Six New Families of Aerobic Arsenate Reducing Bacteria: Leclercia, Raoultella, Kosakonia, Lelliottia, Yokenella, and Kluyvera

Abstract Elevated levels of arsenate can occur in the environment due to processes such as mining activities, and microbes must utilize various detoxification mechanisms to adapt to the associated pressure. The aim of this study was to identify as many aerobic arsenate-reducing bacteria (aARB) as possible in order to investigate their phylogenetic diversity and molecular mechanisms of arsenic resistance. We isolated 24 strains of aARB from a long-standing arsenic contaminated environment and detected the ars genotype in them. All 24 strains could reduce approximately 90% of arsenate, and 23 of them exhibited (6–59%) arsenic removal ability. The 16S rRNA gene analyses revealed aARB representing 16 genera were abundant. The included six genera, namely Leclercia, Raoultella, Kosakonia, Lelliottia, Yokenella, and Kluyvera, that were not previously known to reduce or exhibit resistance to arsenic. Twenty-one of 24 aARB were positive for ars amplification and 17 of them harbored a putative arsC gene, which is well-known for its involvement in arsenate reduction. However, the arsenic resistance associated with aARB strains is not always determined by the ars operon system. These results have provided additional insight into aARB and their potential for arsenic transformation and bioremediation.

[1]  Wenjing Liu,et al.  Arsenic mobilization in spent nZVI waste residue: Effect of Pantoea sp. IMH. , 2017, Environmental pollution.

[2]  L. Bleicher,et al.  Novel arsenic-transforming bacteria and the diversity of their arsenic-related genes and enzymes arising from arsenic-polluted freshwater sediment , 2017, Scientific Reports.

[3]  Yong-guan Zhu,et al.  Recurrent horizontal transfer of arsenite methyltransferase genes facilitated adaptation of life to arsenic , 2017, Scientific Reports.

[4]  Yong-guan Zhu,et al.  Linking Genes to Microbial Biogeochemical Cycling: Lessons from Arsenic. , 2017, Environmental science & technology.

[5]  Ren Zhang,et al.  Draft Genome Sequence of Bacillus sp. Strain CDB3, an Arsenic-Resistant Soil Bacterium Isolated from Cattle Dip Sites , 2017, Genome Announcements.

[6]  C. Jing,et al.  Comparative Genomic Analysis Reveals Organization, Function and Evolution of ars Genes in Pantoea spp. , 2017, Front. Microbiol..

[7]  X. Zhuang,et al.  Arsenic resistance strategy in Pantoea sp. IMH: Organization, function and evolution of ars genes , 2016, Scientific Reports.

[8]  A. Giri,et al.  Characterization of Roseomonas and Nocardioides spp. for arsenic transformation. , 2016, Journal of hazardous materials.

[9]  Yanshan Cui,et al.  Comparison of arsenate reduction and release by three As(V)-reducing bacteria isolated from arsenic-contaminated soil of Inner Mongolia, China. , 2016, Chemosphere.

[10]  Yanshan Cui,et al.  Arsenic redox transformation by Pseudomonas sp. HN-2 isolated from arsenic-contaminated soil in Hunan, China. , 2016, Journal of environmental sciences.

[11]  F. Zhao A novel pathway of arsenate detoxification , 2016, Molecular microbiology.

[12]  T. Oshima,et al.  Comparison of transcriptomes of enlarged spheroplasts of Erythrobacter litoralis and Lelliottia amnigena , 2016 .

[13]  B. Rosen,et al.  New mechanisms of bacterial arsenic resistance , 2016, Biomedical journal.

[14]  Huaming Guo,et al.  Arsenate reduction and mobilization in the presence of indigenous aerobic bacteria obtained from high arsenic aquifers of the Hetao basin, Inner Mongolia. , 2015, Environmental pollution.

[15]  D. Licastro,et al.  Draft Genome Sequence of Rice Endophyte-Associated Isolate Kosakonia oryzae KO348 , 2015, Genome Announcements.

[16]  Haixia Tian,et al.  Arsenic biotransformation in solid waste residue: comparison of contributions from bacteria with arsenate and iron reducing pathways. , 2015, Environmental science & technology.

[17]  Erik M. Quandt,et al.  An Alternate Pathway of Arsenate Resistance in E. coli Mediated by the Glutathione S-Transferase GstB , 2014, ACS chemical biology.

[18]  J. Nelson,et al.  Arsenic speciation in rice cereals for infants. , 2013, Journal of agricultural and food chemistry.

[19]  M. Deb,et al.  Yokenella regensburgei infection in India mimicking enteric fever. , 2013, Journal of medical microbiology.

