Denitrifying bacteria from the genus Rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site

Applied and Environmental Microbiology

Volumn 78, Issue 4, 2012, Pages 1039-1047

  Green, Stefan J ^a,b   Prakash, Om ^a   Jasrotia, Puja ^a   Overholt, Will A ^a   Cardenas, Erick ^c   Hubbard, Daniela ^a,e   Tiedje, James M ^c   Watson, David B ^d   Schadt, Christopher W ^d   Brooks, Scott C ^d   Kostka, Joel E ^a,f  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e SEQUENOM INC   (United States)

^f GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL COMMUNITY; BACTERIAL COMMUNITY STRUCTURE; COMMUNITY COMPOSITION; CONTAMINATED AREAS; DENITRIFIERS; DENITRIFYING BACTERIA; FIELD RESEARCH; FIELD SCALE; FINGERPRINTING ANALYSIS; GAMMAPROTEOBACTERIA; HIGH-THROUGHPUT; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY STRUCTURES; MOLECULAR TOOLS; NITRITE REDUCTASE GENES; NITROGEN SPECIES; NUCLEAR LEGACY; OXYGEN LEVELS; QUANTITATIVE PCR; RELATIVE ABUNDANCE; RRNA GENES; SUBSURFACE CONDITIONS; SUBSURFACE ENVIRONMENT; SUBSURFACE SEDIMENTS;

ANOXIC SEDIMENTS; CONTAMINATION; DENITRIFICATION; GENE ENCODING; GROUNDWATER; POLYMERASE CHAIN REACTION; POPULATION DISTRIBUTION; RADIOACTIVE WASTES; RNA; SOCIAL SCIENCES; URANIUM;

BACTERIA;

BACTERIAL DNA; BACTERIAL RNA; GROUND WATER; NITROGEN; OXYGEN;

BACTERIUM; COMMUNITY COMPOSITION; DENITRIFICATION; MICROBIAL COMMUNITY; NITRATE; PH; RADIOACTIVE WASTE; SAMPLING; URANIUM;

ARTICLE; BIOTA; CHEMISTRY; CLASSIFICATION; DENITRIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; METAGENOME; METAGENOMICS; METHODOLOGY; MICROBIOLOGY; PH; RADIOACTIVE WASTE; SOIL POLLUTANT; XANTHOMONADACEAE;

BIOTA; DENITRIFICATION; DNA, BACTERIAL; GROUNDWATER; HYDROGEN-ION CONCENTRATION; METAGENOME; METAGENOMICS; NITROGEN; OXYGEN; RADIOACTIVE WASTE; RNA, BACTERIAL; SOIL POLLUTANTS, RADIOACTIVE; XANTHOMONADACEAE;

OAK RIDGE RESERVATION; TENNESSEE; UNITED STATES;

BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; RHODANOBACTER;

EID: 84857097221     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06435-11     Document Type: Article

References (56)

