Molybdenum and tungsten oxygen transferases – structural and functional diversity within a common active site motif

Pushie, M. Jake; Cotelesage, Julien J. H.; George, Graham N.

doi:10.1039/c3mt00177f

Cited by 47 publications

(50 citation statements)

References 99 publications

(140 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…2 ). This property is in line with the general observation that biologically relevant (IV/V/VI) redox transitions occur at lower redox potentials in W than in Mo complexes; consequently, W is generally preferred over Mo in low-potential redox catalysis [Andreesen and Makdessi, 2008;L'vov et al, 2002;Pushie et al, 2014;Roy and Adams, 2002]. However, there are also a few exceptions, e.g.…”

Section: Introductionsupporting

confidence: 47%

“…In most cases, Mo/W enzymes have a preference for either of the respective transition metals [Andreesen and Makdessi, 2008;L'vov et al, 2002;Pushie et al, 2014;Rothery and Weiner, 2015]. However, there are also reports on the presence/exchange of both metals in formate dehydrogenases (FDHs) [Hartmann et al, 2014].…”

Section: Introductionmentioning

confidence: 99%

“…1 ). For recent general reviews of Mo/W enzymes see previously published studies [Bevers et al, 2009;Hille, 2013;Hille et al, 2014;Pushie et al, 2014;Romao, 2009;Schwarz et al, 2009].…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Structure and Function of the Unusual Tungsten Enzymes Acetylene Hydratase and Class II Benzoyl-Coenzyme A Reductase

et al. 2016

View full text Add to dashboard Cite

In biology, tungsten (W) is exclusively found in microbial enzymes bound to a bis-pyranopterin cofactor (bis-WPT). Previously known W enzymes catalyze redox oxo/hydroxyl transfer reactions by directly coordinating their substrates or products to the metal. They comprise the W-containing formate/formylmethanofuran dehydrogenases belonging to the dimethyl sulfoxide reductase (DMSOR) family and the aldehyde:ferredoxin oxidoreductase (AOR) families, which form a separate enzyme family within the Mo/W enzymes. In the last decade, initial insights into the structure and function of two unprecedented W enzymes were obtained: the acetaldehyde forming acetylene hydratase (ACH) belongs to the DMSOR and the class II benzoyl-coenzyme A (CoA) reductase (BCR) to the AOR family. The latter catalyzes the reductive dearomatization of benzoyl-CoA to a cyclic diene. Both are key enzymes in the degradation of acetylene (ACH) or aromatic compounds (BCR) in strictly anaerobic bacteria. They are unusual in either catalyzing a nonredox reaction (ACH) or a redox reaction without coordinating the substrate or product to the metal (BCR). In organic chemical synthesis, analogous reactions require totally nonphysiological conditions depending on Hg²⁺ (acetylene hydration) or alkali metals (benzene ring reduction). The structural insights obtained pave the way for biological or biomimetic approaches to basic reactions in organic chemistry.

show abstract

Section: Introductionsupporting

confidence: 47%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Structure and Function of the Unusual Tungsten Enzymes Acetylene Hydratase and Class II Benzoyl-Coenzyme A Reductase

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Cadmium has been shown to stimulate Thalassiosira weissflogii under Zn limiting conditions because it is used in an alternative form of carbonic anhydrase, the enzyme that facilitates the interconversion of dissolved bicarbonate to CO 2 , and vice versa (Lane and Morel, 2000). Tungsten is used by primitive anaerobic prokaryotes and mostly filled roles now played by Mo (Williams et al, 2002;Pushie et al, 2014). Hence, W may also play a key role in the biogeochemical cycling of N prior to the Neoproterozoic.…”

Section: Metals Remaining To Be Investigatedmentioning

confidence: 99%

Trace elements at the intersection of marine biological and geochemical evolution

Robbins

Lalonde

Planavsky

et al. 2016

Earth-Science Reviews

159

View full text Add to dashboard Cite

Life requires a wide variety of bioessential trace elements to act as structural components and reactive centers in metalloenzymes. These requirements differ between organisms and have evolved over geological time, likely guided in some part by environmental conditions. Until recently, most of what was understood regarding trace element concentrations in the Precambrian oceans was inferred by extrapolation, geochemical modeling, and/or genomic studies. However, in the past decade, the increasing availability of trace element and isotopic data for sedimentary rocks of all ages have yielded new, and potentially more direct, insights into secular changes in seawater composition -and ultimately the evolution of the marine biosphere. Compiled records of many bioessential trace elements (including Ni, Mo, P, Zn, Co, Cr, Se, and I) provide new insight into how trace element abundance in Earth's ancient oceans may have been linked to biological evolution. Several of these trace elements display redox-sensitive behavior, while others are redox-sensitive but not bioessential (e.g., Cr, U). Their temporal trends in sedimentary archives provide useful constraints on changes in atmosphere-ocean redox conditions that are linked to biological evolution, for example, the activity of oxygen-producing, photosynthetic cyanobacteria. In this review, we summarize available Precambrian trace element proxy data, and discuss how temporal trends in the seawater concentrations of specific trace elements may be linked to the evolution of both simple and complex life. We also examine several biologically relevant and/or redox-sensitive trace elements that have yet to be fully examined in the A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT3 sedimentary rock record (e.g., Cu, Cd, W) and suggest several directions for future studies.

