Abstract
Ferrous iron- and sulfur-oxidizing Acidihalobacter species and similar so far unclassified bacteria have been isolated from the islands of Vulcano (Italy) and Milos (Greece), specifically from where seawater was acidified at sulfide-rich geothermal sites. Acidithiobacillus species which tolerated concentrations of chloride that inhibit most Acidithiobacillus spp. were also isolated from sites on both islands: these were At. thiooxidans strains and an unclassified species, Acidithiobacillus sp. strain V1. The potential of salt-tolerant acidophiles for industrial application in promoting copper extraction from mineral sulfides where chloride is naturally present at concentrations which would inhibit most acidophiles, or where seawater rather than fresh water is available, appears to be limited by the sensitivity of ferrous-iron oxidizing Acidihalobacter spp. to copper. However, tolerance of copper and chloride shown by At. thiooxidans strain A7 suggests it could oxidize sulfur and benefit acid leaching if ferric iron or copper was provided as the primary oxidant of sulfide ores.
Similar content being viewed by others
References
Alexander B, Leach S, Ingledew WJ (1987) The relationship between chemiosmotic parameters and sensitivity to anions and organic acids in the acidophile Thiobacillus ferrooxidans. J Gen Microbiol 133:1171–1179. https://doi.org/10.1099/00221287-133-5-1171
Antranikian G, Suleiman M, Schäfers C, Adams MWW, Bartolucci S, Blamey JM et al (2017) Diversity of bacteria and archaea from two shallow marine hydrothermal vents from Vulcano Island. Extremophiles 21:733–742. https://doi.org/10.1007/s00792-017-0938-y
Castro M, Moya-Beltrán A, Covarrubias PC, Gonzalez M, Cardenas JP, Issotta F, Nuñez H, Acuña L, Encina G, Holmes DS, Johnson BD, Quatrini R (2017) Draft genome sequence of the type strain of the sulfur-oxidizing acidophile, Acidithiobacillus albertensis (DSM 14366). Stand Genomic Sci 12:77. https://doi.org/10.1186/s40793-017-0282-y
Cisternas LA, Gálvez ED (2018) The use of seawater in mining. Min Process Extr Metall Rev 39:18–33. https://doi.org/10.1080/08827508.2017.1389729
Davis-Belmar CS, Norris PR (2009) Ferrous iron and pyrite oxidation by ‘‘Acidithiomicrobium’’ species. Adv Mater Res 71–73:271–274. https://doi.org/10.4028/www.scientific.net/AMR.71-73.271
Davis-Belmar CS, Le C Nicolle J, Norris PR (2008) Ferrous iron oxidation and leaching of copper ore with halotolerant bacteria in ore columns. Hydrometallurgy 94:144–147. https://doi.org/10.1016/j.hydromet.2008.05.030
Davis-Belmar CS, Cautivo D, Demergasso C, Rautenbach G (2014) Bioleaching of copper secondary sulfide ore in the presence of chloride by means of inoculation with chloride-tolerant microbial culture. Hydrometallurgy 150(2014):308–312. https://doi.org/10.1016/j.hydromet.2014.09.013
Falagán C, Johnson DB (2018) The significance of pH in dictating the relative toxicities of chloride and copper to acidophilic bacteria. Res Microbiol 169:552–557. https://doi.org/10.1016/j.resmic.2018.07.004
Felsenstein J (2006) PHYLIP (phylogeny inference package). Department of Genome Sciences, University of Washington, Seattle
Giovannelli D, d’Errico G, Manini E, Yakimov M, Vetriani C (2013) Diversity and phylogenetic analyses of bacteria from a shallow-water hydrothermal vent in Milos Island (Greece). Front Microbiol. https://doi.org/10.3389/fmicb.2013.00184. Article 184
Goebel BM, Norris PR, Burton NP (2000) Acidophiles in biomining. In: Priest FG, Goodfellow M (eds) Applied microbial systematics. Kluwer, Dordrecht, pp 293–314
Huber H, Stetter KO (1989) Thiobacillus prosperus sp. nov., represents a new group of halotolerant metal-mobilizing bacteria isolated from a marine geothermal field. Arch Microbiol 151:479–485. https://doi.org/10.1007/BF00454862
Kamimura K, Higashino E, Moriya S, Sugio T (2003) Marine acidophilic sulfur-oxidizing bacterium requiring salts for the oxidation of reduced inorganic sulfur compounds. Extremophiles 7:95–99. https://doi.org/10.1007/s00792-002-0300-9
Kamimura K, Sharmin S, Yoshino E, Tokuhisa M, Kanao T (2018) Draft genome sequence of Acidithiobacillus sp. strain SH, a marine acidophilic sulfur-oxidizing bacterium. Genome Announc 6:e01603–e01617. https://doi.org/10.1128/genomeA.01603-17
Khaleque HN, Corbett MK, Ramsay JP, Kaksonen AH, Boxall NJ, Holmes DS, Watkin ELJ (2017) Complete genome sequence of Acidihalobacter prosperus strain F5, an extremely acidophilic, iron- and sulfur-oxidizing halophile with potential industrial applicability in saline water bioleaching of chalcopyrite. J Biotechnol 262:56–59
