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Effects of Arsenic and Iron on the Community and Abundance of Arsenite-Oxidizing Bacteria in an Arsenic-Affected Groundwater Aquifer

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Abstract

Arsenic (As) contamination of groundwater aquifers is a global environmental problem, especially in South and Southeast Asian regions, and poses a risk to human health. Arsenite-oxidizing bacteria that transform As(III) to less toxic As(V) can be potentially used as a groundwater As remediation strategy. This study aimed to examine the community and abundance of arsenite-oxidizing bacteria in groundwater with various As concentrations from Rayong Province, Thailand using PCR-cloning-sequencing and quantitative PCR (qPCR) of catalytic subunit of arsenite oxidase gene (aioA). Key factors influencing their community and abundance were also identified. The results demonstrated that arsenite-oxidizing bacteria retrieved from groundwater were phylogenetically related to Betaproteobacteria and Alphaproteobacteria. The aioA gene abundances ranged from 8.6 × 101 to 1.1 × 104 copies per ng of genomic DNA, accounting for 0.16–1.37% of the total 16S rRNA bacterial gene copies. Although the abundance of arsenite-oxidizing bacteria in groundwater was low, groundwater with As(III) dominance likely promoted their abundance which possibly played an important role in chemolithoautotrophic oxidation of As(III) to As(V). Fe and As(III) were the major environmental factors influencing the community and abundance of arsenite-oxidizing bacteria. The knowledge gained from this study can be used to further contribute to the development of bioremediation strategies for As removal from groundwater resources.

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References

  1. Ali W, Rasool A, Junaid M, Zhang H (2019) A comprehensive review on current status, mechanism, and possible sources of arsenic contamination in groundwater: a global perspective with prominence of Pakistan scenario. Environ Geochem Health 41:737–760

    CAS  PubMed  Google Scholar 

  2. Sultana M, Sanyal SK, Hossain MA (2015) Handbook of research on uncovering new methods for ecosystem management through bioremediation. In: Singh S, Srivastava K (eds) Arsenic pollution in the environment: role of microbes in its bioremediation. IGI Global, Hershey, pp 92–119

    Google Scholar 

  3. Stopelli E, Duyen VT, Mai TT, Trang PT, Viet PH, Lightfoot A, Kipfer R, Schneider M, Eiche E, Kontny A, Neumann T (2020) Spatial and temporal evolution of groundwater arsenic contamination in the Red River delta, Vietnam: interplay of mobilisation and retardation processes. Sci Total Environ 717:137143. https://doi.org/10.1016/j.scitotenv.2020.137143

    Article  CAS  PubMed  Google Scholar 

  4. Tiankao W, Chotpantarat S (2018) Risk assessment of arsenic from contaminated soils to shallow groundwater in Ong Phra sub-district, Suphan Buri Province, Thailand. J Hydrol Reg Stud 19:80–96

    Google Scholar 

  5. Sarkar A, Paul B (2016) The global menace of arsenic and its conventional remediation—a critical review. Chemosphere 158:37–49

    CAS  PubMed  Google Scholar 

  6. Podgorski J, Berg M (2020) Global threat of arsenic in groundwater. Science 368:845–850

    CAS  PubMed  Google Scholar 

  7. Lièvremont D, Bertin PN, Lett MC (2009) Arsenic in contaminated waters: biogeochemical cycle, microbial metabolism and biotreatment processes. Biochimie 91:1229–1237

    PubMed  Google Scholar 

  8. Oremland RS, Saltikov CW, Wolfe-Simon F, Stolz JF (2009) Arsenic in the evolution of earth and extraterrestrial ecosystems. Geomicrobiol J 26:522–536

    CAS  Google Scholar 

  9. Kao AC, Chu YJ, Hsu FL, Liao VH (2013) Removal of arsenic from groundwater by using a native isolated arsenite-oxidizing bacterium. J Contam Hydrol 155:1–8

    CAS  PubMed  Google Scholar 

  10. Driehaus W, Seith R, Jekel M (1995) Oxidation of arsenate (III) with manganese oxides in water treatment. Water Res 29:297–305

