Arsenic release from shallow aquifers of the Hetao basin, Inner Mongolia: evidence from bacterial community in aquifer sediments and groundwater

Ecotoxicology

Volumn 23, Issue 10, 2014, Pages 1900-1914

  Li, Yuan ^a,b   Guo, Huaming ^a,b   Hao, Chunbo ^b  

^a CHINA UNIVERSITY OF GEOSCIENCES   (China)

^b CHINA UNIVERSITY OF GEOSCIENCES   (China)

Author keywords

16S rRNA; Clone library; DGGE; Groundwater; High arsenic; Sediment

Indexed keywords

ARSENIC; BACTERIAL DNA; DNA FRAGMENT; GROUND WATER; IRON OXIDE; NATURAL ORGANIC MATTER; ORGANIC CARBON; RNA 16S; WATER POLLUTANT;

AQUIFER; ARSENIC; BACTERIUM; CLONE; COMMUNITY STRUCTURE; ELECTROKINESIS; GROUNDWATER; MICROBIAL COMMUNITY; MOBILIZATION; RNA; SEDIMENT;

16S RRNA GENE; ANAEROBIC BACTERIUM; AQUIFER; ARSENIC REDUCING BACTERIUM; ARTICLE; BACTERIAL STRAIN; BACTERIAL STRUCTURES; BIOGEOCHEMICAL CYCLING; CHEMICAL COMPOSITION; COMMUNITY STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DENATURATION; DENATURING GRADIENT GEL ELECTROPHORESIS; DIETZIA; DISSOLUTION; DNA LIBRARY; ELECTRON ACCELERATOR; GENETIC SIMILARITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INTRODUCED SPECIES; LIFE EXTENSION; MASS SPECTROMETRY; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROCOSM; MOLECULAR CLONING; MONGOLIA; NITRITE REDUCING BACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISMS BY METABOLISM; OXIDATION REDUCTION POTENTIAL; PHYLOGENY; PHYSICAL CHEMISTRY; POLYMERASE CHAIN REACTION; PSEUDOMONAS; RHODOCOCCUS; SEDIMENT; SEQUENCE ANALYSIS; SULFATE REDUCING BACTERIUM; WATER CONTAMINATION; ANALYSIS; BACTERIA; CHEMISTRY; CHINA; ENVIRONMENTAL MONITORING; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; WATER POLLUTANT;

CHINA; HETAO BASIN; NEI MONGGOL;

BACTERIA (MICROORGANISMS);

ARSENIC; BACTERIA; CHINA; ENVIRONMENTAL MONITORING; GEOLOGIC SEDIMENTS; GROUNDWATER; WATER POLLUTANTS, CHEMICAL;

EID: 84911808035     PISSN: 09639292     EISSN: 15733017     Source Type: Journal    
DOI: 10.1007/s10646-014-1313-8     Document Type: Article

References (92)

