Arsenic hypertolerance in the protist Euglena mutabilis is mediated by specific transporters and functional integrity maintenance mechanisms

Abstract

Arsenic is a toxic metalloid known to cause multiple and severe cellular damages, including lipid peroxidation, protein misfolding, mutagenesis and double and single-stranded DNA breaks. Thus, exposure to this compound is lethal for most organisms but some species such as the photosynthetic protist Euglena mutabilis are able to cope with very high concentrations of this metalloid. Our comparative transcriptomic approaches performed on both an arsenic hypertolerant protist, i.e. E. mutabilis, and a more sensitive one, i.e. E. gracilis, revealed multiple mechanisms involved in arsenic tolerance. Indeed, E. mutabilis prevents efficiently the accumulation of arsenic in the cell through the expression of several transporters. More surprisingly, this protist induced the expression of active DNA reparation and protein turnover mechanisms, which allow E. mutabilis to maintain functional integrity of the cell under challenging conditions. Our observations suggest that this protist has acquired specific functions regarding arsenic and has developed an original metabolism to cope with acid mine drainages-related stresses.

Meneco, a Topology-Based Gap-Filling Tool Applicable to Degraded Genome-Wide Metabolic Networks

“…Due to their complexity and size, no genome sequences are available so far within the genus Euglena . Therefore, we used assembled transcript sequences as described in [ 18 ] and annotated them by similarity search against enzyme reference sequences from MetaCyc. We used a stringent similarity threshold for function assignation to reduce as much as possible the rate of false positive reactions included in the initial network that was subsequently completed by .…”

“…Despite the crucial role of E. mutabilis in these ecosystems and the fact that it has often been considered as an indicator species for acid mine drainages (AMDs), this organism has only been poorly described so far, in contrast to another species of the same genus, Euglena gracilis . The available data for E. mutabilis consists in assembled transcript sequences obtained from de novo transcriptomics and metabolomics experiments previously published in [ 18 ] and in [ 19 ], respectively. This sparse dataset prevented us from using most of the tools described above to construct a metabolic network: the absence of a sequenced genome for the Euglena genus and the fact that this genus is not closely related to any common model organism rendered taxonomy-based methods of network reconstruction unusable [ 10 , 11 ].…”

“…Our second case study presents the first metabolic network for E. mutabilis , based on transcript sequences assembled from previously published transcriptomic and metabolomic data [ 18 ] [ 19 ]. In order to complete this draft with , we selected a set of targets from the list of metabolites that E. mutabilis can accumulate or secrete in minimum mineral medium [ 19 ].…”

Recurrent horizontal transfer of arsenite methyltransferase genes facilitated adaptation of life to arsenic

“…The endosymbiotically-transferred arsM gene logically would have allowed N. gruberi to adapt to high arsenic concentrations in its ecological niche. For example, the capacity for As(III) methylation provides Euglena gracilis , a protist related to N. gruberi , with a distinct arsenite metabolism that allows it to cope with arsenic stress in an acid drainage environment 54 . In addition, fusion of putative arsM genes and selenophosphate synthetase (SelD), as observed in the genome of N. gruberi , is advantageous to a free-living protist faced with potentially threatening environments 55 , 56 .…”

Metabolic response of Agrobacterium tumefaciens 5A to arsenite

“…The studies of microbe-arsenic interactions have progressed to where there is now a foundational understanding of how microbes detect and respond to arsenic. These studies have primarily concerned various major arsenic redox transformations or resistance mechanisms (Stolz and Oremland, 1999;Rosen, 2002;Oremland and Stolz, 2003;Silver and Phung, 2005) as well as non-targeted assessments of arsenic effects at more global levels using proteomics (Parvatiyar et al, 2005;Carapito et al, 2006;Muller et al, 2007;Weiss et al, 2009;Pandey et al, 2012;Andres et al, 2013;Belfiore et al, 2013;Sacheti et al, 2014;Thomas et al, 2014;Ge et al, 2016) and transcriptomics Andres et al, 2013;Sanchez-Riego et al, 2014;Halter et al, 2015). A central theme that has emerged from each study is that As(III) exposure induces bacterial functions directly related to arsenic transformations or resistance (e.g., arsC, arsB and aioBA.…”