    CAS  Google Scholar 

  11. Lett MC, Muller D, Lièvremont D, Silver S, Santini J (2012) Unified nomenclature for genes involved in prokaryotic aerobic arsenite oxidation. J Bacteriol 194:207–208

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Ghosh D, Bhadury P, Routh J (2014) Diversity of arsenite oxidizing bacterial communities in arsenic-rich deltaic aquifers in West Bengal, India. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00602

    Article  PubMed  PubMed Central  Google Scholar 

  13. Nandre VS, Bachate SP, Salunkhe RC, Bagade AV, Shouche YS, Kodam KM (2017) Enhanced detoxification of arsenic under carbon starvation: a new insight into microbial arsenic physiology. Curr Microbiol 74:614–622

    CAS  PubMed  Google Scholar 

  14. Quéméneur M, Cébron A, Billard P, Battaglia-Brunet F, Garrido F, Leyval C, Joulian C (2010) Population structure and abundance of arsenite-oxidizing bacteria along an arsenic pollution gradient in waters of the Upper Isle River Basin, France. Appl Environ Microbiol 76:4566–4570

    PubMed  PubMed Central  Google Scholar 

  15. Paul D, Poddar S, Sar P (2014) Characterization of arsenite-oxidizing bacteria isolated from arsenic-contaminated groundwater of West Bengal. J Environ Sci Health A 49:1481–1492

    CAS  Google Scholar 

  16. Xu Y, Li H, Zeng XC (2020) A novel biofilm bioreactor derived from a consortium of acidophilic arsenite-oxidizing bacteria for the cleaning up of arsenite from acid mine drainage. Ecotoxicology. https://doi.org/10.1007/s10646-020-02283-4

    Article  PubMed  PubMed Central  Google Scholar 

  17. Tong H, Liu C, Hao L, Swanner ED, Chen M, Li F, Xia Y, Liu Y, Liu Y (2019) Biological Fe (II) and As (III) oxidation immobilizes arsenic in micro-oxic environments. Geochim Cosmochim Acta 265:96–108

    CAS  Google Scholar 

  18. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Páez-Espino D, Tamames J, de Lorenzo V, Cánovas D (2009) Microbial responses to environmental arsenic. Biometals 22:117–130

    PubMed  Google Scholar 

  20. Gihring TM, Druschel GK, McCleskey RB, Hamers RJ, Banfield JF (2001) Rapid arsenite oxidation by Thermus aquaticus and Thermus thermophilus: field and laboratory investigations. Environ Sci Technol 35:3857–3862

    CAS  PubMed  Google Scholar 

  21. Andreoni V, Zanchi R, Cavalca L, Corsini A, Romagnoli C, Canzi E (2012) Arsenite oxidation in Ancylobacter dichloromethanicus As3-1b strain: detection of genes involved in arsenite oxidation and CO2 fixation. Curr Microbiol 65:212–218

    CAS  PubMed  Google Scholar 

  22. Costa PS, Scholte LL, Reis MP, Chaves AV, Oliveira PL, Itabayana LB, Suhadolnik ML, Barbosa FA, Chartone-Souza E, Nascimento AM (2014) Bacteria and genes involved in arsenic speciation in sediment impacted by long-term gold mining. PLoS ONE. https://doi.org/10.1371/journal.pone.0095655

    Article  PubMed  PubMed Central  Google Scholar 

  23. Yamamura S, Amachi S (2014) Microbiology of inorganic arsenic: from metabolism to bioremediation. J Biosci Bioeng 118:1–9

    CAS  PubMed  Google Scholar 

  24. Cavalca L, Zecchin S, Zaccheo P, Abbas BA, Rotiroti M, Bonomi T, Muyzer G (2019) Exploring biodiversity and arsenic metabolism of microbiota inhabiting arsenic-rich groundwaters in Northern Italy. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01480

    Article  PubMed  PubMed Central  Google Scholar 

  25. Das S, Kar S, Jean JS, Rathod J, Chakraborty S, Liu HS, Bundschuh J (2013) Depth-resolved abundance and diversity of arsenite-oxidizing bacteria in the groundwater of Beimen, a blackfoot disease endemic area of southwestern Taiwan. Water Res 47:6983–6991