1. Akob DM, et al. 2008. Functional diversity and electron donor dependence of microbial populations capable of U(VI) reduction in radionuclide-contaminated subsurface sediments. Appl. Environ. Microbiol. 74:3159-3170.
2. Akob DM, Mills HJ, Kostka JE. 2007. Metabolically active microbial communities in uranium-contaminated subsurface sediments. FEMS Microbiol. Ecol. 59:95-107.
3. Altschul SF, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. An DS, Lee HG, Lee ST, Im WT. 2009. Rhodanobacter ginsenosidimutans sp. nov., isolated from soil of a ginseng field in South Korea. Int. J. Syst. Evol. Microbiol. 59:691-694.
5. Anderson RT. 2006. DOE genomics: applications to in situ subsurface bioremediation. Remediat. J. 17:23-38.
6. Anderson RT, et al. 2003. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uraniumcontaminated aquifer. Appl. Environ. Microbiol. 69:5884-5891.
7. Bollmann A, Palumbo AV, Lewis K, Epstein SS. 2010. Isolation and physiology of bacteria from contaminated subsurface sediments. Appl. Environ. Microbiol. 76:7413-7419.
8. Bower CE, Holm-Hansen T. 1980. A salicylate-hypochlorite method for determining ammonia in seawater. Can. J. Fish. Aquat. Sci. 37:794-798.
9. Braman RS, Hendrix SA. 1989. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium(III) reduction with chemiluminescence detection. Anal. Chem. 61:2715-2718.
10. Bui TP, Kim YJ, Kim H, Yang DC. 2010. Rhodanobacter soli sp. nov., isolated from soil of a ginseng field. Int. J. Syst. Evol. Microbiol. 60:2935-2939.
11. Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EA. 2010. The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ. Microbiol. 12:1842-1854.
12. Cardenas E, et al. 2008. Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl. Environ. Microbiol. 74:3718-3729.
13. Cardenas E, et al. 2010. Significant association between sulfate-reducing bacteria and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach. Appl. Environ. Microbiol. 76:6778-6786.
14. Chapelle FH. 2000. The significance of microbial processes in hydrogeology and geochemistry. Hydrogeol. J. 8:41-46.
15. Chin KJ, Sharma ML, Russell LA, O'Neill KR, Lovley DR. 2008. Quantifying expression of a dissimilatory (bi)sulfite reductase gene in petroleum-contaminated marine harbor sediments. Microb. Ecol. 55: 489-499.
16. Clarke KR, Warwick RM. 2001. Change in marine communities: an approach to statistical analysis and interpretation. Primer-E, Lutton, United Kingdom.
17. Cole JR, et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141- D145.
18. De Clercq D, et al. 2006. Rhodanobacter spathiphylli sp. nov., a gammaproteobacterium isolated from the roots of Spathiphyllum plants grown in a compost-amended potting mix. Int. J. Syst. Evol. Microbiol. 56:1755-1759.
19. DeSantis TZ, et al. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microb. 72:5069-5072.
20. DeSantis TZ, Jr, et al. 2006. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 34:W394- W399.
21. Friedrich U, Naismith MM, Altendorf K, Lipski A. 1999. Community analysis of biofilters using fluorescence in situ hybridization including a new probe for the Xanthomonas branch of the class Proteobacteria. Appl. Environ. Microbiol. 65:3547-3554.
22. Garside C. 1982. A chemiluminescent technique for the determination of nanomolar concentrations of nitrate, nitrite, or nitrite alone in seawater. Mar. Chem. 11:159-167.
23. Gentile ME, Lynn Nyman J, Criddle CS. 2007. Correlation of patterns of denitrification instability in replicated bioreactor communities with shifts in the relative abundance and the denitrification patterns of specific populations. ISME J. 1:714-728.
24. Goldscheider N, Hunkeler D, Rossi P. 2006. Review: microbial biocenoses in pristine aquifers and an assessment of investigative methods. Hydrogeol. J. 14:926-941.
25. Green SJ, et al. 2010. Denitrifying bacteria from the terrestrial subsurface exposed to mixed waste contamination. Appl. Environ. Microbiol. 76: 3244-3254.
26. Griebler C, Lueders T. 2009. Microbial biodiversity in groundwater ecosystems. Freshwater Biol. 54:649-677.
27. Hemme CL, et al. 2010. Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J. 4:660-672.
28. Hwang CC, et al. 2009. Bacterial community succession during in situ uranium bioremediation: spatial similarities along controlled flow paths. ISME J. 3:47-64.
