Biodegradation of roxarsone by a bacterial community of underground water and its toxic impact

World Journal of Microbiology and Biotechnology

Volumn 31, Issue 8, 2015, Pages 1267-1277

  Mafla, S ^a   Moraga, R ^b   Leon C G ^a   Guzman Fierro V G ^a   Yanez J ^a   Smith, C T ^a   Mondaca, M A ^a   Campos, V L ^a  

^a UNIVERSITY OF CONCEPCIÓN   (Chile)

^b UNIVERSIDAD ARTURO PRAT   (Chile)

Author keywords

Arsenic; Biodegradation; Microcosms; Roxarsone; Toxicity; Underground water

Indexed keywords

ARSENIC; BIODEGRADATION; DEGRADATION; GROUNDWATER; HEALTH RISKS; LEACHING; MICROBIOLOGY; MICROORGANISMS; NUTRIENTS; TOXICITY;

AGRICULTURAL FIELDS; ANAEROBIC CONDITIONS; BACTERIAL COMMUNITY; DEGRADATION ANALYSIS; DEGRADATION PRODUCTS; MICROCOSMS; PROKARYOTIC CELLS; ROXARSONE;

BACTERIA;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); EUKARYOTA; FIRMICUTES; PLANCTOMYCETES; PROKARYOTA; PROTEOBACTERIA; SPIROCHAETES;

GROUND WATER; MANURE; ROXARSONE; SOIL POLLUTANT; WATER POLLUTANT;

ANALYSIS; ANIMAL; BACTERIUM; BIOREMEDIATION; BIOTRANSFORMATION; CHICKEN; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MANURE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; SOIL POLLUTANT; TOXICITY; WATER POLLUTANT;

ANIMALS; BACTERIA; BIODEGRADATION, ENVIRONMENTAL; BIOTRANSFORMATION; CHICKENS; GROUNDWATER; MANURE; MOLECULAR SEQUENCE DATA; ROXARSONE; SOIL POLLUTANTS; WATER POLLUTANTS;

EID: 84933676289     PISSN: 09593993     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11274-015-1886-2     Document Type: Article

References (60)

