Abstract
Arsenic removal consecutive to biological iron oxidation and precipitation is an effective process for treating As-rich acid mine drainage (AMD). We studied the effect of hydraulic retention time (HRT)—from 74 to 456 min—in a bench-scale bioreactor exploiting such process. The treatment efficiency was monitored during 19 days, and the final mineralogy and bacterial communities of the biogenic precipitates were characterized by X-ray absorption spectroscopy and high-throughput 16S rRNA gene sequencing. The percentage of Fe(II) oxidation (10–47%) and As removal (19–37%) increased with increasing HRT. Arsenic was trapped in the biogenic precipitates as As(III)-bearing schwertmannite and amorphous ferric arsenate, with a decrease of As/Fe ratio with increasing HRT. The bacterial community in the biogenic precipitate was dominated by Fe-oxidizing bacteria whatever the HRT. The proportion of Gallionella and Ferrovum genera shifted from respectively 65 and 12% at low HRT to 23 and 51% at high HRT, in relation with physicochemical changes in the treated water. aioA genes and Thiomonas genus were detected at all HRT although As(III) oxidation was not evidenced. To our knowledge, this is the first evidence of the role of HRT as a driver of bacterial community structure in bioreactors exploiting microbial Fe(II) oxidation for AMD treatment.
Similar content being viewed by others
References
Acero P, Ayora C, Torrentó C, Nieto J-M (2006) The behavior of trace elements during schwertmannite precipitation and subsequent transformation into goethite and jarosite. Geochim Cosmochim Acta 70:4130–4139. https://doi.org/10.1016/j.gca.2006.06.1367
Asta MP, Ayora C, Román-Ross G, Cama J, Acero P, Gault AG, Charnock JM, Bardelli F (2010) Natural attenuation of arsenic in the Tinto Santa Rosa acid stream (Iberian Pyritic Belt, SW Spain): the role of iron precipitates. Chem Geol 271:1–12. https://doi.org/10.1016/j.chemgeo.2009.12.005
Auld RR, Myre M, Mykytczuk NCS, Leduc LG, Merritt TJS (2013) Characterization of the microbial acid mine drainage microbial community using culturing and direct sequencing techniques. J Microbiol Methods 93:108–115. https://doi.org/10.1016/j.mimet.2013.01.023
Baker BJ, Hugenholtz P, Dawson SC, Banfield JF (2003) Extremely acidophilic protists from acid mine drainage host Rickettsiales-lineage endosymbionts that have intervening sequences in their 16S rRNA genes. Appl Environ Microbiol 69:5512–5518. https://doi.org/10.1128/AEM.69.9.5512-5518.2003
Barret M, Briand M, Bonneau S, Préveaux A, Valière S, Bouchez O, Hunault G, Simoneau P, Jacquesa M-A (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81:1257–1266. https://doi.org/10.1128/AEM.03722-14
Battaglia-Brunet F, Dictor M-C, Garrido F, Crouzet C, Morin D, Dekeyser K, Clarens M, Baranger P (2002) An arsenic (III)-oxidizing bacterial population: selection, characterization, and performance in reactors. J Appl Microbiol 93:656–667. https://doi.org/10.1046/j.1365-2672.2002.01726.x
Battaglia-Brunet F, Itard Y, Garrido F, Delorme F, Crouzet C, Greffie C, Joulian C (2006a) A simple biogeochemical process removing arsenic from a mine drainage water. Geomicrobiol J 23:201–211. https://doi.org/10.1080/01490450600724282
Battaglia-Brunet F, Joulian C, Garrido F, Dictor M-C, Morin D, Coupland K, Barrie Johnson D, Hallberg KB, Baranger P (2006b) Oxidation of arsenite by Thiomonas strains and characterization of Thiomonas arsenivorans sp. nov. Antonie Van Leeuwenhoek 89:99–108. https://doi.org/10.1007/s10482-005-9013-2