Khaleque HN, González C, Kaksonen AH, Boxall NJ, Holmes DS, Watkin ELJ (2019) Genome-based classification of two halotolerant extreme acidophiles, Acidihalobacter prosperus V6 (= DSM 14174 = JCM 32253) and ‘Acidihalobacter ferrooxidans’ V8 (= DSM 14175 = JCM 32254) as two new species, Acidihalobacter aeolianus sp. nov. and Acidihalobacter ferrooxydans sp. nov., respectively. Int J Syst Evol Microbiol 69:1557–1565. https://doi.org/10.1099/ijsem.0.003313
Le C Nicolle J (2007) The characterisation of “Thiobacillus prosperus”-like halotolerant acidophiles. Dissertation, University of Warwick
Le C Nicolle J, Bathe S, Norris PR (2009) Ferrous iron oxidation and rusticyanin in halotolerant, acidophilic Thiobacillus prosperus. Microbiology 155:1302–1309. https://doi.org/10.1099/mic.0.023192-0
Maugeri TL, Bianconi G, Canganella F, Danovaro R, Gugliandolo C, Italiano F, Lentini V, Manini E, Nicolaus B (2010) Shallow hydrothermal vents in the southern Tyrrhenian Sea. Chem Ecol 26(Supp 1):285–298. https://doi.org/10.1080/02757541003693250
Ni Y-Q, Wan D-S, He KY (2008) 16S rDNA and 16S–23S internal transcribed spacer sequence analyses reveal inter- and intraspecific Acidithiobacillus phylogeny. Microbiology 154:2397–2407. https://doi.org/10.1099/mic.0.2007/016295-0
Norris PR, Barr DW (1985) Growth and iron oxidation by acidophilic moderate thermophiles. FEMS Microbiol Lett 28:221–224. https://doi.org/10.1111/j.1574-6968.1985.tb00795.x
Norris PR, Simmons S (2004) Pyrite oxidation by halotolerant, acidophilic bacteria. In: Tsezos M, Hatzikioseyian A, Remoundaki E (eds) Biohydrometallurgy: a sustainable technology in evolution part II. National Technical University of Athens, Athens, pp 1347–1351
Norris PR, Davis-Belmar C, Le C Nicolle J, Calvo-Bado LA, Angelatou V (2010) Pyrite oxidation and copper sulfide ore leaching by halotolerant, thermotolerant bacteria. Hydrometallurgy 104:432–436. https://doi.org/10.1016/j.hydromet.2010.03.025
Norris PR, Laigle L, Ogden TJ, Gould OJ (2017) Selection of thermophiles for base metal sulfide concentrate leaching, Part I: effect of temperature on copper concentrate leaching and silver recovery. Miner Eng 106:7–12. https://doi.org/10.1016/j.mineng.2016.12.003
Nuñez H, Moya-Beltrán A, Covarrubias PC, Issotta F, Cárdenas JP, González M et al. (2017) Molecular systematics of the genus Acidithiobacillus: insights into the phylogenetic structure and diversification of the taxon. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.00030. Article 30
Pablo Cárdenas J, Ortiz R, Norris PR, Watkin E, Holmes DS (2015) Reclassification of ‘Thiobacillus prosperus’ Huber and Stetter 1989 as Acidihalobacter prosperus gen. nov., sp. nov., a member of the family Ectothiorhodospiraceae. Int J Syst Evol Microbiol 65:3641–3644. https://doi.org/10.1099/ijsem.0.000468
Quatrini R, Escudero LV, Moya-Beltrán A, Galleguillos PA, Issotta F, Acosta M, Cárdenas JP, Nuñez H, Salinas K, Holmes DS, Demergasso C (2017) Draft genome sequence of Acidithiobacillus thiooxidans CLST isolated from the acidic hypersaline Gorbea salt flat in northern Chile. Stand Genomic Sci. https://doi.org/10.1186/s40793-017-0305-8. Article 84
Simmons S (2001) The microbial ecology of acidic environments. Dissertation, University of Warwick
Simmons S, Norris PR (2002) Acidophiles of saline water at thermal vents of Vulcano, Italy. Extremophiles 6:201–207. https://doi.org/10.1007/s007920100242
Watling HR (2014) Chalcopyrite hydrometallurgy at atmospheric pressure: 2 review of acidic chloride process options. Hydrometallurgy 146:96–110. https://doi.org/10.1016/j.hydromet.2014.03.013
Watling HR, Shiers DW, Zhang GJ (2012) Microbial behaviour under conditions relevant to heap leaching: studies using the sulfur-oxidising, moderate thermophile Acidithiobacillus caldus. Hydrometallurgy 127–128:104–111. https://doi.org/10.1016/j.hydromet.2012.07.012
Acknowledgements
This work was supported by the University of Warwick Overseas Research Student Fund, BHPBilliton and BHP CHILE INC.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Oren.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Norris, P.R., Davis-Belmar, C.S., Calvo-Bado, L.A. et al. Salt-tolerant Acidihalobacter and Acidithiobacillus species from Vulcano (Italy) and Milos (Greece). Extremophiles 24, 593–602 (2020). https://doi.org/10.1007/s00792-020-01178-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-020-01178-w