Dynamic Microbial Community Associated with Iron-Arsenic Co-Precipitation Products from a Groundwater Storage System in Bangladesh

Microbial Ecology

Volumn 64, Issue 1, 2012, Pages 171-186

  Gorra, Roberta ^a,b   Webster, Gordon ^b,c   Martin, Maria ^a   Celi, Luisella ^a   Mapelli, Francesca ^d   Weightman, Andrew J ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL DNA; ARSENIC; BACTERIAL DNA; GROUND WATER; IRON; RNA 16S;

ARCHAEON; ARTICLE; BACTERIUM; BANGLADESH; CHEMISTRY; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY;

ARCHAEA; ARSENIC; BACTERIA; BANGLADESH; DNA, ARCHAEAL; DNA, BACTERIAL; GROUNDWATER; IRON; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S;

ARCHAEA; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; EURYARCHAEOTA; GALLIONELLA; PROKARYOTA;

EID: 84862494678     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-012-0014-1     Document Type: Article

References (76)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic Local Alignment Search Tool. J Mol Biol 215: 403-410.
2. Anthony C (1982) The biochemistry of methylotrophs. Academic, New York.
3. Araujo JC, Teran FC, Oliveira RA, Nour EAA, Montenegro MAP, Campos JR, Vazoller RF (2003) Comparison of hexamethyidisilazane and critical point drying treatments for SEM analysis of anaerobic biofilms and granular sludge. J Electron Microsc 52: 429-433.
4. Banning N, Brock F, Fry JC, Parkes RJ, Hornibrook ERC, Weightman AJ (2005) Investigation of the methanogen population structure and activity in a brackish lake sediment. Environ Microbiol 7: 947-960.
5. Battaglia-Brunet F, Itard Y, Garrido F, Delorme F, Crouzet C, Greffie C, Joulian C (2006) A simple biogeochemical process removing arsenic from a mine drainage water. Geomicrobiol J 23: 201-211.
6. BGS, DPHE (2001) Arsenic contamination of groundwater in Bangladesh. In: Kinniburgh, DG, Smedley, P. L. (ed.) British Geological Survey (Technical Report, WC/00/19). British Geological Survey, Keyworth.
7. Borrel G, Lehours AC, Bardot C, Bailly X, Fonty G (2010) Members of candidate divisions OP11, OD1 and SR1 are widespread along the water column of the meromictic Lake Pavin (France). Arch Microbiol 192: 559-567.
8. Brosius J, Dull TJ, Sleeter DD, Noller HF (1981) Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J Mol Biol 148: 107-127.
9. Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personne JC (2006) Diversity of microorganisms in Fe-As-rich acid mine drainage waters of Carnoules, France. Appl Environ Microbiol 72: 551-556.
10. Cadillo-Quiroz H, Brauer S, Yashiro E, Sun C, Yavitt J, Zinder S (2006) Vertical profiles of methanogenesis and methanogens in two contrasting acidic peatlands in central New York State, USA. Environ Microbiol 8: 1428-1440.
11. Celi L, Schnitzer M, Negre M (1997) Analysis of carboxyl groups in soil humic acids by a wet chemical method, Fourier-transform infrared spectrophotometry, and solution-state carbon-13 nuclear magnetic resonance. A comparative study. Soil Sci 162: 189-197.
12. Cerli C, Celi L, Kaiser K, Guggenberger G, Johansson MB, Cignetti A, Zanini E (2008) Changes in humic substances along an age sequence of Norway spruce stands planted on former agricultural land. Org Geochem 39: 1269-1280.
13. Conrad R, Klose M, Noll M, Kemnitz D, Bodelier PLE (2008) Soil type links microbial colonization of rice roots to methane emission. Glob Chang Biol 14: 657-669.
14. Cummings DE, Caccavo F, Fendorf S, Rosenzweig RF (1999) Arsenic mobilization by the dissimilatory Fe(III)-reducing bacterium Shewanella alga BrY. Environ Sci Technol 33: 723-729.
15. Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89: 5685-5689.
16. Emerson D, Revsbech NP (1994) Investigation of an iron-oxidizing microbial mat community located near Aarhus, Denmark: laboratory studies. Appl Environ Microbiol 60: 4032-4038.
17. Gault AG, Islam FS, Polya DA, Charnock JM, Boothman C, Chatterjee D, Lloyd JR (2005) Microcosm depth profiles of arsenic release in a shallow aquifer, West Bengal. Mineral Mag 69: 855-863.
18. Geets J, Borrernans B, Diels L, Springael D, Vangronsveld J, van der Lelie D, Vanbroekhoven K (2006) DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria. J Microbiol Methods 66: 194-205.
19. Grosskopf R, Stubner S, Liesack W (1998) Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl Environ Microbiol 64: 4983-4989.
20. Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW, Saunders JR (1996) Isolation and identification of methanogen-specific DNA from blanket bog feat by PCR amplification and sequence analysis. Appl Environ Microbiol 62: 668-675.
21. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
22. Hanert HH (2006) The genus Gallionella. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, vol. 7. Springer, New York, pp 990-995.
23. Harris JK, Kelley ST, Pace NR (2004) New perspective on uncultured bacterial phylogenetic division OP11. Appl Environ Microbiol 70: 845-849.
24. Harvey CF, Swartz CH, Badruzzaman ABM, Keon-Blute N, Yu W, Ali MA, Jay J, Beckie R, Niedan V, Brabander D, Oates PM, Ashfaque KN, Islam S, Hemond HF, Ahmed MF (2002) Arsenic mobility and groundwater extraction in Bangladesh. Science 298: 1602-1606.
25. Henckel T, Friedrich M, Conrad R (1999) Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Appl Environ Microbiol 65: 1980-1990.
26. Hering JG, Kneebone PE (2002) Biogeochemical controls on arsenic occurrence and mobility in water supplies. In: Frankenberger WT (ed) Environmental chemistry of arsenic. Marcel Dekker, New York, pp 155-180.
27. Hery M, van Dongen BE, Gill F, Mondal D, Vaughan DJ, Pancost RD, Polya DA, Lloyd JR (2010) Arsenic release and attenuation in low organic carbon aquifer sediments from West Bengal. Geobiology 8: 155-168.
28. Hong S, Bunge J, Leslin C, Jeon S, Epstein SS (2009) Polymerase chain reaction primers miss half of rRNA microbial diversity. ISME 3: 1365-1373.
29. Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
30. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180: 366-376.
31. Islam FS, Gault AG, Boothman C, Polya DA, Charnock JM, Chatterjee D, Lloyd JR (2004) Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430: 68-71.
32. Kalbitz K, Kaiser K (2008) Contribution of dissolved organic matter to carbon storage in forest mineral soils. J Plant Nutr Soil Sci-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 171: 52-60.
33. Kappler A, Straub KL (2005) Geomicrobiological cycling of iron. Rev Mineral Geochem 59: 85-108.
34. Katsoyiannis IA, Zouboulis AI (2004) Application of biological processes for the removal of arsenic from groundwaters. Water Res 38: 17-26.
35. Kennedy CB, Scott SD, Ferris FG (2003) Ultrastructure and potential sub-seafloor evidence of bacteriogenic iron oxides from axial volcano, Juan de Fuca Ridge, North-east Pacific Ocean. FEMS Microbiol Ecol 43: 247-254.
36. Kogel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34: 139-162.
37. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115-175.
38. Lear G, Song B, Gault AG, Polya DA, Lloyd JR (2007) Molecular analysis of arsenate-reducing bacteria within Cambodian sediments following amendment with acetate. Appl Environ Microbiol 73: 1041-1048.
39. Li H, Zhang Y, Li DS, Xu H, Chen GX, Zhang CG (2009) Comparisons of different hypervariable regions of rrs genes for fingerprinting of microbial communities in paddy soils. Soil Biol Biochem 41: 954-968.
40. Lidstrom ME (2006) Aerobic methylotrophic prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, vol. 1. Springer, New York, pp 618-634.
41. Liu D, Dong H, Bishop ME, Wang H, Agrawal A, Tritschler S, Eberl DD, Xie S (2011) Reduction of structural Fe(III) in nontronite by methanogen Methanosarcina barkeri. Geochim Cosmochim Acta 75: 1057-1071.
42. Lockhart PJ, Steel MA, Hendy MD, Penny D (1994) Recovering evolutionary trees under a more realistic model of sequence evolution. Mol Biol Evol 11: 605-612.
43. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology-Sgm 148: 3521-3530.
44. Macur RE, Jackson CR, Botero LM, McDermott TR, Inskeep WP (2004) Bacterial populations associated with the oxidation and reduction of arsenic in an unsaturated soil. Environ Sci Technol 38: 104-111.
45. Meyer J, Michalke K, Kouril T, Hensel R (2008) Volatilisation of metals and metalloids: an inherent feature of methanoarchaea? Syst Appl Microbiol 31: 81-87.
46. Mukhopadhyay R, Rosen BP, Pung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26: 311-325.
47. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16 s ribosomal-RNA. Appl Environ Microbiol 59: 695-700.
48. Neubauer SC, Emerson D, Megonigal JP (2002) Life at the energetic edge: kinetics of circumneutral iron oxidation by lithotrophic iron-oxidizing bacteria isolated from the wetland-plant rhizosphere. Appl Environ Microbiol 68: 3988-3995.
