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Haloarchaea from the Andean Puna: Biological Role in the Energy Metabolism of Arsenic

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Abstract

Biofilms, microbial mats, and microbialites dwell under highly limiting conditions (high salinity, extreme aridity, pH, and elevated arsenic concentration) in the Andean Puna. Only recent pioneering studies have described the microbial diversity of different Altiplano lakes and revealed their unexpectedly diverse microbial communities. Arsenic metabolism is proposed to be an ancient mechanism to obtain energy by microorganisms. Members of Bacteria and Archaea are able to exploit arsenic as a bioenergetic substrate in either anaerobic arsenate respiration or chemolithotrophic growth on arsenite. Only six aioAB sequences coding for arsenite oxidase and three arrA sequences coding for arsenate reductase from haloarchaea were previously deposited in the NCBI database. However, no experimental data on their expression and function has been reported. Recently, our working group revealed the prevalence of haloarchaea in a red biofilm from Diamante Lake and microbial mat from Tebenquiche Lake using a metagenomics approach. Also, a surprisingly high abundance of genes used for anaerobic arsenate respiration (arr) and arsenite oxidation (aio) was detected in the Diamante’s metagenome. In order to study in depth the role of arsenic in these haloarchaeal communities, in this work, we obtained 18 haloarchaea belonging to the Halorubrum genus, tolerant to arsenic. Furthermore, the identification and expression analysis of genes involved in obtaining energy from arsenic compounds (aio and arr) showed that aio and arr partial genes were detected in 11 isolates, and their expression was verified in two selected strains. Better growth of two isolates was obtained in presence of arsenic compared to control. Moreover, one of the isolates was able to oxidize As[III]. The confirmation of the oxidation of arsenic and the transcriptional expression of these genes by RT-PCR strongly support the hypothesis that the arsenic can be used in bioenergetics processes by the microorganisms flourishing in these environments.

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Acknowledgements

This work was supported by the Argentinean National Fund for Science and Technology (FONCyT; project PICT 2013 numbers 0730 and PICT V 2015 numbers 3825). OFO and MEF are researchers from the National Research Council (CONICET) in Argentina. MCR is a recipient of a postdoctoral fellowship from CONICET Argentina, and MNS is a recipient of a doctoral fellowship from FONCyT. We also want to thank Mr. Luis Ahumada for his assistance in field trip and the Environment Secretary of Catamarca province government for their valuable support.

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  1. Omar Federico Ordoñez and María Cecilia Rasuk contributed equally to this work.

Authors and Affiliations

  1. Laboratorio de Investigaciones Microbiológicas de Lagunas Andinas (LIMLA), Planta Piloto de Procesos Industriales y Microbiológicos (PROIMI), CCT, CONICET, Av. Belgrano y Pasaje Caseros, 4000, Tucumán, Argentina

    Omar Federico Ordoñez, María Cecilia Rasuk, Mariana Noelia Soria & María Eugenia Farías

  2. Centro de Ecología Aplicada (CEA), Suecia 3304, 56-2-2741872, Ñuñoa, Santiago, Chile

    Manuel Contreras

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Correspondence to María Eugenia Farías.

Electronic Supplementary Material

Supplementary Figure S1

Amplification products of putative aioA and arrA genes from isolated strains. A) Amplification of aioA (line 1 to 5) and arrA (line 6 to 10) genes in isolates from Diamante lake. Line 1 and 6: DM1, line 2 and 7: DM2, line 3 and 8: DM3, line 4 and 9: DM4, line 5 and 10: DM5, M: 100 bp molecular marker, line 1 and 12: negative control. B1) Amplification of aioA from Tebenquiche isolates. Line 1: TC1, Line 2: TC3, Line 3: TC5, Line 4: TC7, Line 5: TC8, Line 6: TC9, Line 7: TC11, Line 8: TC16, Line 9: TC28, Line 10: negative control, M: 100 bp molecular marker. B2) Amplification of arrA from Tebenquiche isolates. Line 1: TC1, Line 2: TC3, Line 3: TC8, M: 100 bp molecular marker Line 4: negative control, Line 5: TC9, Line 6: TC11, Line 7: TC28 (GIF 85 kb)

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Ordoñez, O.F., Rasuk, M.C., Soria, M.N. et al. Haloarchaea from the Andean Puna: Biological Role in the Energy Metabolism of Arsenic. Microb Ecol 76, 695–705 (2018). https://doi.org/10.1007/s00248-018-1159-3

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