Bhandari N, Reeder RJ, Strongin DR (2011) Photoinduced oxidation of arsenite to arsenate on ferrihydrite. Environ. Sci. Technol. 45:2783–2789. https://doi.org/10.1021/es103793y
Bhandari N, Reeder RJ, Strongin DR (2012) Photoinduced oxidation of arsenite to arsenate on goehite. Environ Sci Technol 46:8044–8051. https://doi.org/10.1021/es300988p
Bruneel O, Personné JC, Casiot C, Leblanc M, Elbaz-Poulichet F, Mahler BJ, Le Flèche A, Grimont PAD (2003) Mediation of arsenic oxidation by Thiomonas sp. in acid-mine drainage (Carnoulès, France). J Appl Microbiol 95:492–499. https://doi.org/10.1046/j.1365-2672.2003.02004.x
Bruneel O, Volant A, Gallien S, Chaumande B, Casiot C, Carapito C, Bardil A, Morin G, Brown GE Jr, Personné JC, Le Paslier D, Schaeffer C, Van Dorsselaer A, Bertin PN, Elbaz-Poulichet F, Arsène-Ploetze F (2011) Characterization of the active bacterial community involved in natural attenuation processes in arsenic-rich creek sediments. Microb Ecol 61:793–810. https://doi.org/10.1007/s00248-011-9808-9
Carlson L, Bigham JM, Schwertmann U, Kyek A, Wagner F (2002) Scavenging of As from acid mine drainage by schwertmannite and ferrihydrite: a comparison with synthetic analogues. Environ. Sci. Technol. 36:1712–1719
Casiot C, Morin G, Juillot F, Bruneel O, Personné J-C, Leblanc M, Duquesne K, Bonnefoy V, Elbaz-Poulichet F (2003) Bacterial immobilization and oxidation of arsenic in acid mine drainage (Carnoulès creek, France). Water Res 37:2929–2936. https://doi.org/10.1016/S0043-1354(03)00080-0
Chen L, Li J, Chen Y, Huang L, Hua Z, Hu M, Shu W (2013) Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 15:2431–2444. https://doi.org/10.1111/1462-2920.12114
Cheng H, Hu Y, Luo J, Xu B, Zhao J (2009) Geochemical processes controlling fate and transport of arsenic in acid mine drainage (AMD) and natural systems. J Hazard Mater 165:13–26. https://doi.org/10.1016/j.jhazmat.2008.10.070
Courtin-Nomade A, Grosbois C, Bril H, Roussel C (2005) Spatial variability of arsenic in some iron-rich deposits generated by acid mine drainage. Appl Geochem 20:383–396. https://doi.org/10.1016/j.apgeochem.2004.08.002
Duquesne K, Lieutaud A, Ratouchniak J, Muller D, Lett M-C, Bonnefoy V (2008) Arsenite oxidation by a chemoautotrophic moderately acidophilic Thiomonas sp.: from the strain isolation to the gene study. Environ Microbiol 10:228–237. https://doi.org/10.1111/j.1462-2920.2007.01447.x
Edwards KJ, Gihring TM, Banfield JF (1999) Seasonal variations in microbial populations and environmental conditions in an extreme acid mine drainage environment. Appl Environ Microbiol 65:3627–3632
Egal M, Casiot C, Morin G, Elbaz-Poulichet F, Cordier M-A, Bruneel O (2010) An updated insight into the natural attenuation of As concentrations in Reigous Creek (southern France). Appl Geochem 25:1949–1957. https://doi.org/10.1016/j.apgeochem.2010.10.012
Egal M, Casiot C, Morin G, Parmentier M, Bruneel O, Lebrun S, Elbaz-Poulichet F (2009) Kinetic control on the formation of tooeleite, schwertmannite and jarosite by Acidithiobacillus ferrooxidans strains in an As(III)-rich acid mine water. Chem Geol 265:432–441. https://doi.org/10.1016/j.chemgeo.2009.05.008
Elbaz-Poulichet F, Bruneel O, Casiot C (2006) The Carnoulès mine. Generation of As-rich acid mine drainage, natural attenuation processes and solutions for passive in-situ remediation. In: Difpolmine (Diffuse Pollution From Mining Activities), Montpellier, Dec 2006
