Analysis of the Genome and Mobilome of a Dissimilatory Arsenate Reducing Aeromonas sp. O23A Reveals Multiple Mechanisms for Heavy Metal Resistance and Metabolism.

Witold Uhrynowski,Leszek Lipinski,Lukasz Dziewit,Dorota Adamska,Pawel S Krawczyk,Lukasz Drewniak,Monika Radlinska,Przemyslaw Decewicz

doi:10.3389/fmicb.2017.00936

Abstract

Aeromonas spp. are among the most ubiquitous microorganisms, as they have been isolated from different environmental niches including waters, soil, as well as wounds and digestive tracts of poikilothermic animals and humans. Although much attention has been paid to the pathogenicity of Aeromonads, the role of these bacteria in environmentally important processes, such as transformation of heavy metals, remains to be discovered. Therefore, the aim of this study was a detailed genomic characterization of Aeromonas sp. O23A, the first representative of this genus capable of dissimilatory arsenate reduction. The strain was isolated from microbial mats from the Zloty Stok mine (SW Poland), an environment strongly contaminated with arsenic. Previous physiological studies indicated that O23A may be involved in both mobilization and immobilization of this metalloid in the environment. To discover the molecular basis of the mechanisms behind the observed abilities, the genome of O23A (∼5.0 Mbp) was sequenced and annotated, and genes for arsenic respiration, heavy metal resistance (hmr) and other phenotypic traits, including siderophore production, were identified. The functionality of the indicated gene modules was assessed in a series of minimal inhibitory concentration analyses for various metals and metalloids, as well as mineral dissolution experiments. Interestingly, comparative analyses revealed that O23A is related to a fish pathogen Aeromonas salmonicida subsp. salmonicida A449 which, however, does not carry genes for arsenic respiration. This indicates that the dissimilatory arsenate reduction ability may have been lost during genome reduction in pathogenic strains, or acquired through horizontal gene transfer. Therefore, particular emphasis was placed upon the mobilome of O23A, consisting of four plasmids, a phage, and numerous transposable elements, which may play a role in the dissemination of hmr and arsenic metabolism genes in the environment. The obtained results indicate that Aeromonas sp. O23A is well-adapted to the extreme environmental conditions occurring in the Zloty Stok mine. The analysis of genome encoded traits allowed for a better understanding of the mechanisms of adaptation of the strain, also with respect to its presumable role in colonization and remediation of arsenic-contaminated waters, which may never have been discovered based on physiological analyses alone.

Highlights

Aeromonads are ubiquitous microorganisms found in different environmental niches such as fresh and marine waters, sediments and soil (e.g., Dumontet et al, 2000)
Aeromonads are known for their ubiquitous nature, which is to a great extent determined by the carried pool of genes, and especially those found within mobile genetic elements
Genomic research is mostly focused on clinically important determinants of these bacteria, such as antibiotic resistance genes, and much less attention is being paid to other adaptive genes, related to, e.g., heavy metal resistance

Summary

Introduction

Aeromonads are ubiquitous microorganisms found in different environmental niches such as fresh and marine waters, sediments and soil (e.g., Dumontet et al, 2000). Environmental isolates of Aeromonas spp. are known to affect the cycle of inorganic and organic matter in the environment (e.g., Wang et al, 2009; Watts and Lloyd, 2013) This is the case for arsenic, a metalloid, which constitutes a particular threat to living organisms due to its high toxicity, but to which many microorganisms, including Aeromonads, evolved resistance (Drewniak et al, 2010). Given the ubiquitousness and versatility of metabolism of Aeromonas spp., only two dissimilatory arsenate reducing strains belonging to this genus have so far been described: O23A (Drewniak et al, 2010) and OM4 (Drewniak et al, 2014). Both the strains originate from an ancient gold mine in Zloty Stok (SW Poland)

Objectives

Methods

Results

Conclusion