A nine year study was carried out on the evolution of macroscopic “acid streamer” growths in acidic, metal-rich mine water from the point of construction of a new channel to drain an abandoned underground copper mine. The new channel became rapidly colonized by acidophilic bacteria: two species of autotrophic iron-oxidizers ( Acidithiobacillus ferrivorans and “ Ferrovum myxofaciens”) and a heterotrophic iron-oxidizer (a novel genus/species with the proposed name “ Acidithrix ferrooxidans”). The same bacteria dominated the acid streamer communities for the entire nine year period, with the autotrophic species accounting for ~80% of the micro-organisms in the streamer growths (as determined by terminal restriction enzyme fragment length polymorphism (T-RFLP) analysis). Biodiversity of the acid streamers became somewhat greater in time, and included species of heterotrophic acidophiles that reduce ferric iron ( Acidiphilium, Acidobacterium, Acidocella and gammaproteobacterium WJ2) and other autotrophic iron-oxidizers ( Acidithiobacillus ferrooxidans and Leptospirillum ferrooxidan s). The diversity of archaea in the acid streamers was far more limited; relatively few clones were obtained, all of which were very distantly related to known species of euryarchaeotes. Some differences were apparent between the acid streamer community and planktonic-phase bacteria. This study has provided unique insights into the evolution of an extremophilic microbial community, and identified several novel species of acidophilic prokaryotes.
References
[1]
Johnson, D.B. Extremophiles: acidic environments. In Encyclopaedia of Microbiology, 2nd Edition; Schaechter, M., Ed.; Elsevier: Oxford, UK, 2009; pp. 107–126.
Edwards, K.J.; Gihring, T.M.; Banfield, J.F. Seasonal variations in microbial populations and environmental conditions in an extreme acid mine drainage environment. Appl. Environ. Microbiol.？1999, 65, 3627–3632. 10427059
[4]
Zeigler, S.; Ackermann, S.; Majzian, J.; Gescher, J. Matrix composition and community structure analysis of a novel bacterial leaching community. Environ. Microbiol.？2009, 11, 2329–2338, doi:10.1111/j.1462-2920.2009.01959.x.
[5]
Jones, D.S.; Albrecht, H.L.; Dawson, K.S.; Schaperdoth, I.; Freeman, K.H.; Pi, Y.; Pearson, A.; Macalady, J.L. Community genomic analysis of an extremely acidophilic sulfur-oxidizing biofilm. ISME J.？2012, 6, 158–170, doi:10.1038/ismej.2011.75.
[6]
Bevins, R.E. A Mineralogy of Wales; Geological Series No. 16; National Museum of Wales Press: Cardiff, UK, 1994.
[7]
Walton, K.C.; Johnson, D.B. Microbiological and chemical characteristics of an acidic stream draining a disused copper mine. Environ. Pollut.？1992, 76, 169–175, doi:10.1016/0269-7491(92)90105-J.
[8]
Coupland, K.; Johnson, D.B. Geochemistry and microbiology of an impounded subterranean acidic water body at Mynydd Parys, Anglesey, Wales. Geobiol.？2004, 2, 77–86, doi:10.1111/j.1472-4677.2004.00023.x.
[9]
Valente, T.M.; Gomez, C.L. The role of two acidophilic algae as ecological indicators of acid mine drainage sites. J. Iberian Geol.？2007, 33, 283–294.
[10]
Hallberg, K.B.; Coupland, K.; Kimura, S.; Johnson, D.B. Macroscopic “acid streamer” growths in acidic, metal-rich mine waters in north Wales consist of novel and remarkably simple bacterial communities. Appl. Environ. Microbiol.？2006, 72, 2022–2030, doi:10.1128/AEM.72.3.2022-2030.2006.
[11]
Kimoto, K.; Aizawa, T.; Urai, M.; Bao Ve, N.; Suzuki, K.; Nakajima, M.; Sunairi, M. Acidocella. aluminiidurans sp. nov., an aluminium-tolerant bacterium isolated from Panicum. repens grown in a highly acidic swamp in actual acid sulfate soil area of Vietnam. Int. J. Syst. Evol. Microbiol.？2010, 60, 764–768, doi:10.1099/ijs.0.011569-0.
[12]
Johnson, D.B.; Rolfe, S.; Hallberg, K.B.; Iversen, E. Isolation and phylogenetic characterisation of acidophilic microorganisms indigenous to acidic drainage waters at an abandoned Norwegian copper mine. Environ. Microbiol.？2001, 3, 630–637, doi:10.1046/j.1462-2920.2001.00234.x.
[13]
Kishimoto, N.; Kosako, Y.; Wakao, N.; Tano, T.; Hiraishi, A. Transfer of Acidiphilium facilis and Acidiphilium aminolytica to the genus Acidocella gen. nov., and emendation of the genus Acidiphilium. Syst. Appl. Microbiol.？1995, 18, 85–91, doi:10.1016/S0723-2020(11)80453-4.
[14]
Hallberg, K.B.; González-Toril, E.; Johnson, D.B. Acidithiobacillus ferrivorans sp. nov.; facultatively anaerobic, psychrotolerant, iron- and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles？2010, 14, 9–19, doi:10.1007/s00792-009-0282-y.
[15]
Johnson, D.B.; Bacelar-Nicolau, P.; Okibe, N.; Thomas, A.; Hallberg, K.B. Characteristics of Ferrimicrobium acidiphilum gen. nov., sp. nov., and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic iron-oxidizing, extremely acidophilic Actinobacteria. Int. J. Syst. Evol. Microbiol.？2009, 59, 1082–1089, doi:10.1099/ijs.0.65409-0.