1. Achour AR, Bauda P, Billard P (2007) Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res Microbiol 158:128–137
2. Afkar E, Lisak J, Saltikov C, Basu P, Oremland RS, Stolz JF (2003) The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiol Lett 226:107–112
3. Ahmann D, Krumholz LR, Hemond HF, Lovley DR, Morel FMM (1997) Microbial mobilization of arsenic from sediments of the Aberjona watershed. Environ Sci Technol 31:2923–2930
4. Akai J, Izumi K, Fukuhara H, Masuda H, Nakano S, Yoshimura T, Ohfuji H, Anawar HM, Akai K (2004) Mineralogical and geomicrobiological investigations on groundwater arsenic enrichment in Bangladesh. Appl Geochem 19:215–230
5. Akai J, Kanekiyo A, Hishida N, Ogawa M, Naganuma T, Fukuhara H, Anawar HN (2008) Biogeochemical characterization of bacterial assemblages in relation to release of arsenic from South East Asia (Bangladesh) sediments. Appl Geochem 23:3177–3186
6. Anawar HM, Akai J, Yoshioka T, Konohira E, Lee JY, Fukuhara H, Alam MTK, Garcia-Sanchez A (2006) Mobilization of arsenic in groundwater of Bangladesh: evidence from an incubation study. Environ Geochem Health 28:553–565
7. Anderson CR, Cook GM (2004) Isolation and characterization of arsenate-reducing bacteria from arsenic-contaminated sites in New Zealand. Curr Microbiol 48:341–347
8. Andrews SC (1998) Iron storage in bacteria. Adv Microb Physiol 40:281–351
9. Bhattacharya P, Chatterjee D, Jacks G (1997) Occurrence of arsenic contaminated groundwater in alluvial aquifers from Delta Plains, eastern India: options for safe drinking water supply. Int J Water Res Dev 13:79–92
10. Bhattacharya P, Jacks G, Jana J, Sracek A, Gustafsson JP, Chatterjee D (2001) Geochemistry of the Holocene alluvial sediments of Bengal Delta Plain from West Bengal, India; Implications on arsenic contamination in groundwater. In: Jacks G, Bhattacharya P, Khan AA (eds) Groundwater arsenic contamination in the Bengal Delta Plain of Bangladesh. Proceedings of the KTH-Dhaka University Seminar. KTH Special Publication, TRITA-AMI Report 3084, pp 21–40
11. Bissen M, Frimmel FH (2003) Arsenic-a review. Part II. Oxidation of arsenic and its removal in water treatment. Acta Hydrochim Hydrobiol 31:97–107
12. Braun V, Braun M (2002) Active transport of iron and siderophore antibiotics. Curr Opin Microbiol 5:194–201
13. Braun V, Killmann H (1999) Bacterial solutions to the iron-supply problem. Trends Biochem Sci 24:104–109
14. Cai L, Liu GH, Rensing C, Wang G (2009) Genes involved in arsenic transformation and resistance associated with different levels of arsenic-contaminated soils. BMC Microbiol 9:4–10
15. Chang JS, Yoon IH, Kim KW (2007) Isolation and ars detoxification of arsenite-oxidizing bacteria from abandoned arsenic-contaminated mines. J Microbiol Biotechnol 17:812–821
16. Colquhoun JA, Mexson J, Goodfellow M, Ward AC, Horikoshi K, Bull AT (1998) Novel Rhodococci and other Mycolate actinomycetes from the deep sea. Antonie Van Leeuwenhoek 74:27–40
17. Cummings DE, Caccavo F Jr, Fendorf S, Rosenzweig RF (1999) Arsenic mobilization by the dissimilatory Fe(III)-reducing bacterium Shewanella alga BrY. Environ Sci Technol 33:723–729
18. Das D, Samanta G, Mandal BK et al (1996) Arsenic in groundwater in six districts of West Bengal, India. Environ Geochem Health 18:5–15
19. Deb C, Stackebrandt E, Pradella S, Saha A, Roy P (2004) Phylogenetically diverse new sulfur chemolithotrophs of Alpha-proteobacteria isolated from Indian soils. Curr Microbiol 48:452–458
20. Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89:5685–5689
21. Dick GJ, Lee YE, Tebo BM (2006) Manganese(II)-Oxidizing Bacillus spores in Guaymas basin hydrothermal sediments and plumes. Appl Environ Microbiol 72:3184–3190
22. Dowling CB, Poreda RJ, Basu AR, Peters SL (2002) Geochemical study of arsenic release mechanisms in the Bengal basin groundwater. Water Resour Res 38:1–18
23. Drewniak L, Styczek A, Majder-Lopatka M, Sklodowska A (2008) Bacteria, hypertolerant to arsenic in the rocks of an ancient gold mine, and their potential role in dissemination of arsenic pollution. Environ Pollut 156:1069–1074
24. Drewniak L, Matlakowska R, Rewerski B, Sklodowska A (2010) Arsenic release from gold mine rocks mediated by the activity of indigenous bacteria. Hydrometallurgy 104:437–442
25. Duckworth AW, Grant S, Grant WD, Jones BE, Meijer D (1998) Dietzia natronolimnaios sp. nov., a new member of the genus Dietzia isolated from an East African soda lake. Extremophiles 2:359–366
26. Fauque GD (1995) Ecology of sulfate-reducing bacteria. In: Barton L (ed) sulfate-reducing bacteria. Plenum Press, New York, pp 217–241
27. Finnerty WR (1992) The biology and genetics of the genus Rhodococcus. Annu Rev Microbiol 46:193–218
28. Focardi S, Pepi M, Ruta M, Marvasi M, Bernardini E, Gasperini S, Focardi SE (2010) Arsenic precipitation by an anaerobic arsenic-respiring bacterial strain isolated from the polluted sediments of Orbetello Lagoon, Italy. Lett Appl Microbiol 51:578–585
29. Gounot AM (1994) Microbial oxidation and reduction of manganese: consequences in groundwater and applications. FEMS Microbiol Rev 14:339–349
30. Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48:743–772
31. Guo HM, Yang SZ, Shen ZL (2007) High arsenic groundwater in the world: overview and research perspectives. Adv Earth Sci 22:1109–1117 (In Chinese with English Abstract)
32. Guo HM, Yang SZ, Tang XH, Li Y, Shen ZL (2008a) Groundwater geochemistry and its implications for arsenic mobilization in shallow aquifers of the Hetao basin, Inner Mongolia. Sci Total Environ 393:131–144
33. Guo HM, Tang XH, Yang SZ, Shen ZL (2008b) Effect of indigenous bacteria on geochemical behavior of arsenic in aquifer sediments from the Hetao basin, Inner Mongolia Evidence from sediment incubations. Appl Geochem 23:3267–3277
34. Guo MR, Lin YM, Xu XP, Chen ZL (2010) Bioleaching of iron from kaolin using Fe(III)-reducing bacteria with various carbon nitrogen sources. Appl Clay Sci 48:379–383
35. Guo HM, Zhang B, Zhang Y (2011) Control of organic and iron colloids on arsenic partition and transport in high arsenic groundwaters in the Hetao basin, Inner Mongolia. Appl Geochem 26:360–370
36. Guo HM, Zhang Y, Xing LN, Jia YF (2012) Spatial variation in arsenic and fluoride concentrations of shallow groundwater from the town of Shahai in the Hetao basin, Inner Mongolia. Appl Geochem 27:2187–2196
37. Guo HM, Liu C, Lu H, Wanty RB, Wang J, Zhou YZ (2013) Pathways of coupled arsenic and iron cycling in high arsenic groundwater of the Hetao basin, Inner Mongolia, China: An iron isotope approach. Geochim Cosmochim Acta 112:130–145
38. Guo HM, Wen DG, Liu ZY, Jia YF, Guo Q (2014) A review of high arsenic groundwater in Mainland and Taiwan, China: distribution, characteristics and geochemical processes. Appl Geochem 41:196–217
39. Harvey CF, Swartz CH, Badruzzaman ABM, Keon-Blute N, Yu W, Ali AM, Jay J, Beckie R, Niedan V, Brabander D, Oates PM, Ashfaque KN, Islam S, Hemond Ahmed MF (2002) Arsenic mobility and groundwater extraction in Bangladesh. Science 298(5598):1602–1606