show abstract

“…Indeed, tungsten and molybdenum have such similar chemical and physical properties that almost all microorganisms cannot distinguish between them and often times incorporate tungsten into their molybdoenzymes. This typically renders them nonfunctional (11), although tungsten can be incorporated into some members of the DMSOR family (formate dehydrogenase, formyl methanofuran dehydrogenase, and acetylene hydratase) to yield active enzyme (12). Only a very few microorganisms are known to absolutely require tungsten for growth, and they incor-porate it into the so-called true family of tungstoenzymes represented by aldehyde ferredoxin oxidoreductase (AOR) (12,13).…”

mentioning

confidence: 99%

A New Class of Tungsten-Containing Oxidoreductase in Caldicellulosiruptor, a Genus of Plant Biomass-Degrading Thermophilic Bacteria

Scott

Rubinstein

Lipscomb

et al. 2015

Appl Environ Microbiol

View full text Add to dashboard Cite

bCaldicellulosiruptor bescii grows optimally at 78°C and is able to decompose high concentrations of lignocellulosic plant biomass without the need for thermochemical pretreatment. C. bescii ferments both C 5 and C 6 sugars primarily to hydrogen gas, lactate, acetate, and CO 2 and is of particular interest for metabolic engineering applications given the recent availability of a genetic system. Developing optimal strains for technological use requires a detailed understanding of primary metabolism, particularly when the goal is to divert all available reductant (electrons) toward highly reduced products such as biofuels. During an analysis of the C. bescii genome sequence for oxidoreductase-type enzymes, evidence was uncovered to suggest that the primary redox metabolism of C. bescii has a completely uncharacterized aspect involving tungsten, a rarely used element in biology. An active tungsten utilization pathway in C. bescii was demonstrated by the heterologous production of a tungsten-requiring, aldehyde-oxidizing enzyme (AOR) from the hyperthermophilic archaeon Pyrococcus furiosus. Furthermore, C. bescii also contains a tungsten-based AOR-type enzyme, here termed XOR, which is phylogenetically unique, representing a completely new member of the AOR tungstoenzyme family. Moreover, in C. bescii, XOR represents ca. 2% of the cytoplasmic protein. XOR is proposed to play a key, but as yet undetermined, role in the primary redox metabolism of this cellulolytic microorganism.T hermophilic bacteria of the genus Caldicellulosiruptor are currently under intense investigation due to their ability to decompose lignocellulosic plant biomass anaerobically at high temperature, thereby potentially mitigating costly thermochemical pretreatment steps (1, 2). One of these species, Caldicellulosiruptor bescii, has an optimal growth temperature of 78°C and is the most thermophilic cellulose degrader known to date. It is able to ferment high concentrations of cellulosic feedstock primarily to hydrogen gas, lactate, acetate, and CO 2 (3, 4). Species from this genus can degrade cellulose (and also xylan), using novel multidomain glycosyl hydrolases, representing a new paradigm in cellulose conversion by anaerobic thermophiles (2). Moreover, the recent development of a genetic system for C. bescii creates potential for using this and related species for consolidated biomass processing in the production of liquid fuels (5).Developing metabolic engineering strategies for any microorganism obviously requires an in-depth understanding of their primary metabolism. Evidence that C. bescii may have a completely uncharacterized aspect to its primary redox metabolism came from an analysis of its genome sequence for molybdoenzymes (6). These are present in virtually all forms of life, serving diverse roles in primary metabolism of carbon, nitrogen and sulfur (7). As expected, we found that the C. bescii genome contains genes necessary for the synthesis of the pyranopterin cofactor that coordinates molybdenum (Mo) in such enzymes (7). Accordin...

show abstract

Molybdenum and tungsten oxygen transferases – structural and functional diversity within a common active site motif

Cited by 47 publications

References 99 publications

Structure and Function of the Unusual Tungsten Enzymes Acetylene Hydratase and Class II Benzoyl-Coenzyme A Reductase

Structure and Function of the Unusual Tungsten Enzymes Acetylene Hydratase and Class II Benzoyl-Coenzyme A Reductase

Trace elements at the intersection of marine biological and geochemical evolution

A New Class of Tungsten-Containing Oxidoreductase in Caldicellulosiruptor, a Genus of Plant Biomass-Degrading Thermophilic Bacteria

Contact Info

Product

Resources

About