Fabisch M, Freyer G, Johnson CA, Büchel G, Akob DM, Neu TR, Küsel K (2016) Dominance of ‘Gallionella capsiferriformans’ and heavy metal association with Gallionella-like stalks in metal-rich pH 6 mine water discharge. Geobiology 14:68–90. https://doi.org/10.1111/gbi.12162
Fernandez-Rojo L, Héry M, Le Pape P, Braungardt C, Desoeuvre A, Torres E, Tardy V, Resongles E, Laroche E, Delpoux S, Joulian C, Battaglia-Brunet F, Boisson J, Grapin G, Morin G, Casiot C (2017) Biological attenuation of arsenic and iron in a continuous flow bioreactor treating acid mine drainage (AMD). Water Res 123:594–606. https://doi.org/10.1016/j.watres.2017.06.059
Fukushi K, Sasaki M, Sato T, Yanase N, Amano H, Ikeda H (2003) A natural attenuation of arsenic in drainage from an abandoned arsenic mine dump. Appl Geochem 18:1267–1278. https://doi.org/10.1016/S0883-2927(03)00011-8
González-Toril E, Aguilera A, Souza-Egipsy V, López Pamo E, Sánchez España J, Amils R (2011) Geomicrobiology of La Zarza-Perrunal acid mine effluent (Iberian Pyritic Belt, Spain). Appl Environ Microbiol 77:2685–2694. https://doi.org/10.1128/AEM.02459-10
Hallberg KB (2010) New perspectives in acid mine drainage microbiology. Hydrometallurgy 104:448–453. https://doi.org/10.1016/j.hydromet.2009.12.013
Hanert HH (2006) The genus Gallionella. In: The prokaryotes. Springer New York, New York, NY, pp 990–995
Hao C, Wang L, Gao Y, Zhang L, Dong H (2010) Microbial diversity in acid mine drainage of Xiang Mountain sulfide mine, Anhui Province, China. Extremophiles 14:465–474. https://doi.org/10.1007/s00792-010-0324-5
Hao C, Zhang L, Wang L, Li S, Dong H (2012) Microbial community composition in acid mine drainage lake of Xiang Mountain sulfide mine in Anhui province, China. Geomicrobiol J 29:886–895. https://doi.org/10.1080/01490451.2011.635762
Hedrich S, Johnson DB (2012) A modular continuous flow reactor system for the selective bio-oxidation of iron and precipitation of schwertmannite from mine-impacted waters. Bioresour Technol 106:44–49. https://doi.org/10.1016/j.biortech.2011.11.130
Hedrich S, Johnson DB (2014) Remediation and selective recovery of metals from acidic mine waters using novel modular bioreactors. Environ Sci Technol 48:12206–12212. https://doi.org/10.1021/es5030367
Heinzel E, Janneck E, Glombitza F, Schlömann M, Seifert J (2009) Population dynamics of iron-oxidizing communities in pilot plants for the treatment of acid mine waters. Environ. Sci. Technol. 43:6138–6144. https://doi.org/10.1021/es900067d
Hovasse A, Bruneel O, Casiot C, Desoeuvre A, Farasin J, Hery M, Van Dorsselaer A, Carapito C, Arsène-Ploetze F (2016) Spatio-temporal detection of the Thiomonas population and the Thiomonas arsenite oxidase involved in natural arsenite attenuation processes in the Carnoulès acid mine drainage. Front Cell Dev Biol 4:1–14. https://doi.org/10.3389/fcell.2016.00003
Johnson DB, Hallberg KB, Hedrich S (2014) Uncovering a microbial enigma: isolation and characterization of the streamer-generating, iron-oxidizing, acidophilic bacterium Ferrovum myxofaciens. Appl Environ Microbiol 80:672–680. https://doi.org/10.1128/AEM.03230-13
Jones DS, Kohl C, Grettenberger C, Larson LN, Burgos WD, Macaladya JL (2015) Geochemical niches of iron-oxidizing acidophiles in acidic coal mine drainage. Appl Environ Microbiol 81:1242–1250. https://doi.org/10.1128/AEM.02919-14
Jones RM, Johnson DB (2016) Iron kinetics and evolution of microbial populations in low-pH, ferrous iron-oxidizing bioreactors. Environ. Sci. Technol. 50:8239–8245. https://doi.org/10.1021/acs.est.6b02141