40. Herbel MJ, Fendorf S (2005) Transformation and transport of arsenic within ferric hydroxide coated sands upon dissimilatory reducing bacterial activity. In: O’Day P, Vlassopoulos D, Meng X, Benning L (eds) Advances in arsenic research integration of experimental and observational studies and implications for mitigation ACS symposium series, vol 915. American Chemical Society, Washington DC, pp 77–90
41. Horneman A, van Geen A, Kent DV, Mathe PE, Zheng Y, Dhar RK, O’Connell S, Hoque MA, Aziz Z, Shamsudduha M, Seddique AA, Ahmed KM (2004) Decoupling of As and Fe release to Bangladesh groundwater under reducing conditions. Part I: evidence from sediment profiles. Geochim Cosmochim Acta 68:3459–3473
42. Ishii S, Yamamoto M, Kikuchi M, Oshima K, Hattori M, Otsuka S, Senoo K (2009) Microbial populations responsive to denitrification-inducing conditions in rice paddy soil, as revealed by comparative 16S rRNA gene analysis. Appl Environ Microbiol 75:7070–7078
43. Islam FS, Gault AG, Boothman C, Polya DA, Charnock JM, Chatterjee D, Lloyd JR (2004) Role of metal-reducing bacteria in arsenic release from sediments. Nature 430:68–71
44. Jones BE, Grant WD, Duckworth AW, Owenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2:191–200
45. Kalmbach S, Manz W, Wecke J, Szewzyk U (1999) Aquabacterium gen. nov., with description of Aquabacterium citratiphilum sp. nov., Aquabacteriumparvum sp. nov. and Aquabacteriumcommune sp. nov., three in situ dominant bacterial species from the Berlin drinking water system. Int J Syst Bacteriol 49:769–777
46. Kalyuzhnaya MG, De Marco P, Bowerman S et al (2006) Methyloversatilis universalis gen. nov., sp. nov., a novel taxon within the Betaproteobacteria represented by three methylotrophic isolates. Int J Syst Evol Microbiol 56:2517–2522
47. Klouche N, Fardeau ML, ois Lascourrèges JF et al (2007) Geosporobacter subterraneus gen. nov., sp. nov., a spore-forming bacterium isolated from a deep subsurface aquifer. Int J Syst Evol Microbiol 57:1757–1761
48. Li SF, Li HJ (1994) Study on characteristics and the origin of geological environment in endemic arseniasis area, Hetao, Inner Mongolia. Chinese J Geol Hazard Contr 5:213–219 (in Chinese with English Abstract)
49. Lin MC, Jiang SR, Chou JH, Arun AB, Young CC, Chen WM (2009) Aquabacterium fontiphilum sp. nov., isolated from spring water. Int J Syst Evol Microbiol 59:681–685
50. Lloyd JR (2003) Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425
51. Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJ, Gorby YA, Goodwin S (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
52. Ma YZ, Wu KG, Xia YJ, Yu GJ, Li YH (1995) Epidemiological characteristics of endemic arsenism in Inner Mongolia. Chin J Endem 14:34–36 (In Chinese with English abstract)
53. Macy JM, Santini JM, Pauling BV, O’Neil AH, Sly LI (2000) Two new arsenate/sulfate-reducing bacteria: mechanisms of arsenate reduction. Arch Microbiol 173:49–57
54. McArthur JM, Banerjee DM, Hudson-Edwards KA, Mishra R, Purohit R, Ravenscroft P, Cronin A, Howarth RJ, Chatterjee A, Talukder R, Lowry D, Houghton S, Chadha DK (2004) Natural organic matter in sedimentary basins and its relation to arsenic in anoxic ground water: the example of West Bengal and its worldwide implications. Appl Geochem 19:1255–1293
55. McGuire JT, Long DT, Klug MJ, Haack SK, Hyndman DW (2002) Evaluating behavior of oxygen, nitrate, and sulfate during recharge and quantifying reduction rates in a contaminated aquifer. Environ Sci Technol 36:2693–2700
