Balkwill DL, Kostka JE. (2004). Change in bacterial community structure during in situ biostimulation of subsurface sediment cocontaminated with uranium and nitrate. Appl Environ Microbiol 70: 4911-4920.
47. Palmer MW. (1993). Putting things in even better order: the advantages of canonical correspondence analysis. Ecology 74: 2215-2230.
48. Petrie L, North NN, Dollhopf SL, Balkwill DL, Kostka JE. (2003). Enumeration and characterization of iron(III)- reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI). Appl Environ Microbiol 69: 7467-7479.
49. Pringault O, Duran R, Jacquet S, Torréton JP. (2007). Temporal variations of microbial activity and diversity in marine tropical sediments (New Caledonia Lagoon). Microb Ecol 55: 247-258.
50. Ramette A. (2007). Multivariate analyses in microbial ecology. Minireview. FEMS Microbiol Ecol 62: 142-160.
51. Rubin MA, Leff LG. (2007). Nutrients and other abiotic factors affecting bacterial communities in an Ohio River (USA). Microb Ecol 54: 374-383.
52. Sapp M, Wichels A, Wiltshire KH, Gerdts G. (2007). Bacterial community dynamics during the winterspring transition in the North Sea. FEMS Microbiol Ecol 59: 622-637.
53. Schloss PD, Handelsman J. (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501-1506.
54. Suzuki Y, Kelly SD, Kemner KM, Banfield JF. (2003). Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment. Appl Environ Microbiol 69: 1337-1346.
55. 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.
56. ter Braak CJF, Smilauer P. (2002). CANOCO Reference Manual and CanoDraw for Windows Users Guide: Software for Canonical Community Ordination (v. 4.5). Microcomputer Power: Ithaca, NY.
57. Thompson JD, Higgins DG, Gibson TJ. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weigh matrix choice. Nucleic Acids Res 22: 4673-4680.
58. Tilman D, Wedin D, Knops J. (1996). Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379: 718-720.
59. Titeux N, Dufrene M, Jacob JP, Paquay M, Defourny P. (2004). Multivariate analysis of a fine-scale breeding bird atlas using a geographical information system and partial canonical correspondence analysis: environmental and spatial effects. J Biogeogr 31: 1841-1856.
60. Vrionis HA, Anderson RT, Ortiz-Bernad I, O'Neill KR, Resch CT, Peacock AD et al. (2005). Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site. Appl Environ Microbiol 71: 6308-6318.
61. Wu WM, Carley J, Fienen M, Mehlhorn T, Lowe K, Nyman J et al. (2006a). Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer 1: conditioning of a treatment zone. Environ Sci Technol 40: 3978-3985.
62. Wu WM, Carley J, Gentry T, Ginder-Vogel MA, Fienen M, Mehlhorn T et al. (2006b). Pilot-scale in situ remediation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability. Environ Sci Technol 40: 3986-3995.
63. Wu WM, Carley J, Luo J, Ginder-Vogel MA, Cardenas E, Leigh MB et al. (2007). In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ Sci Technol 41: 5716-5723.
64. Yan T, Fields MW, Wu L, Zu Y, Tiedje JM, Zhou J. (2003). Molecular diversity and characterization of nitrite reductase gene fragments (nirK and nirS) from nitrateand uranium-contaminated groundwater. Environ Microbiol 5: 13-24.
65. Yannarell AC, Triplett EW. (2005). Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71: 227-239.
66. Zhou J, Bruns MA, Tiedje JM. (1996). DNA recovery from soils of diverse composition. Appl Environ Microbiol 62: 316-322.