Jwair RJ, Tischler JS, Janneck E, Schlömann M (2016) Acid mine water treatment using novel acidophilic iron-oxidizing bacteria of the genus ‘Ferrovum’: effect of oxygen and carbon dioxide on survival. In: Drebenstedt C, Paul M (eds) Mining meets water—conflicts and solutions. 1060–1063
Kimura S, Bryan CG, Hallberg KB, Johnson DB (2011) Biodiversity and geochemistry of an extremely acidic, low-temperature subterranean environment sustained by chemolithotrophy. Environ Microbiol 13:2092–2104. https://doi.org/10.1111/j.1462-2920.2011.02434.x
Kuang J-L, Huang L-N, Chen L-X, Hua Z-S, Li S-J, Hu M, Li J-T, Shu W-S (2013) Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J 7:1038–1050. https://doi.org/10.1038/ismej.2012.139
Larson LN, Sánchez-España J, Kaley B, Sheng Y, Bibby K, Burgos WD (2014) Thermodynamic controls on the kinetics of microbial low-pH Fe(II) oxidation. Environ Sci Technol 48:9246–9254. https://doi.org/10.1021/es501322d
Lawrence RW, Higgs SATW (1999) Removing and stabilizing As in acid mine water. JOM 51:27–29. https://doi.org/10.1007/s11837-999-0154-z
Lear G, Niyogi D, Harding J, Dong Y, Lewis G (2009) Biofilm bacterial community structure in streams affected by acid mine drainage. Appl Environ Microbiol 75:3455–3460. https://doi.org/10.1128/AEM.00274-09
Macías F, Caraballo MA, Nieto JM, Rötting TS, Ayora C (2012) Natural pretreatment and passive remediation of highly polluted acid mine drainage. J Environ Manage 104:93–100. https://doi.org/10.1016/j.jenvman.2012.03.027
Maillot F, Morin G, Juillot F, Bruneel O, Casiot C, Ona-Nguema G, Wang Y, Lebrun S, Aubry E, Vlaic G, Brown GE Jr (2013) Structure and reactivity of As (III)- and As(V)-rich schwertmannites and amorphous ferric arsenate sulfate from the Carnoulès acid mine drainage, France: comparison with biotic and abiotic model compounds and implications for As remediation. Geochim Cosmochim Acta 104:310–329. https://doi.org/10.1016/j.gca.2012.11.016
Modis K, Adam K, Panagopoulos K, Kontopoulos A (1998) Development and validation of a geostatistical model for prediction of acid mine drainage in underground sulphide mines. In: Transactions - Institution of Mining and Metallurgy. Section A. Mining Industry. Institution of Mining & Metallurgy, A102–A107
Morin G, Juillot F, Casiot C, Bruneel O, Personné J-C, Elbaz-Poulichet F, Leblanc M, Ildefonse P, Calas G (2003) Bacterial formation of tooeleite and mixed arsenic (III) or arsenic (V)–iron (III) gels in the Carnoulès acid mine drainage, France. A XANES, XRD, and SEM study. Environ. Sci. Technol. 37:1705–1712. https://doi.org/10.1021/es025688p
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. https://doi.org/10.1016/j.chemgeo.2004.08.018
Paikaray S (2015) Arsenic geochemistry of acid mine drainage. Mine Water Environ 34:181–196. https://doi.org/10.1007/s10230-014-0286-4
Pozdnyakov IP, Ding W, Xu J, Chen L, Wu F, Grivin VP, Plyusnin VF (2016) Photochemical transformation of an iron (III)-arsenite complex in acidic aqueous solution. Photochem Photobiol Sci 15:431–439. https://doi.org/10.1039/c5pp00240k
Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541. https://doi.org/10.1107/S0909049505012719
Resongles E, Le Pape P, Fernandez-Rojo L, Morin G, Brest J, Guo S, Casiot C (2016) Routine determination of inorganic arsenic speciation in precipitates from acid mine drainage using orthophosphoric acid extraction followed by HPLC-ICP-MS. Anal Methods 8:7420–7426. https://doi.org/10.1039/c6ay02084d
