A protein trisulfide couples dissimilatory sulfate reduction to energy conservation

Santos, Andrea M.; Venceslau, Sofia S.; Grein, Fabian; Leavitt, William D.; Dahl, Christiane; Johnston, David T.; Pereira, Inês A. C.

doi:10.1126/science.aad3558

Cited by 206 publications

(240 citation statements)

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“…3A) 30,31 . DsrC, specifically, dictates sulfur metabolism rates, as it provides the sulfur substrate to DsrAB-sulfite reductase for processing 32 . A conserved C-terminal motif with two cysteine residues CysBX10CysA is essential for this function.…”

mentioning

confidence: 99%

Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses

Roux

Brum

Dutilh

et al. 2016

Nature

622

815

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Tara Oceans CoordinatorsInternational audienceOcean microbes drive biogeochemical cycling on a global scale. However, this cycling is constrained by viruses that affect community composition, metabolic activity, and evolutionary trajectories. Owing to challenges with the sampling and cultivation of viruses, genome-level viral diversity remains poorly described and grossly understudied, with less than 1% of observed surface-ocean viruses known. Here we assemble complete genomes and large genomic fragments from both surface- and deep-ocean viruses sampled during the Tara Oceans and Malaspina research expeditions, and analyse the resulting ‘global ocean virome’ dataset to present a global map of abundant, double-stranded DNA viruses complete with genomic and ecological contexts. A total of 15,222 epipelagic and mesopelagic viral populations were identified, comprising 867 viral clusters (defined as approximately genus-level groups. This roughly triples the number of known ocean viral populations and doubles the number of candidate bacterial and archaeal virus genera, providing a near-complete sampling of epipelagic communities at both the population and viral-cluster level. We found that 38 of the 867 viral clusters were locally or globally abundant, together accounting for nearly half of the viral populations in any global ocean virome sample. While two-thirds of these clusters represent newly described viruses lacking any cultivated representative, most could be computationally linked to dominant, ecologically relevant microbial hosts. Moreover, we identified 243 viral-encoded auxiliary metabolic genes, of which only 95 were previously known. Deeper analyses of four of these auxiliary metabolic genes (dsrC, soxYZ, P-II (also known as glnB) and amoC) revealed that abundant viruses may directly manipulate sulfur and nitrogen cycling throughout the epipelagic ocean. This viral catalog and functional analyses provide a necessary foundation for the meaningful integration of viruses into ecosystem models where they act as key players in nutrient cycling and trophic networks

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confidence: 99%

Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses

Roux

Brum

Dutilh

et al. 2016

Nature

622

815

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“…The formation of the Fe-S bond between siroheme and sulfite may be the critical reaction controlling isotope fractionation. Following this, sulfite is reduced by the transfer of two electrons to form a S 2+ intermediate (Santos et al, 2015). Under in vivo conditions, the sulfur intermediate was suggested to be withdrawn from the DsrAB complex by the small transfer protein DsrC (Oliveira et al, 2008b;Venceslau et al, 2014), and this has been recently demonstrated (Santos et al, 2015).…”

Section: Fractionation At the Intracellular Scalementioning

confidence: 96%

“…Following this, sulfite is reduced by the transfer of two electrons to form a S 2+ intermediate (Santos et al, 2015). Under in vivo conditions, the sulfur intermediate was suggested to be withdrawn from the DsrAB complex by the small transfer protein DsrC (Oliveira et al, 2008b;Venceslau et al, 2014), and this has been recently demonstrated (Santos et al, 2015). Under in vitro conditions, DsrC is generally absent, and the reduced sulfur in the active site may react with excess sulfite, forming thiosulfate and trithionate (Figure 1; Drake and Akagi, 1976).…”

Section: Fractionation At the Intracellular Scalementioning

confidence: 99%

“…The subsequent reduction occurs via electron transfer from an adjacent Fe-S cluster (Oliveira et al, 2008a,b;Parey et al, 2010). In vivo, DsrAB has been proposed to generate intermediate valence sulfur, which is then bound to DsrC and converted to sulfide via DsrC/MK (Oliveira et al, 2008b;Venceslau et al, 2013Venceslau et al, , 2014Santos et al, 2015). Sulfide then leaves the cell by diffusion (as H 2 S) (Mathai et al, 2009) or through anion transport (as HS − or S 2− ) (Czyzewski and Wang, 2012), though the mechanism of sulfide exit in MSR is still not well known.…”

Section: Introductionmentioning

confidence: 99%

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Sulfur Isotope Effects of Dissimilatory Sulfite Reductase