    CAS  PubMed  Google Scholar 

  26. Sonthiphand P, Rattanaroongrot P, Mek-yong K, Kusonmano K, Rangsiwutisak C, Uthaipaisanwong P, Chotpantarat S, Termsaithong T (2021) Microbial community structure in aquifers associated with arsenic: analysis of 16S rRNA and arsenite oxidase genes. PeerJ 9:e10653. https://doi.org/10.7717/peerj.10653

    Article  PubMed  PubMed Central  Google Scholar 

  27. Jiang Z, Li P, Jiang D, Wu G, Dong H, Wang Y, Li B, Wang Y, Guo Q (2014) Diversity and abundance of the arsenite oxidase gene aioA in geothermal areas of Tengchong, Yunnan, China. Extremophiles 18:161–170

    CAS  PubMed  Google Scholar 

  28. Boonkaewwan S, Sonthiphand P, Chotpantarat S (2020) Mechanisms of arsenic contamination associated with hydrochemical characteristics in coastal alluvial aquifers using multivariate statistical technique and hydrogeochemical modeling: a case study in Rayong Province, Eastern Thailand. Environ Geochem Health. https://doi.org/10.1007/s10653-020-00728-7

    Article  PubMed  Google Scholar 

  29. Department of Groundwater Resources (2010) the eastern seaboard groundwater management project; to assess groundwater potential, installation of groundwater contamination monitor, and development of remediation plan in the area of Rayong and Chonburi provinces. Ministry of Natural Resources and Environment, Bangkok

    Google Scholar 

  30. Sonthiphand P, Ruangroengkulrith S, Mhuantong W, Charoensawan V, Chotpantarat S, Boonkaewwan S (2019) Metagenomic insights into microbial diversity in a groundwater basin impacted by a variety of anthropogenic activities. Environ Sci Pollut Res 26:26765–26781

    CAS  Google Scholar 

  31. Bhunia GS, Shit PK, Maiti R (2018) Comparison of GIS-based interpolation methods for spatial distribution of soil organic carbon (SOC). J Saudi Soc Agric Sci 17:114–126

    Google Scholar 

  32. Oke A, Sangodoyin A, Ogedengbe K, Omodele T (2013) Mapping of river water quality using inverse distance weighted interpolation in Ogun-Osun river basin, Nigeria. AGD Landsc Environ 7:48–62

    Google Scholar 

  33. Zargar K, Conrad A, Bernick DL, Lowe TM, Stolc V, Hoeft S, Oremland RS, Stolz J, Saltikov CW (2012) ArxA, a new clade of arsenite oxidase within the DMSO reductase family of molybdenum oxidoreductases. Environ Microbiol 14:1635–1645

    CAS  PubMed  Google Scholar 

  34. Inskeep WP, Macur RE, Hamamura N, Warelow TP, Ward SA, Santini JM (2007) Detection, diversity and expression of aerobic bacterial arsenite oxidase genes. Environ Microbiol 9:934–943

    CAS  PubMed  Google Scholar 

  35. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    CAS  PubMed  Google Scholar 

  36. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    CAS  PubMed  Google Scholar 

  37. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol-Prog Ser 92:205–205

    Google Scholar 

  42. Jones DL (2015) Fathom toolbox for Matlab: software for multivariate ecological and oceanographic data analysis. College of Marine Science, University of South Florida, St. Petersburg

    Google Scholar 

  43. Polizzotto ML, Kocar BD, Benner SG, Sampson M, Fendorf S (2008) Near-surface wetland sediments as a source of arsenic release to ground water in Asia. Nature 454:505–508

    CAS  PubMed  Google Scholar 

  44. Hassan Z, Sultana M, van Breukelen BM, Khan SI, Röling WF (2015) Diverse arsenic-and iron-cycling microbial communities in arsenic-contaminated aquifers used for drinking water in Bangladesh. FEMS Microbiol Ecol 91:fiv026. https://doi.org/10.1093/femsec/fiv026

