Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism

Chernyh, N. A.; Neukirchen, Sinje; Frolov, Evgenii N.; Sousa, Filipa L.; Miroshnichenko, M. L.; Merkel, Alexander Y.; Pimenov, Nikolai V.; Sorokin, Dimitry Y.; Ciordia, Sergio; Mena, Montaña; Ferrer, Manuel; Golyshin, Peter N.; Lebedinsky, Alexander V.; Pereira, Inês A. C.; Bonch-Osmolovskaya, E. A.

doi:10.1038/s41564-020-0776-z

Cited by 37 publications

(49 citation statements)

References 67 publications

(106 reference statements)

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“…The selection was based in one of two criteria. Firstly, a genome was reported in the literature to possess the DsrAB proteins [14,18,45,[56][57][58][59][60][61][62][63][64][65][66][67][68][69][70][71][72]. The presence of DsrAB proteins was validated using the rBBHs of DsrAB proteins following same rBBH strategy as in the complete genome dataset.…”

Section: Methods Validation and Comparisonmentioning

confidence: 99%

“…Similarly to AprAB, the Soe complex, is not specific of the oxidative Dsr-pathway, and SoeABC participate in additional sulphur oxidation pathways [42]. In contrast, in dSRP, the Sat, AprAB and Qmo proteins are strictly needed for the activation of sulphate to APS [43] and its reduction to sulphite [44,45].…”

Section: Significance As a Bioresource To The Communitymentioning

confidence: 99%

“…However, DsrD is not essential to perform sulphate reduction, albeit its conserved genomic arrangement across dSRP indicates a possible regulatory function in this type of metabolism [53,54]. Some cultured micro-organisms are able to use sulphate as an electron acceptor, without the aid of the DsrD protein [45]. Thus, using this protein as a single marker for the distinction between dSRP from other dSOB might lead to incorrect assignments.…”

Section: Significance As a Bioresource To The Communitymentioning

confidence: 99%

“…A second dataset (from now on referred to as the metagenomic dataset) composed of the protein sequences of 193 978 prokaryotic (meta)genomic assemblies and 1900 (meta) genomes belonging to potential new lineages with the ability to use the Dsr-dependent dissimilatory sulphur metabolism [14,18,45,[56][57][58][59][60][61][62][63][64][65][66][67][68][69][70][71][72] was created (Table S3). These additional 1900 (meta)genomes were collected from a survey of recent publications describing potential micro-organisms containing Dsr proteins in the following manner: all assemblies related to the publication BioProject (described or not in the text as a micro-organism having the Dsr pathway) were downloaded and added to the metagenomic dataset, if not already present.…”

Section: Genomic Datasetsmentioning

confidence: 99%

“…The combined results of phylogenetic reconstructions, similarity networks and genomic arrangements led to the identification of paralogous proteins, highly similar to enzymes from the Dsr-pathways. A QmoABC complex distinct from known QmoABCs and whose QmoAB subunits are both closely related with the HdrA subunit of the HdrABC complex was recently identified [ 45 ]. For a better orthologous to paralogous distinction, additional HMM profiles were created using representatives of heterodisulphide reductases from methanogens and Proteobacteria [ 89 ], assimilatory Sat as well as the AprAB-like paralogues previously identified in AprAB sequence similarity searches and/or phylogenies [ 45 ].…”

Section: Introductionmentioning

confidence: 99%

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DiSCo: a sequence-based type-specific predictor of Dsr-dependent dissimilatory sulphur metabolism in microbial data

Neukirchen

Sousa

2021

Microbial Genomics

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Current methods in comparative genomic analyses for metabolic potential prediction of proteins involved in, or associated with the Dsr (dissimilatory sulphite reductase)-dependent dissimilatory sulphur metabolism are both time-intensive and computationally challenging, especially when considering metagenomic data. We developed DiSCo, a Dsr-dependent dissimilatory sulphur metabolism classification tool, which automatically identifies and classifies the protein type from sequence data. It takes user-supplied protein sequences and lists the identified proteins and their classification in terms of protein family and predicted type. It can also extract the sequence data from user-input to serve as basis for additional downstream analyses. DiSCo provides the metabolic functional prediction of proteins involved in Dsr-dependent dissimilatory sulphur metabolism with high levels of accuracy in a fast manner. We ran DiSCo against a dataset composed of over 190 thousand (meta)genomic records and efficiently mapped Dsr-dependent dissimilatory sulphur proteins in 1798 lineages across both prokaryotic domains. This allowed the identification of new micro-organisms belonging to Thaumarchaeota and Spirochaetes lineages with the metabolic potential to use the Dsr-pathway for energy conservation. DiSCo is implemented in Perl 5 and freely available under the GNU GPLv3 at https://github.com/Genome-Evolution-and-Ecology-Group-GEEG/DiSCo.