[20]  G. Zhuang,et al.  Bacillus sp. SXB and Pantoea sp. IMH, aerobic As(V)‐reducing bacteria isolated from arsenic‐contaminated soil , 2013, Journal of applied microbiology.

[21]  Pinaki Sar,et al.  Characterization of arsenic resistant bacteria from arsenic rich groundwater of West Bengal, India , 2013, Ecotoxicology.

[22]  Vernissia Tam,et al.  Isolation of Leclercia adecarboxylata from a wound infection after exposure to hurricane-related floodwater , 2012, BMJ Case Reports.

[23]  G. Zhuang,et al.  Arsenic interception by cell wall of bacteria observed with surface-enhanced Raman scattering. , 2012, Journal of microbiological methods.

[24]  M. Sadowsky,et al.  Phylogenetic and phenotypic analyses of arsenic-reducing bacteria isolated from an old tin mine area in Thailand , 2012, World journal of microbiology & biotechnology.

[25]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[26]  F. Chang,et al.  Arsenite-oxidizing and arsenate-reducing bacteria associated with arsenic-rich groundwater in Taiwan. , 2011, Journal of contaminant hydrology.

[27]  A. Raggi,et al.  Arsenic contamination of the environment-food chain: a survey on wheat as a test plant to investigate phytoavailable arsenic in Italian agricultural soils and as a source of inorganic arsenic in the diet. , 2010, Journal of agricultural and food chemistry.

[28]  L. Ross,et al.  Raoultella ornithinolytica bacteremia in an infant with visceral heterotaxy. , 2010, The Pediatric Infectious Disease Journal.

[29]  E. Canzi,et al.  Arsenic-resistant bacteria associated with roots of the wild Cirsium arvense (L.) plant from an arsenic polluted soil, and screening of potential plant growth-promoting characteristics. , 2010, Systematic and applied microbiology.

[30]  L. Cavalca,et al.  Arsenic‐resistant bacteria isolated from agricultural soils of Bangladesh and characterization of arsenate‐reducing strains , 2009, Journal of applied microbiology.

[31]  Guanghui Liu,et al.  Genes involved in arsenic transformation and resistance associated with different levels of arsenic-contaminated soils , 2009, BMC Microbiology.

[32]  C. Su,et al.  Sedimentary arsenite‐oxidizing and arsenate‐reducing bacteria associated with high arsenic groundwater from Shanyin, Northwestern China , 2008, Journal of applied microbiology.

[33]  Yang-Hoon Kim,et al.  The ars genotype characterization of arsenic-resistant bacteria from arsenic-contaminated gold–silver mines in the Republic of Korea , 2008, Applied Microbiology and Biotechnology.

[34]  H. Kawahata,et al.  Arsenic resistance and removal by marine and non-marine bacteria. , 2007, Journal of biotechnology.

[35]  S. Silver,et al.  A bacterial view of the periodic table: genes and proteins for toxic inorganic ions , 2005, Journal of Industrial Microbiology and Biotechnology.

[36]  S. Silver,et al.  Genes and Enzymes Involved in Bacterial Oxidation and Reduction of Inorganic Arsenic , 2005, Applied and Environmental Microbiology.

[37]  G. Cook,et al.  Isolation and Characterization of Arsenate-Reducing Bacteria from Arsenic-Contaminated Sites in New Zealand , 2004, Current Microbiology.

[38]  C. Jackson,et al.  Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase , 2003, BMC Evolutionary Biology.

[39]  John F. Stolz,et al.  The Ecology of Arsenic , 2003, Science.

[40]  P. Grimont,et al.  β-Lactamases of Kluyvera ascorbata, Probable Progenitors of Some Plasmid-Encoded CTX-M Types , 2002, Antimicrobial Agents and Chemotherapy.

[41]  S. Silver,et al.  Microbial arsenic: from geocycles to genes and enzymes. , 2002, FEMS microbiology reviews.

[42]  W. Inskeep,et al.  Microbial populations associated with the reduction and enhanced mobilization of arsenic in mine tailings. , 2001, Environmental science & technology.

[43]  P. B. Kavi Kishor,et al.  Molecular identification of arsenic-resistant estuarine bacteria and characterization of their ars genotype , 2011, Ecotoxicology.

[44]  M. F. Villegas-Torres,et al.  Horizontal arsC gene transfer among microorganisms isolated from arsenic polluted soil , 2011 .

[45]  Hemant J Purohit,et al.  Identification of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludge metagenomic library. , 2009, FEMS microbiology ecology.