56. Mukherjee A, Bhattacharya P, Shi F, Fryar AE, Mukherjee AB, Xie ZM, Jacks G, Bundschuh J (2009) Chemical evolution in the high arsenic groundwater of the Huhhot basin (Inner Mongolia, PR China) and its difference from the western Bengal basin (India). Appl Geochem 24:1835–1851
57. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726
58. Newman DK, Kennedy EK, Coates JD, Ahmann D, Ellis DJ, Lovley DR, Morel FMM (1997) Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. Arch Microbiol 168:380–388
59. Nickson R, McArthur J, Burgess W, Ahmed KM, Ravenscroft P, Rahman M (1998) Arsenic poisoning of Bangladesh groundwater. Nature 395:338
60. Nickson R, McArthur J, Ravenscroft P, Burgess WG, Ahmed KM (2000) Mechanism of arsenic release to groundwater, Bangladesh and West Bengal. Appl Geochem 15:403–413
61. Niggemyer A, Spring S, Stakenbrandt E, Rosenzweig RF (2001) Isolation and characterization of a novel As(V)-reducing bacterium: implications for arsenic mobilization and the genus Desuflitobacterium. Appl Environ Microbiol 67:5568–5580
62. Nübel U, Engelen B, Felsre A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643
63. Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944
64. Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13:45–49
65. Pepi M, Lobianco A, Renzi M, Perra G, Bernardini E, Marvasi M, Gasperini S, Volterrani M, Franchi E, Heipieper HJ, Focardi SE (2009) Two naphthalene degrading bacteria belonging to the genera Paenibacillus and Pseudomonas isolated from a highly polluted lagoon perform different sensitivities to the organic and heavy metal contaminants. Extremophiles 13:839–848
66. 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
67. Polizzotto ML, Harvey CF, Li GC, Badruzzman B, Ali A, Newville M, Sutton S, Fendorf S (2006) Solid-phases and desorption processes of arsenic within Bangladesh sediments. Chem Geol 228:97–111
68. Procópio L, Alvarez VM, Jurelevicius DA, Hansen L, Sørensen SJ, Cardoso JS, Pádula M, Leitão ÁC, Seldin L, van Elsas JD (2012) Insight from the draft genome of Dietzia cinnamea P4 reveals mechanisms of survival in complex tropical soil habitats and biotechnology potential. Antonie Van Leeuwenhoek 101:289–302
69. Ravenscroft P, McArthur JM, Hoque BA (2001) Geochemical and palaeohydrological controls on pollution of groundwater by arsenic. In: Chappell WR, Abernathy CO, Calderon R (eds) Arsenic exposure and health effects IV. Elsevier, Oxford, pp 53–78
70. Rhine ED, Phelps CD, Young LY (2006) Anaerobic arsenite oxidation by novel denitrifying isolates. Environ Microbiol 8:899–908
71. Rodríguez-Lado L, Sun G, Berg M, Zhang Q, Xue H, Zheng Q, Johnson CA (2013) Groundwater arsenic contamination throughout China. Science 341:866–868
72. Rowland HAL, Pederick RL, Polya DA, Pancost RD, Van Dongen BE, Gault AG, Vaughan DJ, Bryant C, Anderson B, Lloyd JR (2007) The control of organic matter on microbially mediated iron reduction and arsenic release in shallow alluvial aquifers, Cambodia. Geobiology 5:281–292
73. Salmassi TM, Walker JJ, Newman DK, Leadbetter JR, Pace NR, Hering JG (2006) Community and cultivation analysis of arsenite oxidizing biofilms at Hot Creek. Environ Microbiol 8:50–59
74. Santini JM, Sly LI, Schnagl RD, Macy JM (2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl Environ Microbiol 66:92–97