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Section: Methods Validation and Comparisonmentioning

confidence: 99%

Section: Significance As a Bioresource To The Communitymentioning

confidence: 99%

Section: Significance As a Bioresource To The Communitymentioning

confidence: 99%

Section: Genomic Datasetsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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DiSCo: a sequence-based type-specific predictor of Dsr-dependent dissimilatory sulphur metabolism in microbial data

Neukirchen

Sousa

2021

Microbial Genomics

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Characterization of DsrD and its interaction with the DsrAB dissimilatory sulfite reductase

Barbosa,

Venceslau,

Ferreira

et al. 2024

Protein Science

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Microbial dissimilatory sulfate reduction is a key process in the global sulfur and carbon cycles in anoxic ecosystems. In this anaerobic respiration, sulfate is phosphorylated and reduced to sulfite, which is further reduced to a DsrC‐trisulfide by the dissimilatory sulfite reductase DsrAB. DsrD is a small protein that acts as an allosteric activator of DsrAB, increasing the efficiency of sulfite reduction. Here, we report a detailed study of DsrD and its interaction with DsrAB. Sequence similarity analyses show that there are three groups of DsrD in organisms with a reductive‐type DsrAB. The protein regions involved in the DsrD–DsrAB interaction and activity‐promoting effect were investigated through in vitro and in silico studies, including mutations of conserved DsrD residues. The results reveal that the conserved β‐loop of DsrD is involved in the interaction, contributing to a better understanding of its mechanism of action.

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Structural evolution of the ancient enzyme, dissimilatory sulfite reductase

et al. 2022

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Dissimilatory sulfite reductase is an ancient enzyme that has linked the global sulfur and carbon biogeochemical cycles since at least 3.47 Gya. While much has been learned about the phylogenetic distribution and diversity of DsrAB across environmental gradients, far less is known about the structural changes that occurred to maintain DsrAB function as the enzyme accompanied diversification of sulfate/sulfite reducing organisms (SRO) into new environments. Analyses of available crystal structures of DsrAB from Archaeoglobus fulgidus and Desulfovibrio vulgaris, representing early and late evolving lineages, respectively, show that certain features of DsrAB are structurally conserved, including active siro-heme binding motifs. Whether such structural features are conserved among DsrAB recovered from varied environments, including hot spring environments that host representatives of the earliest evolving SRO lineage (e.g., MV2-Eury), is not known. To begin to overcome these gaps in our understanding of the evolution of DsrAB, structural models from MV2.Eury were generated and evolutionary sequence covariance analyses were conducted on a curated DsrAB database. Phylogenetically diverse DsrAB harbor many conserved functional residues including those that ligate active siroheme(s). However, evolutionary co-variance analysis of monomeric DsrAB subunits revealed several False Positive Evolutionary Couplings (FPEC) that correspond to residues that have co-evolved despite being too spatially distant in the monomeric structure to allow for direct contact. One set of FPECs corresponds to residues that form a structural path between the two active siro-heme moieties across the interface between heterodimers, suggesting the potential for allostery or electron transfer within the enzyme complex. Other FPECs correspond to structural loops and gaps that may have been selected to stabilize enzyme function in different environments. These structural bioinformatics results suggest that DsrAB has maintained allosteric communication pathways between subunits as SRO diversified into new environments. The observations outlined here provide a framework for future biochemical and structural analyses of DsrAB to examine potential allosteric control of this enzyme.

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Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism

Cited by 37 publications

References 67 publications

DiSCo: a sequence-based type-specific predictor of Dsr-dependent dissimilatory sulphur metabolism in microbial data

DiSCo: a sequence-based type-specific predictor of Dsr-dependent dissimilatory sulphur metabolism in microbial data

Characterization of DsrD and its interaction with the DsrAB dissimilatory sulfite reductase

Structural evolution of the ancient enzyme, dissimilatory sulfite reductase

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