29. Im WT, Lee ST, Yokota A. 2004. Rhodanobacter fulvus sp. nov., a betagalactosidase-producing gammaproteobacterium. J. Gen. Appl. Microbiol. 50:143-147.
30. Istok JD, et al. 2004. In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environ. Sci. Technol. 38:468-475.
31. Kostka JE, Green SJ. 2011. Microorganisms and processes linked to uranium reduction and immobilization, p 117-138. In Stolz JF, Oremland RS (ed), Microbial metal and metalloid metabolism: advances and applications. ASM Press, Washington, DC.
32. Lee CS, Kim KK, Aslam Z, Lee ST. 2007. Rhodanobacter thiooxydans sp. nov., isolated from a biofilm on sulfur particles used in an autotrophic denitrification process. Int. J. Syst. Evol. Microbiol. 57:1775-1779.
33. Löffler FE, Edwards EA. 2006. Harnessing microbial activities for environmental cleanup. Curr. Opin. Biotechnol. 17:274-284.
34. Lozupone C, Hamady M, Knight R. 2006. UniFrac: an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371.
35. Lozupone C, Knight R. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228-8235.
36. Ludwig W, Klenk HP. 2001. Overview: a phylogenetic backbone and taxonomic framework for prokaryotic systematics, p 49-65. In Garrity G (ed), Bergey's manual of systematic bacteriology, 2nd ed. Springer, New York, NY.
37. Ludwig W, et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
38. Martinez RJ, et al. 2006. Horizontal gene transfer of PIB-type ATPases among bacteria isolated from radionuclide- and metal-contaminated subsurface soils. Appl. Environ. Microbiol. 72:3111-3118.
39. Nadkarni MA, Martin FE, Jacques NA, Hunter N. 2002. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257-266.
40. Nalin R, Simonet P, Vogel TM, Normand P. 1999. Rhodanobacter lindaniclasticus gen. nov., sp. nov., a lindane-degrading bacterium. Int. J. Syst. Bacteriol. 49(Pt 1):19-23.
41. Napier JM, Bustamante RB. 1988. In situ biodenitrification of the S-3 ponds. Environ. Prog. Sustain. Energ. 7:13-16.
42. Prakash O, et al. 25 November 2011. Description of Rhodanobacter denitrificans sp. nov., isolated from nitrate-rich zones of a contaminated aquifer. Int. J. Syst. Evol. Microbiol. [Epub ahead of print.] doi:10.1099/ ijs.0.035840-0.
43. Ramette A. 2007. Multivariate analyses in microbial ecology. FEMS Microbiol. Ecol. 62:142-160.
44. Riley RG, Zachara JM. 1992. Chemical contaminants on DOE lands and selection of contaminant mixtures for subsurface research, report no. DOE/ER-0547T. Office of Energy Research, Subsurface Science Program, US Department of Energy, Washington, DC.
45. Roesch LF, et al. 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1:283-290.
46. Ryan TA, Joiner BL. 1976. Normal probability plots and tests for normality. The Pennsylvania State University, University Park, PA.
47. Spain AM, et al. 2007. Identification and isolation of a Castellaniella species important during biostimulation of an acidic nitrate- and uranium-contaminated aquifer. Appl. Environ. Microbiol. 73:4892-4904.
48. Tiedje J. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium, p 179-244. In Zehnder AJB (ed), Biology of anaerobic microorganisms. John Wiley & Sons, New York, NY.
49. van den Heuvel RN, van der Biezen E, Jetten MS, Hefting MM, Kartal B. 2010. Denitrification at pH 4 by a soil-derived Rhodanobacterdominated community. Environ. Microbiol. 12:3264-3271.
50. Wang L, et al. 2011. Rhodanobacter panaciterrae sp. nov., with ginsenoside converting activity isolated from soil of a ginseng field. Int. J. Syst. Evol. Microbiol. 61(Pt 12):3028-3032.
51. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
52. Watson DB, Kostka JE, Fields MW, Jardine PM. 2004. The Oak Ridge Field Research Center conceptual model. NABIR Field Research Center Report, Oak Ridge, TN. http://public.ornl.gov/orifc/FRC-conceptual -model.pdf.
53. Weon HY, et al. 2007. Rhodanobacter ginsengisoli sp. nov. and Rhodanobacter terrae sp. nov., isolated from soil cultivated with Korean ginseng. Int. J. Syst. Evol. Microbiol. 57:2810-2813.
54. Wu WM, et al. 2006. Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 1. Conditioning of a treatment zone. Environ. Sci. Technol. 40:3978-3985.
55. Wu WM, et al. 2010. Effects of nitrate on the stability of uranium in a bioreduced region of the subsurface. Environ. Sci. Technol. 44:5104-5111.
56. Zhang J, et al. 2011. Rhodanobacter xiangquanii sp. nov., a novel anilofosdegrading bacterium isolated from a wastewater treating system. Curr. Microbiol. 62:645-649.