75. Sass H, Wieringa E, Cypionka H, Babenzien HD, Overmann J (1998) High genetic and physiological diversity of sulfate-reducing bacteria isolated from an oligotrophic lake sediment. Arch Microbiol 170:243–251
76. Schröder I, Johnson E, De Vries S (2003) Microbial ferric iron reductases. FEMS Microbiol Rev 27:427–447
77. Screen J, Moya E, Blagbrough IS, Smith AW (1995) Iron uptake in Pseudomonas aeruginosa mediated by N–(2,3-dihydroxybenzoyl)–l-serine and 2,3-dihydroxybenzoic acid. FEMS Microbiol Lett 127:145–149
78. Shinoda Y, Sakai Y, Ue M, Hiraishi A, Kato N (2000) Isolation and characterization of a new denitrifying spirillum capable of anaerobic degradation of phenol. Appl Environ Microbiol 66:1286–1291
79. Smedley PL, Zhang M, Zhang G, Luo Z (2003) Mobilisation of arsenic and other trace elements in fluviolacustrine aquifers of the Huhhot basin, Inner Mongolia. Appl Geochem 18:1453–1477
80. Song B, Palleroni NJ, Häggblom MM (2000a) Description of strain 3CB-1, a genomovar of Thaueraaromatica, capable of degrading 3-chlorobenzoate coupled to nitrate reduction. Int J Syst Evol Microbiol 50:551–558
81. Song B, Palleroni NJ, Häggblom MM (2000b) Isolation and characterization of diverse halobenzoate-degrading denitrifying bacteria from soils and sediments. Appl Environ Microbiol 66:3446–3453
82. Switzer BJ, Bindi AB, Buzzelli J, Stolz JF, Oremland RS (1998) Bacillus arsenoselenatis sp. nov., and Bacillus selenitireducens sp. nov.: two haloalkaliphiles from Mono Lake, California, which respire oxyanions of selenium and arsenic. Arch Microbiol 171:19–30
83. Takami H, Inoue A, Fuji F, Horikoshi K (1997) Microbial flora in the deepest sea mud of the Mariana Trench. FEMS Microbiol Lett 152:279–285
84. Tang J, Lin NF, Bian JM, Liu WZ, Zhang ZL (1996) Environmental geochemistry of arsenism areas in Hetao Plain, Inner Mongolia. Hydrogeol Eng Geol 1:49–54 (In Chinese with English abstract)
85. Ten LN, Baek SH, Im WT, Larina LL, Lee JS, Oh HM, Lee ST (2007) Bacillus pocheonensis sp. nov., a moderately halotolerant, aerobic bacterium isolated from soil of a ginseng field. Int J Syst Evol Microbiol 57:2532–2537
86. Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51(7):844–851
87. Turpeinen R, Kairesalo T, Haggblom MM (2004) Microbial community structure and activity in arsenic-, chromium- and copper contaminated soils. FEMS Microbiol Ecol 47(1):39–50
88. van der Zaan B, de Weert J, Rijnaarts H, de Vos WM, Smidt H, Gerritse J (2009) Degradation of 1,2-dichloroethane by microbial communities from river sediment at various redox conditions. Water Res 43:3207–3216
89. van Geen A, Rose J, Thoral S, Garnier JM, Zheng Y, Bottero JY (2004) Decoupling of As and Fe release to Bangladesh groundwater under reducing conditions. Part II: evidence from sediment incubations. Geochim Cosmochim Acta 68:3475–3486
90. Van Stempvoort DR, Millar K, Lawrence JR (2009) Accumulation of short-chain fatty acids in an aquitard linked to anaerobic biodegradation of petroleum hydrocarbons. Appl Geochem 24(1):77–85
91. Weelink SAB, Van Doesburg W, Saia FT, Rijpstra WIC, RÖling WFM, Smidt AJM, Stams WIC (2009) A strictly anaerobic Betaproteobacterium Georgfuchsiatoluolica gen. nov., sp. nov. degrades aromatic compounds with Fe(III), Mn(IV) or nitrate as an electron acceptor. FEMS Microbiol Ecol 70:575–585
92. Zhang XX, Jia YF, Wang X, Xu L (2008) Phylogenetic analysis and arsenate reduction effect of the arsenic-reducing bacteria enriched from contaminated soils at an abandoned smelter site. J Environ Sci 20:1501–1507