Comparative Genomics Analysis of a New Exiguobacterium Strain from Salar de Huasco Reveals a Repertoire of Stress-Related Genes and Arsenic Resistance

Juan Castro-Severyn,Cesar Salinas,Jonathan Fortt,Cristina Dorador,Daniel Aguayo,Francisco Remonsellez,Claudia P Saavedra,Pablo Aguilar,Coral Pardo-Esté,Franck Molina,Raquel Quatrini,Sandro L Valenzuela,Eduardo Castro-Nallar

doi:10.3389/fmicb.2017.00456

Abstract

The Atacama Desert hosts diverse ecosystems including salt flats and shallow Andean lakes. Several heavy metals are found in the Atacama Desert, and microorganisms growing in this environment show varying levels of resistance/tolerance to copper, tellurium, and arsenic, among others. Herein, we report the genome sequence and comparative genomic analysis of a new Exiguobacterium strain, sp. SH31, isolated from an altiplanic shallow athalassohaline lake. Exiguobacterium sp. SH31 belongs to the phylogenetic Group II and its closest relative is Exiguobacterium sp. S17, isolated from the Argentinian Altiplano (95% average nucleotide identity). Strain SH31 encodes a wide repertoire of proteins required for cadmium, copper, mercury, tellurium, chromium, and arsenic resistance. Of the 34 Exiguobacterium genomes that were inspected, only isolates SH31 and S17 encode the arsenic efflux pump Acr3. Strain SH31 was able to grow in up to 10 mM arsenite and 100 mM arsenate, indicating that it is arsenic resistant. Further, expression of the ars operon and acr3 was strongly induced in response to both toxics, suggesting that the arsenic efflux pump Acr3 mediates arsenic resistance in Exiguobacterium sp. SH31.

Highlights

Extremophiles are microorganisms from all three domains of life (Bacteria, Archaea and Eukarya) that grow in the most hostile environments found on Earth, where they must withstand conditions including extreme pH, temperature, salinity, pressure, UV radiation, and the presence of heavy metals or toxic compounds
In agreement with what was found in other isolates, 2992 coding sequences (CDS; including 902 hypothetical proteins), 23 ribosomal RNA genes, and 49 transference RNA genes were identified in strain SH31
Most of the CDS found in Exiguobacterium sp. strain SH31 were annotated using the Clusters of Orthologous Groups (COG) system (2,079 genes annotated; Figure 1A)

Summary

Introduction

Extremophiles are microorganisms from all three domains of life (Bacteria, Archaea and Eukarya) that grow in the most hostile environments found on Earth, where they must withstand conditions including extreme pH, temperature, salinity, pressure, UV radiation, and the presence of heavy metals or toxic compounds. To survive under extreme conditions, microbes finely tune gene expression, modulating the levels of proteins implicated in the response to stress (Duché et al, 2002) Since their discovery, extremophiles have attracted researchers because of their unique physiology, ability to adapt to different environments, and for their potential use in biotechnology (Rothschild and Mancinelli, 2001). Water bodies found in the Altiplano (i.e., shallow lakes, ponds, streams, etc.) are highly diverse, showing different chemical compositions, temperatures, evaporation rates, and depths, among other conditions Together, these factors drive the changing community structure of rich polyextreme microbiota that populates these lakes (Márquez-García et al, 2009; Dorador et al, 2013; Cordero et al, 2014). High concentrations of heavy metals and metalloids, especially arsenic (up to 200 ppm), are found in HAALs, primarily because of the geological foundation (Fernandez-Zenoff et al, 2006; Zenoff et al, 2006; Dib et al, 2009; Farias et al, 2009; Albarracín et al, 2012)

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