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Sheng Y, Bibby K, Grettenberger C, Kaley B, Macalady JL, Wang G, Burgos WD (2016) Geochemical and temporal influences on the enrichment of acidophilic iron-oxidizing bacterial communities. Appl Environ Microbiol 82:3611–3621. https://doi.org/10.1128/AEM.00917-16
Sun W, Xiao E, Kalin M, Krumins V, Dong Y, Ning Z, Liu T, Sun M, Zhao Y, Wu S, Mao J, Xiao T (2016) Remediation of antimony-rich mine waters: assessment of antimony removal and shifts in the microbial community of an onsite field-scale bioreactor. Environ Pollut 215:213–222. https://doi.org/10.1016/j.envpol.2016.05.008
Tardy V, Casiot C, Fernandez-Rojo L, Resongles E, Desoeuvre A, Joulian C, Battaglia-Brunet F, Héry M (2018) Temperature and nutrients as drivers of microbially mediated arsenic oxidation and removal from acid mine drainage. Appl Microbiol Biotechnol 102:2413–2424. https://doi.org/10.1007/s00253-017-8716-4
Teng W, Kuang J, Luo Z, Shu W (2017) Microbial diversity and community assembly across environmental gradients in acid mine drainage. Minerals 7:106. https://doi.org/10.3390/min7060106
Vasquez Y, Escobar MC, Neculita CM, Arbeli Z, Roldan F (2016) Biochemical passive reactors for treatment of acid mine drainage: effect of hydraulic retention time on changes in efficiency, composition of reactive mixture, and microbial activity. Chemosphere 153:244–253. https://doi.org/10.1016/j.chemosphere.2016.03.052
Vasquez Y, Escobar MC, Saenz JS, Quiceno-Vallejo MF, Neculita CM, Arbeli Z, Roldan F (2018) Effect of hydraulic retention time on microbial community in biochemical passive reactors during treatment of acid mine drainage. Bioresour Technol 247:624–632. https://doi.org/10.1016/j.biortech.2017.09.144
Volant A, Bruneel O, Desoeuvre A, Héry M, Casiot C, Bru N, Delpoux S, Fahy A, Javerliat F, Bouchez O, Duran R, Bertin PN, Elbaz-Poulichet F, Lauga B (2014) Diversity and spatiotemporal dynamics of bacterial communities: physicochemical and other drivers along an acid mine drainage. FEMS Microbiol Ecol 90:247–263. https://doi.org/10.1111/1574-6941.12394
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang Y, Qian P-Y (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 4:e7401. https://doi.org/10.1371/journal.pone.0007401
Williams M (2001) Arsenic in mine waters: an international study. Environ Geol 40:267–278. https://doi.org/10.1007/s002540000162
Acknowledgements
The authors thank the Agence Nationale de la Recherche (ANR) (IngECOST-DMA project, ANR-13-ECOT-0009), the OSU OREME (SO POLLUMINE Observatory, funded since 2009), and the Ecole Doctorale GAIA (PhD fellowship of Lidia Fernandez-Rojo, 2014-2017) for the financial support. We thank Remi Freydier for ICP-MS analysis on the AETE-ISO platform (OSU OREME, University of Montpellier). We thank Christophe Duperray, from the Montpellier RIO Imaging microscopy platform, for his kind assistance in cytometry. Mickaël Charron from BRGM is gratefully acknowledged for its technical assistance on aioA gene quantification. We also thank Luca Olivi from the XAFS beamline at the ELETTRA synchrotron (Trieste, Italy).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Electronic supplementary material
ESM 1
(PDF 836 kb)
Rights and permissions
About this article
Cite this article
Fernandez-Rojo, L., Casiot, C., Tardy, V. et al. Hydraulic retention time affects bacterial community structure in an As-rich acid mine drainage (AMD) biotreatment process. Appl Microbiol Biotechnol 102, 9803–9813 (2018). https://doi.org/10.1007/s00253-018-9290-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-9290-0