[16]
Winch, S.; Mills, H.J.; Kostka, J.E.; Fortin, D.; Lean, D.R. Identification of sulfate-reducing bacteria in methylmercury-contaminated mine tailings by analysis of SSU rRNA genes. FEMS Microbiol. Ecol.？2009, 68, 94–107, doi:10.1111/j.1574-6941.2009.00658.x. 19291023
[17]
Jiang, C.Y.; Liu, Y.; Liu, Y.Y.; You, X.Y.; Guo, X.; Liu, S.J. Alicyclobacillus ferrooxydans sp. nov., a ferrous-oxidizing bacterium from solfataric soil. Int. J. Syst. Evol. Microbiol.？2008, 58, 2898–2903, doi:10.1099/ijs.0.2008/000562-0.
[18]
Urbieta, M.S.; Gonzalez Toril, E.; Aguilera, A.; Giaveno, M.A.; Donati, E. First prokaryotic biodiversity assessment using molecular techniques of an acidic river in Neuquen, Argentina. Microb. Ecol.？2012, 64, 91–104, doi:10.1007/s00248-011-9997-2. 22214994
[19]
Dridi, B.; Fardeau, M.L.; Ollivier, B.; Raoult, D.; Drancourt, M. Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int. J. Syst. Evol. Microbiol.？2012, 62, 1902–1907, doi:10.1099/ijs.0.033712-0.
[20]
Brofft, J.E.; McArthur, J.V.; Shimkets, L.J. Recovery of novel bacterial diversity from a forested wetland impacted by reject coal. Environ. Microbiol.？2002, 4, 764–769, doi:10.1046/j.1462-2920.2002.00337.x.
[21]
Itoh, T.; Yoshikawa, N.; Takashina, T. Thermogymnomonas acidicola gen. nov., sp. nov., a novel thermoacidophilic, cell wall-less archaeon in the order Thermoplasmatales, isolated from a solfataric soil in Hakone, Japan. Int. J. Syst. Evol. Microbiol.？2007, 57, 2557–2561, doi:10.1099/ijs.0.65203-0. 17978217
[22]
Volant, A.; Desoeuvre, A.; Casiot, C.; Lauga, B.; Delpoux, S.; Morin, G.; Personne, J.C.; Hery, M.; Elbaz-Poulichet, F.; Bertin, P.N.; et al. Archaeal diversity: temporal variation in the arsenic-rich creek sediments of Carnoulès Mine, France. Extremophiles.？2012, 16, 645–657, doi:10.1007/s00792-012-0466-8.
[23]
Heinzel, E.; Janneck, E.; Glombitza, F.; Schl？mann, M.; Seifert, J. Population dynamics of iron-oxidizing communities in pilot plants for the treatment of acid mine waters. Environ. Sci. Technol.？2009, 43, 6138–6144, doi:10.1021/es900067d.
[24]
Hedrich, S.; Schl？mann, M.; Johnson, D.B. The iron-oxidizing Proteobacteria. Microbiol.？2011, 157, 1551–1564, doi:10.1099/mic.0.045344-0.
[25]
Kimura, S.; Bryan, C.G.; Hallberg, K.B.; Johnson, D.B. Biodiversity and geochemistry of an extremely acidic, low temperature subterranean environment sustained by chemolithotrophy. Environ. Microbiol.？2011, 13, 2092–2104, doi:10.1111/j.1462-2920.2011.02434.x. 21382147
[26]
Rowe, O.F.; Sánchez-Espa？a, J.; Hallberg, K.B.; Johnson, D.B. Microbial communities and geochemical dynamics in an extremely acidic, metal-rich stream at an abandoned sulfide mine (Huelva, Spain) underpinned by two functional primary production systems. Environ. Microbiol.？2007, 9, 1761–1771, doi:10.1111/j.1462-2920.2007.01294.x.
[27]
ancucheo, I.; Johnson, D.B. Acidophilic algae isolated from mine-impacted environments and their roles in sustaining heterotrophic acidophiles. Front. Microbiol.？2012, 3, 325. 22973267
[28]
Johnson, D.B.; Ghauri, M.A.; Said, M.F. Isolation and characterisation of an acidophilic heterotrophic bacterium capable of oxidizing ferrous iron. Appl. Environ. Microbiol.？1992, 58, 1423–1428. 1622207
[29]
ancucheo, I.; Johnson, D.B. Selective removal of transition metals from acidic mine waters by novel consortia of acidophilic sulfidogenic bacteria. Microb. Biotechnol.？2012, 5, 34–44, doi:10.1111/j.1751-7915.2011.00285.x.
[30]
Kolmert, A.; Wikstrom, P.; Hallberg, K.B. A fast and simple turbidometric method for the determination of sulfate in sulfate-reducing bacterial cultures. J. Microbiol. Meth.？2000, 41, 179–184, doi:10.1016/S0167-7012(00)00154-8.
[31]
Lovley, D.R.; Phillips, E.J.P. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol.？1987, 53, 1536–1540. 16347384
[32]
Suzuki, M.T.; Giovannoni, S.J. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl. Environ. Microbiol.？1996, 62, 625–630. 8593063
[33]
Sambrook, J.; Fritsch, E.F.; Maniatis, T. Molecular Cloning: A Laboratory Manual, 2nd Ed. ed.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 1989.
[34]
Johnson, D.B.; Hallberg, K.B. Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. In Biomining; Rawlings, D.E., Johnson, D.B., Eds.; Springer-Verlag: Heidelberg, Germany, 2007; pp. 237–262.