49. Neumann RB, Ashfaque KN, Badruzzaman ABM, Ali MA, Shoemaker JK, Harvey CF (2010) Anthropogenic influences on groundwater arsenic concentrations in Bangladesh. Nat Geosci 3: 46-52.
50. Nicol GW, Glover LA, Prosser JI (2003) The impact of grassland management on archaeal community structure in upland pasture rhizosphere soil. Environ Microbiol 5: 152-162.
51. Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55: 892-895.
52. Ohnuki T, Sakamoto F, Kozai N, Ozaki T, Yoshida T, Narumi I, Wakai E, Sakai T, Francis AJ (2004) Mechanisms of arsenic immobilization in a biomat from mine discharge water. Chem Geol 212: 279-290.
53. Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300: 939-944.
54. Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13: 45-49.
55. O'Sullivan LA, Webster G, Fry JC, Parkes RJ, Weightman AJ (2008) Modified linker-PCR primers facilitate complete sequencing of DGGE DNA fragments. J Microbiol Methods 75: 579-581.
56. Ovreas L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63: 3367-3373.
57. Roberts LC, Hug SJ, Dittmar J, Voegelin A, Saha GC, Ali MA, Badruzzanian ABM, Kretzschniar R (2007) Spatial distribution and temporal variability of arsenic in irrigated rice fields in Bangladesh. 1. Irrigation water. Environ Sci Technol 41: 5960-5966.
58. Silver S, Phung LT (2005) A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotechnol 32: 587-605.
59. Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17: 517-568.
60. Sobolev D, Roden EE (2002) Evidence for rapid microscale bacterial redox cycling of iron in circumneutral environments. Antonie van Leeuwenhoek 81: 587-597.
61. Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol 74: 6663-6671.
62. Straub KL, Benz M, Schink B, Widdel F (1996) Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl Environ Microbiol 62: 1458-1460.
63. Sultana M, Haertig C, Planer-Friedrich B, Seifert J, Schloemann M (2011) Bacterial communities in Bangladesh aquifers differing in aqueous arsenic concentration. Geomicrobiol J 28: 198-211.
64. Sutton NB, van der Kraan GM, van Loosdrecht MCM, Muyzer G, Bruining J, Schotting RJ (2009) Characterization of geochemical constituents and bacterial populations associated with As mobilization in deep and shallow tube wells in Bangladesh. Water Res 43: 1720-1730.
65. 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.
66. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
67. Violante A, Del Gaudio S, Pigna M, Ricciardella M, Banerjee D (2007) Coprecipitation of arsenate with metal oxides. 2. Nature, mineralogy, and reactivity of iron(III) precipitates. Environ Sci Technol 41: 8275-8280.
68. Violante A, Krishnamurti GSR, Huang PM (2002) Impact of organic substances on the formation and trasformation of metal oxides in soil environments. In: Huang PM, Bollag JM, Senesi N (eds) Interactions between soil particles and microorganisms. Wiley, Chichester, UK, pp 133-171.
69. Wagner M, Roger AJ, Flax JL, Brusseau GA, Stahl DA (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J Bacteriol 180: 2975-2982.
70. Wang JJ, Muyzer G, Bodelier PLE, Laanbroek HJ (2009) Diversity of iron oxidizers in wetland soils revealed by novel 16S rRNA primers targeting Gallionella-related bacteria. ISME J 3: 715-725.
71. Webster G, Newberry CJ, Fry JC, Weightman AJ (2003) Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J Microbiol Methods 55: 155-164.
72. Webster G, Parkes RJ, Cragg BA, Newberry CJ, Weightman AJ, Fry JC (2006) Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru Margin. FEMS Microbiol Ecol 58: 65-85.
73. Webster G, Sass H, Cragg BA, Gorra R, Knab NJ, Green CJ, Mathes F, Fry JC, Weightman AJ, Parkes RJ (2011) Enrichment and cultivation of prokaryotes associated with the sulphate-methane transition zone of diffusion-controlled sediments of Aarhus Bay, Denmark, under heterotrophic conditions. FEMS Microbiol Ecol 77: 248-263.
74. Webster G, Yarram L, Freese E, Koester J, Sass H, Parkes RJ, Weightman AJ (2007) Distribution of candidate division JS1 and other Bacteria in tidal sediments of the German Wadden Sea using targeted 16S rRNA gene PCR-DGGE. FEMS Microbiol Ecol 62: 78-89.
75. Wu ZJ, Yuan LX, Jia N, Wang YH, Sun LG (2009) Microbial biomineralization of iron seepage water: implication for the iron ores formation in intertidal zone of Zhoushan Archipelago, East China Sea. Geochem J 43: 167-177.
76. Zhou JZ, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62: 316-322.