1. Ahmad S, Sayed M, Barua S, Khan M, Faruquee M, Jalil A, Hadi S, Talukder H (2001) Arsenic in drinking water and pregnancy outcomes. Environ Health Perspect 109:629–631
2. Akinde S, Obire O (2008) Aerobic heterotrophic bacteria and petroleum-utilizing bacteria from cow dung and poultry manure. World J Microbiol Biotechnol 9:1999–2002
3. Amann R, Ludwig W, Schleifer K (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
4. Anderson CE (1999) Arsenicals as feed additives for poultry and swine. In: Lederer WH, Fensterheim RJ (eds) Arsenic–industrial, biomedical, environmental perspectives. Van Nostrand Reinhold Co, New York, pp 89–97
5. Andreae MO (1979) Arsenic speciation in seawater and interstitial waters: the influence of biological-chemical interactions on the speciation of a trace element. Limnol Oceanogr 24:440–452
6. Arai Y, Lanzirotti A, Sutton S, Davis J, Sparks D (2003) Arsenic speciation and reactivity in poultry litter. Environ Sci Technol 37:4083–4090
7. Arunlertaree C, Moolthongnoi C (2008) The use of fermented feather meal for replacement of fish meal in the diet of Oreochromis niloticus. Environ Nat Resour J 6:13–24
8. Bansal N, Sinha I, Virdi J (2000) Virulence plasmid (pYV)-associated susceptibility of Yersinia enterocolitica to chlorine and heavy metals. J Appl Microbiol 89:663–667
9. Barone JR, Schmidt W (2006) Effect of formic acid exposure on keratin fiber derived from poultry feather biomass. Bioresour Technol 97:233–242
10. Basu P, Ghosh RN, Grove LE, Klei L, Barchowsky A (2008) Angiogenic potential of 3-nitro-4-hydroxy benzene arsonic Acid (roxarsone). Environ Health Perspect 16:520–523
11. Bednar A, Garbarino J, Ferrer I, Rutherford D, Wershaw R, Ranville J, Wildeman T (2003) Photodegradation of roxarsone in poultry litter leachates. Sci Total Environ 302:237–245
12. Brosius J, Palmer M, Kennedy P, Noller H (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75:4801–4805
13. Butcher B, Deane S, Rawlings D (2000) The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66:1826–1833
14. Cai J, Salmon K, DuBow M (1998) A chromosomal ars operon homologue of Pseudomonas aeruginosa confers increased resistance to arsenic and antimony in Escherichia coli. Microbiology 144:2705–2713
15. Campos VL, León C, Mondaca MA, Yáñez J, Zaror C (2011) Arsenic mobilization by epilithic bacterial communities associated with volcanic rocks from Camarones River, Atacama Desert, Northern Chile. Arch Environ Contam Toxicol 61:185–192
16. Carlin A, Shi W, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177:981–986
17. Chapman HD, Johnson ZB (2002) Use of antibiotics and roxarsone in broiler chickens in the USA: analysis of the years 1995 to 2000. Poultry Sci 81:356–364
18. Chen Y, Graziano J, Parvez F, Liu M, Slavkovich V, Kalra T, Argos M, Islam T, Ahmed A, Rakibuz-Zaman M, Hasan R, Sarwar G, Levy D, Van Geen A, Ahsan H (2011) Arsenic exposure from drinking water and mortality from cardiovascular disease in Bangladesh: prospective cohort study. Br Med J 342:d2431
19. Christen K (2001) Environmental news: chickens, manure, and arsenic. Environ Sci Technol 35:184–185
20. Church C, Kleinman P, Bryant R, Saporito L, Allen A (2010) Occurrence of arsenic and phosphorus in ditch flow from litter-amended soils and barn area. J Environ Qual 39:2080–2088
21. Cortinas I, Field J, Kopplin M, Garbarino J, Gandolfi A, Sierra-Alvarez R (2006) Anaerobic biotransformation of roxarsone and related N-substituted phenylarsonic acids. Environ Sci Technol 40:2951–2957
22. Cressman M, Yu Z, Nelson M, Moeller S, Lilburn M, Zerby H (2010) Interrelations between the microbiotas in the litter and in the intestines of commercial broiler chickens. Appl Environ Microbiol 76:6572–6582
23. Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (2000) Can excrement and feathers of nestling songbirds be used as biomonitors for heavy metal pollution? Arch Environ Contam Toxicol 39:541–546
24. Diorio C, Cai J, Marmor J, Shinder R, DuBow M (1995) An Escherichia coli chromosomal ars operon homolog is functional in arsenic detoxification and is conserved in gram-negative bacteria. J Bacteriol 177:2050–2056
25. Dopson M, Lindstrom E, Hallberg K (2001) Chromosomally encoded arsenical resistance of the moderately Thermophilic acidophile Acidithiobacillus caldus. Extremophiles 5:247–255
26. EPA (1998) Special report on ingested inorganic arsenic Skin cancer nutritional essentiality US Environmental Protection Agency. EPA 625:3–87
27. EPA (2000) Estándares del Reglamento Nacional Primario de Agua Potable. EPA 815-F-00-007
28. Garbarino JR, Bednar A, Rutherford D, Beyer R, Wershaw R (2003) Environmental fate of roxarsone in poultry litter I. Degradation of roxarsone during composting. Environ Sci Technol 37:1509–1514
29. Guzmán-Fierro VG, Moraga R, León CG, Campos VL, Smith C, Mondaca MA (2014) Isolation and characterization of an aerobic bacterial consortium able to degrade roxarsone. Int J Environ Sci Technol 12:1353–1362
30. Hancock T, Denver J, Riedel G, Miller C (2002) Source transport and fate of arsenic in the Pocomoke River Basin a poultry dominated Chesapeake Bay Watershed. In: Proceedings of Arsenic in the Environment Workshop February 21–22 2001 US Geological Survey Denver Colorado