    Article  CAS  PubMed  Google Scholar 

  45. Yamamura S, Watanabe K, Suda W, Tsuboi S, Watanabe M (2014) Effect of antibiotics on redox transformations of arsenic and diversity of arsenite-oxidizing bacteria in sediment microbial communities. Environ Sci Technol 48:350–357

    CAS  PubMed  Google Scholar 

  46. Heinrich-Salmeron A, Cordi A, Brochier-Armanet C, Halter D, Pagnout C, Abbaszadeh-Fard E, Montaut D, Seby F, Bertin PN, Bauda P, Arsène-Ploetze F (2011) Unsuspected diversity of arsenite-oxidizing bacteria as revealed by widespread distribution of the aoxB gene in prokaryotes. Appl Environ Microbiol 77:4685–4692

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Zeng XC, Guoji E, Wang J, Wang N, Chen X, Mu Y, Li H, Yang Y, Liu Y, Wang Y (2016) Functions and unique diversity of genes and microorganisms involved in arsenite oxidation from the tailings of a realgar mine. Appl Environ Microbiol 82:7019–7029

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Guo XP, Niu ZS, Lu DP, Feng JN, Chen YR, Tou FY, Liu M, Yang Y (2017) Bacterial community structure in the intertidal biofilm along the Yangtze Estuary, China. Mar Pollut Bull 124:314–320

    CAS  PubMed  Google Scholar 

  49. Chotpantarat S, Amasvata C (2020) Influence of pH on transport of arsenate (As5+) through different reactive media using column experiments and transport modeling. Sci Rep 10:3512. https://doi.org/10.1038/s41598-020-59770-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Gillispie EC, Andujar E, Polizzotto ML (2016) Chemical controls on abiotic and biotic release of geogenic arsenic from Pleistocene aquifer sediments to groundwater. Environ Sci-Process Impacts 18:1090–1103

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was financially supported by the Thailand Research Fund (TRF) Grant for New Scholar (MRG6180127), the Thailand Toray Science Foundation (TTSF) through the Science & Technology Research Grant, and the Faculty of Science, Mahidol University. The authors would like to thank Philip D. Round for constructive comments and English proofreading.

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Authors and Affiliations

  1. International Postgraduate Program in Hazardous Substance and Environmental Management, Chulalongkorn University, Bangkok, Thailand

    Phurinat Pipattanajaroenkul

  2. Department of Geology, Faculty of Science, Chulalongkorn University, Bangkok, Thailand

    Srilert Chotpantarat

  3. Research Program on Controls of Hazardous Contaminants in Raw Water Resources for Water Scarcity Resilience, Center of Excellence On Hazardous Substance Management (HSM), Chulalongkorn University, Bangkok, Thailand

    Srilert Chotpantarat

  4. Research Unit of Green Mining (GMM), Chulalongkorn University, Bangkok, Thailand

    Srilert Chotpantarat

  5. Learning Institute, King Mongkut’s University of Technology Thonburi, Bangkok, Thailand

    Teerasit Termsaithong

  6. Theoretical and Computational Science Center (TaCS), King Mongkut’s University of Technology Thonburi, Bangkok, Thailand

    Teerasit Termsaithong

  7. Department of Biology, Faculty of Science, Mahidol University, 272 Rama VI Road, Ratchathewi, Bangkok, 10400, Thailand

    Prinpida Sonthiphand

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  1. Phurinat Pipattanajaroenkul
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  2. Srilert Chotpantarat
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  3. Teerasit Termsaithong
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  4. Prinpida Sonthiphand
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Contributions

PP involved in the analysis and discussion of arsenite-oxidizing bacterial community. SC provided inputs on arsenic geochemistry. TT conducted statistical and multivariate analyses. PS involved in the analysis of arsenite-oxidizing bacterial abundance, interpreted the results, and wrote the main manuscript. All authors reviewed the manuscript.

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Correspondence to Prinpida Sonthiphand.

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Pipattanajaroenkul, P., Chotpantarat, S., Termsaithong, T. et al. Effects of Arsenic and Iron on the Community and Abundance of Arsenite-Oxidizing Bacteria in an Arsenic-Affected Groundwater Aquifer. Curr Microbiol 78, 1324–1334 (2021). https://doi.org/10.1007/s00284-021-02418-8

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