Leavitt

Bradley

Santos

et al. 2015

Preprint

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The precise interpretation of environmental sulfur isotope records requires a quantitative understanding of the biochemical controls on sulfur isotope fractionation by the principle isotope-fractionating process within the S cycle, microbial sulfate reduction (MSR). Here we provide the only direct observation of the major ( 34 S/ 32 S) and minor ( 33 S/ 32 S, 36 S/ 32 S) sulfur isotope fractionations imparted by a central enzyme in the energy metabolism of sulfate reducers, dissimilatory sulfite reductase (DsrAB). Results from in vitro sulfite reduction experiments allow us to calculate the in vitro DsrAB isotope effect in 34 S/ 32 S (hereafter, 34 ε ‰ DsrAB ) to be 15.3 ± 2 , 2σ. The accompanying minor isotope effect in 33 S, described as 33 λ DsrAB , is calculated to be 0.5150 ± 0.0012, 2σ. These observations facilitate a rigorous evaluation of the isotopic fractionation associated with the dissimilatory MSR pathway, as well as of the environmental variables that govern the overall magnitude of fractionation by natural communities of sulfate reducers. The isotope effect induced by DsrAB upon sulfite reduction is a factor of 0.3-0.6 times prior indirect estimates, which have ranged from 25 to 53‰ in 34 ε DsrAB . The minor isotope fractionation observed from DsrAB is consistent with a kinetic or equilibrium effect. Our in vitro constraints on the magnitude of 34 ε DsrAB is similar to the median value of experimental observations compiled from all known published work, where 34 ε r−p = 16.1 (r-p indicates reactant vs. product, n = 648). This value closely matches those of MSR operating at high sulfate reduction rates in both laboratory chemostat experiments ( 34 ε SO4− = H2S17.3 ± 1.5 , 2σ) and in modern marine sediments ( 34 ε SO4− = H2S17.3 ± 3.8 ). Targeting the direct isotopic consequences of a specific enzymatic processes is a fundamental step toward a biochemical foundation for reinterpreting the biogeochemical and geobiological sulfur isotope records in modern and ancient environments.

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“…is important in evolution, whether carbon (2,3), sulfur (4,5), nitrogen (6), or the geochemical context of physiology (7). Dickerson's quote also puts a very natural and nonchalant 1980s mention of lateral gene transfer (LGT) into the picture of microbial evolution as a common component of genetic variation among prokaryotes, long before people were debating the significance of LGT in prokaryote evolution.…”

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confidence: 99%

Physiology, phylogeny, and the energetic roots of life

Martin

2017

Period Biol

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Before the days of molecular phylogenies, the standard way of viewing microbial evolution was as process of physiological evolution: the ordering of the sequence of events in which different pathways that microbes use to harness carbon and energy arose. The physiological view of microbial evolution was, of course, replaced in the 1980s by a gene centered view of microbial evolution that was built around the ribosomal RNA tree of life, also called the universal tree or the three domain tree. The universal tree installed long sought order into microbial systematics, but left physiological evolution out in the cold, because physiology never mapped properly onto the rRNA tree. LGT decoupLes physioLoGy from phyLoGeny T he foregoing quote from Dickerson (1) typifies a physiological view of evolution, one in which lateral gene transfer between prokaryotes is normal and distributes metabolic capabilities among lineages. Almost four decades later, the quote is still quite modern. It embodies a particular approach to understanding microbial evolution, a view from the standpoint of physiology -the chemical reactions at the core of carbon and energy metabolism that drive the process of life forward. Physiology is important in evolution, whether carbon (2, 3), sulfur (4, 5), nitrogen (6), or the geochemical context of physiology (7). Dickerson's quote also puts a very natural and nonchalant 1980s mention of lateral gene transfer (LGT) into the picture of microbial evolution as a common component of genetic variation among prokaryotes, long before people were debating the significance of LGT in prokaryote evolution. It even goes so far as to say that That was not because the universal tree had an incorrect branching pattern. Rather it was because physiological characters have never mapped neatly onto any phylogenetic tree for prokaryotes, regardless of its topology. The reason is that prokaryotes, though they have an undeniable tendency to vertically inherit their ribosome, distribute the physiological traits that enable synthesis of ribosomes via lateral gene transfer (LGT).LGT could possibly transform non-respiring lineages into respiring lineages via the transfer of many genes, something that we now know does actually occur during microbial evolution (8).Dickerson noted that the "evolutionary record" of microbes might have been scrambled. We have concepts about microbial evolution that are based on their evolutionary record, but what is the evolutionary record of microbes? What is it made of? It would appear that for microbial evolution there are only two kinds of records: geological and genomic. It is said that Earth records its own history (9), so do genomes. Putting geological and genomic evidence into a consistent picture of microbial evolution is a challenging undertaking, but that is the deliverable if we want a fuller picture of microbial evolution. Yet the only real connection between the two kinds of substance of the microbial evolutionary record -rocks and genes -is physiology. Physiology is arguably what...

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A protein trisulfide couples dissimilatory sulfate reduction to energy conservation

Cited by 206 publications

References 40 publications

Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses

Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses

Sulfur Isotope Effects of Dissimilatory Sulfite Reductase

Physiology, phylogeny, and the energetic roots of life

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