Flavoprotein-Mediated Tellurite Reduction: Structural Basis and Applications to the Synthesis of Tellurium-Containing Nanostructures

Abstract

The tellurium oxyanion tellurite (TeO32-) is extremely harmful for most organisms. It has been suggested that a potential bacterial tellurite resistance mechanism would consist of an enzymatic, NAD(P)H-dependent, reduction to the less toxic form elemental tellurium (Te0). To date, a number of enzymes such as catalase, type II NADH dehydrogenase and terminal oxidases from the electron transport chain, nitrate reductases, and dihydrolipoamide dehydrogenase (E3), among others, have been shown to display tellurite-reducing activity. This activity is generically referred to as tellurite reductase (TR). Bioinformatic data resting on some of the abovementioned enzymes enabled the identification of common structures involved in tellurite reduction including vicinal catalytic cysteine residues and the FAD/NAD(P)+-binding domain, which is characteristic of some flavoproteins. Along this line, thioredoxin reductase (TrxB), alkyl hydroperoxide reductase (AhpF), glutathione reductase (GorA), mercuric reductase (MerA), NADH: flavorubredoxin reductase (NorW), dihydrolipoamide dehydrogenase, and the putative oxidoreductase YkgC from Escherichia coli or environmental bacteria were purified and assessed for TR activity. All of them displayed in vitro TR activity at the expense of NADH or NADPH oxidation. In general, optimal reducing conditions occurred around pH 9–10 and 37°C. Enzymes exhibiting strong TR activity produced Te-containing nanostructures (TeNS). While GorA and AhpF generated TeNS of 75 nm average diameter, E3 and YkgC produced larger structures (>100 nm). Electron-dense structures were observed in cells over-expressing genes encoding TrxB, GorA, and YkgC.

Peer Review #1 of "Comparative genomic analysis of a new tellurite-resistant Psychrobacter strain isolated from the Antarctic Peninsula (v0.3)"

“…Psychrophilic and psychrotolerant microorganisms require several genes to increase their phenotypic flexibility to survive in extreme environments such as cold habitats. Thus, in addition to genes associated with cold shock proteins, membrane fluidity, among others, the presence of metal(loid) resistance genes seems to favor their adaptation (Dziewit and Bartosik, 2014;Rodríguez-Rojas et al, 2016). This is also the case of P. glacincola BNF20, which harbors over 100 putative metal resistance genes (Supplementary Table 2).…”

“…Some of the genes implicated in tellurite resistance include trgAB from Rhodobacter sphaeroides (unknown function, encoding likely membrane-associated proteins) (O´Gara et al, 1997), tmp from Pseudomonas syringae (encoding a thiopurine methyltransferase, involved in tellurium alkylation) (Prigent-Combaret et al, 2012), lpdA from Aeromonas caviae ST (encoding dihydrolipoamide dehydrogenase, involved in tellurite reduction) (Castro et al, 2008) and gor from Pseudomonas sp. (encoding glutathione reductase, involved in tellurite reduction) (Arenas et al, 2016;Pugin et al, 2014). Tellurite resistance genes were also identified in the ter operon (terZABCDEF) from Escherichia coli and other pathogenic species (Taylor, 1999;Whelan et al, 1997).…”

Synthesis and Antibacterial Activity of Metal(loid) Nanostructures by Environmental Multi-Metal(loid) Resistant Bacteria and Metal(loid)-Reducing Flavoproteins

“…Metal(loid) reduction by microbial systems could be of great help in decontaminating soluble metal ions from soils, forming insoluble, less-toxic derivatives that often generate metal arrangements at the nanoscale (Narayanan and Sakthivel, 2010 ; Thakkar et al, 2010 ), also known as nanostructures (NS) exhibiting one or more dimensions <100 nm. Gold (Correa-Llantén et al, 2013 ), selenium (Song et al, 2017 ), silver (Gurunathan et al, 2009 ), tellurium (Arenas-Salinas et al, 2016 ), and uranium (Suresh, 2012 ) NS have been reported, opening a great interest because of their potential application in the field of biotechnology.…”

“…A number of flavoproteins able of metal ion reduction to less toxic, insoluble forms have been described, including (i) mercury reductase (MerA) (Silver and Phung, 2005 ), (ii) glutathione reductase (Au 3+ and reduction, Pugin et al, 2014 ), (iii) fumarate reductase (selenite reduction, Song et al, 2017 ), (iv) thioredoxin reductase and alkyl hydroperoxide reductase that reduce tellurite (Arenas-Salinas et al, 2016 ) and (v) nitrate reductase, able to reduce tellurite as well as silver (Kumar et al, 2007 ).…”

Comparative genomic analysis of a new tellurite-resistantPsychrobacterstrain isolated from the Antarctic Peninsula

“…Some of the genes implicated in tellurite resistance include trgAB from Rhodobacter sphaeroides (unknown function, encoding likely membrane-associated proteins) ( O’Gara, Gomelsky & Kaplan, 1997 ), tmp from Pseudomonas syringae (encoding a thiopurine methyltransferase, involved in tellurium alkylation) ( Prigent-Combaret et al, 2012 ), lpdA from Aeromonas caviae ST (encoding dihydrolipoamide dehydrogenase, involved in tellurite reduction) ( Castro et al, 2008 ) and gor from Pseudomonas sp. (encoding glutathione reductase, involved in tellurite reduction) ( Arenas et al, 2016 ; Pugin et al, 2014 ). Tellurite resistance genes were also identified in the ter operon ( terZABCDEF ) from Escherichia coli and other pathogenic species ( Taylor, 1999 ; Whelan, Sherburne & Taylor, 1997 ).…”