31. Jackson B, Bertsch P, Cabrera M, Camberato J, Seaman J, Wood C (2003) Trace element speciation in poultry litter. J Environ Qual 32:535–540
32. Kiranmayi M, Asok A, Lee B (2015) Organoarsenicals in poultry litter: detection, fate, and toxicity. Environ Int 75:68–80
33. Kumaresan M, Riyazuddin P (2001) Overview of speciation chemistry of arsenic. Curr Sci 80:837–846
34. Kuramata M, Futa S, Ryota K, Tadashi A, Maki A, Koji B, Kazuhiro T, Satotu I (2014) Arsenic biotransformation by Streptomyces sp. isolated from rice rhizosphere. Environ microbial. doi:10.1111/1462-2920.12572
35. Kwan K, Dutka B (1992) Evaluation of toxi-chromotest direct sediment toxicity testing procedure and mirotox solid-phase testing procedure. Bull Environ Contam Toxicol 49:656–662
36. León C, Campos V, Urrutia R, Mondaca M (2012) Metabolic and molecular characterization of bacterial community associated to Patagonian Chilean oligotrophic-lakes of quaternary glacial origin. World J Microbiol Biotechnol 28:1511–1521
37. Liu H, Wang G, Ge J, Liu L, Chen G (2014) Fate of roxarsone during biological nitrogen removal process in wastewater treatment systems. Chem Eng J 225:500–505
38. Lovley D, Phillips E (1988) Novel mode of microbial energy metabolism: organic carbon metabolism coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480
39. Maki T, Hasegawa H, Ueda K (2005) Seasonal dynamics of dimethylarsinic-acid-decomposing bacteria dominating in Lake Kahokugata. Appl Organomet Chem 19:231–238
40. Mangalgiri K, Adak A, Blaney L (2015) Organoarsenicals in poultry litter: detection, fate, and toxicity. Environ Int 75:68–80
41. Manz W, Amann R, Ludwig W, Wagner M, Schleifer K (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600
42. Meier H, Amann R, Ludwig W, Schleifer K (1999) Specific oligonucleotide probes for in situ detection of a major group of gram-positive bacteria with low DNA G+ C content. Syst Appl Microbiol 22:186–196
43. Morrison JL (1969) Distribution of arsenic from poultry litter in broiler chickens soil and crops. J Agric Food Chem 17:1288–1290
44. Muyzer G, De Waal EC, Uitterlinden AG (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 59:695–700
45. Nachman KE, Graham JP, Price LB, Silbergeld EK (2005) Arsenic: a roadblock to potential animal waste management solutions. Environ Health Perspect 113:1123–1124
46. Nachman KE, Raber G, Francesconi KA, Navas-Acien A, Love DC (2012) Arsenic species in poultry feather meal. Sci Total Environ 418:183–188
47. Nachman KE, Baron PA, Raber G, Francesconi KA, Navas-Acien A, Love DC (2013) Roxarsone, inorganic arsenic, and other arsenic species in chicken: a US-based market basket sample. Environ Health Perspect 121:818–824
48. Neyt C, Iriarte M, Thi VH, Cornelis GR (1997) Virulence and arsenic resistance in Yersiniae. J Bacteriol 179:612–619
49. Rutherford DW, Bednar AJ, Garbarino JR, Needham R, Staver KW, Wershaw RL (2003) Environmental fate of roxarsone in poultry litter. Part II. Mobility of arsenic in soils amended with poultry litter. Environ Sci Technol 37:1515–1520
50. Shi L, Wang W, Yuan S, Hu Z (2014) Electrochemical stimulation of microbial roxarsone degradation under anaerobic conditions. Environ Sci Technol 48:7951–7958
51. Sierra-Alvarez R, Yenal U, Field JA, Kopplin M, Gandolfi AJ, Garbarino JR (2006) Anaerobic biotransformation of organoarsenical pesticides monomethylarsonic acid and dimethylarsinic acid. J Agric Food Chem 54:3959–3966
52. Silbergelda E, Nachmanb K (2008) The environmental and public health risks associated with arsenical use in animal feeds. Ann NY Acad Sci 1140:346–357
53. Stolz JF, Perera E, Kilonzo B, Kail B, Crable B, Fisher E (2007) Biotransformation of 3-nitro-4-hydroxybenzene arsonic acid (roxarsone) and release of inorganic arsenic by Clostridium species. Environ Sci Technol 41:818–823
54. Suzuki K, Wakao N, Kimura T, Sakka K, Ohmiya K (1998) Expression and regulation of the arsenic resistance operon of Acidiphilum multivorum AIU 301 plasmid pKW301 in Escherichia coli. Appl Environ Microbiol 64:411–418
55. Torres SK, Campos VL, León CG, Rodríguez-Llamazares SM, Rojas SM, González M, Smith C, Mondaca MA (2012) Biosynthesis of selenium nanoparticles by Pantoea agglomerans and their antioxidant activity. J Nanopart Res 14:1236–1244
56. Torres-Escribano et al (2011) Sci Total Environ 409:604–611
57. Wershaw R, Garbarino J, Burkhardt M (1999) Roxarsone in natural water systems. In: Effects of Animal Feeding Operations on Water Resources and the Environment Proceedings of Technical Meeting US Geological Survey, Fort Collins, CO
58. Wiegel J (2009) Family I. Clostridiaceae Pribram 1933, 90AL. In: Whitman WB, Parte AC (eds) Bergey’s manual of systematic bacteriology, vol 3. Springer, New York, p 737
59. Zhang W, Xu F, Han J, Sun Q, Yang K (2015) Comparative cytotoxicity and accumulation of Roxarsone and its photodegradates in freshwater Protozoan Tetrahymena thermophila. J Hazard Mater 286:171–178
60. Zhanga F, Wanga W, Yuana S, Hua Z (2014) Biodegradation and speciation of roxarsone in an anaerobic granular sludge system and its impacts. J Hazard Mater 279:562–568