Stepwise pathway for early evolutionary assembly of dissimilatory sulfite and sulfate reduction

Funding Information: FLS and SN acknowledge support from the Wiener Wissenschafts, Forschungs- und Technologiefonds (Austria) through the grant VRG15-007. FLS gratefully acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation program (grant agreement 803768). IACP acknowledges support from Fundação para a Ciência e Tecnologia (Portugal) through grants PTDC/BIA-MIC/6512/2014 and PTDC/BIA-BQM/29118/2017, R&D unit MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020), and LS4FUTURE Associated Laboratory (LA/P/0087/2020). The computational results of this work have been achieved using the Life Science Compute Cluster (LiSC) of the University of Vienna. Funding Information: FLS and SN acknowledge support from the Wiener Wissenschafts, Forschungs- und Technologiefonds (Austria) through the grant VRG15-007. FLS gratefully acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation program (grant agreement 803768). IACP acknowledges support from Fundação para a Ciência e Tecnologia (Portugal) through grants PTDC/BIA-MIC/6512/2014 and PTDC/BIA-BQM/29118/2017, R&D unit MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020), and LS4FUTURE Associated Laboratory (LA/P/0087/2020). The computational results of this work have been achieved using the Life Science Compute Cluster (LiSC) of the University of Vienna. Publisher Copyright: © 2023, The Author(s).Microbial dissimilatory sulfur metabolism utilizing dissimilatory sulfite reductases (Dsr) influenced the biochemical sulfur cycle during Earth’s history and the Dsr pathway is thought to be an ancient metabolic process. Here we performed comparative genomics, phylogenetic, and synteny analyses of several Dsr proteins involved in or associated with the Dsr pathway across over 195,000 prokaryotic metagenomes. The results point to an archaeal origin of the minimal DsrABCMK(N) protein set, having as primordial function sulfite reduction. The acquisition of additional Dsr proteins (DsrJOPT) increased the Dsr pathway complexity. Archaeoglobus would originally possess the archaeal-type Dsr pathway and the archaeal DsrAB proteins were replaced with the bacterial reductive-type version, possibly at the same time as the acquisition of the QmoABC and DsrD proteins. Further inventions of two Qmo complex types, which are more spread than previously thought, allowed microorganisms to use sulfate as electron acceptor. The ability to use the Dsr pathway for sulfur oxidation evolved at least twice, with Chlorobi and Proteobacteria being extant descendants of these two independent adaptations.publishersversioninpres

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

Dissimilatory sulfate reduction (DSR)—an important reaction in the biogeochemical sulfur cycle—has been dated to the Palaeoarchaean using geological evidence, but its evolutionary history is poorly understood. Several lineages of bacteria carry out DSR, but in archaea only Archaeoglobus, which acquired DSR genes from bacteria, has been proven to catalyse this reaction. We investigated substantial rates of sulfate reduction in acidic hyperthermal terrestrial springs of the Kamchatka Peninsula and attributed DSR in this environment to Crenarchaeota in the Vulcanisaeta genus. Community profiling, coupled with radioisotope and growth experiments and proteomics, confirmed DSR by ‘Candidatus Vulcanisaeta moutnovskia’, which has all of the required genes. Other cultivated Thermoproteaceae were briefly reported to use sulfate for respiration but we were unable to detect DSR in these isolates. Phylogenetic studies suggest that DSR is rare in archaea and that it originated in Vulcanisaeta, independent of Archaeoglobus, by separate acquisition of qmoABC genes phylogenetically related to bacterial hdrA genes.This work was supported by the Russian Science Foundation (grant number 17-74-30025) and in part by the grant from the Russian Ministry of Science and Higher Education (to N.A.C., A.V.L., E.N.F., M.L.M., A.Y.M., N.V.P. and E.A.B.-O.). Sequencing of PCR amplicons was performed using the scientific equipment of the core research facility ‘Bioengineering’ by T. Kolganova. The proteomics analysis was performed at the Proteomics Facility of the Spanish National Center for Biotechnology (CNB-CSIC), which belongs to ProteoRed, PRB2-ISCIII, supported by grant PT13/0001 (to S.C., M.C.M. and M.F.). P.N.G. acknowledges funding from the UK Biotechnology and Biological Sciences Research Council (BBSRC) within the ERA NET-IB2 programme, grant number ERA-IB-14-030 and the European Union Horizon 2020 Research and Innovation programme (Blue Growth: Unlocking the Potential of Seas and Oceans) under grant agreement number 634486, as well as support from the Centre for Environmental Biotechnology project, part funded by the European Regional Development Fund (ERDF) through the Welsh Government, and support from the Centre of Environmental Biotechnology. D.Y.S. was supported by the SIAM/Gravitation Program (Dutch Ministry of Education, Culture and Science; grant 24002002) and RFBR grant 19-04-00401. F.L.S. and S.N. acknowledge support from the Wiener Wissenschafts, Forschungs- und Technologiefonds (Austria) through the grant VRG15-007. F.L.S. gratefully acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation programme (grant agreement 803768). I.A.C.P. acknowledges support from the Fundação para a Ciência e Tecnologia (Portugal) through grant PTDC/BIA-BQM/29118/2017 and R&D unit MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020)

The Future of Origin of Life Research: Bridging Decades-Old Divisions.

Research on the origin of life is highly heterogeneous. After a peculiar historical development, it still includes strongly opposed views which potentially hinder progress. In the 1st Interdisciplinary Origin of Life Meeting, early-career researchers gathered to explore the commonalities between theories and approaches, critical divergence points, and expectations for the future. We find that even though classical approaches and theories-e.g. bottom-up and top-down, RNA world vs. metabolism-first-have been prevalent in origin of life research, they are ceasing to be mutually exclusive and they can and should feed integrating approaches. Here we focus on pressing questions and recent developments that bridge the classical disciplines and approaches, and highlight expectations for future endeavours in origin of life research

Supplementary Data of "Stepwise pathway for early evolutionary assembly of dissimilatory sulfite and sulfate reduction"

   Sinje Neukirchen1, Inês A. C. Pereira2, Filipa L. Sousa1* 1 Genome Evolution and Ecology Group, Department of Functional and Evolutionary Ecology, University of Vienna, Djerassiplatz 1, 1030 Wien, Austria 2 Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Av. da República, 2780-157 Oeiras, Portugal.    Supplementary Data 1 – FASTA files containing all amino acid sequences including the NCBI RefSeq/GenBank/IMG accession numbers per protein. Supplementary Data 2 – Mapping table of selected sequences after 90 % global identity redundancy reduction to the corresponding protein sequence accession numbers, genome identifiers, and taxonomic affiliation. Supplementary Data 3 – Trimmed multiple sequence alignments of protein sequences present in only complete genomes. Supplementary Data 4 – Trimmed multiple sequence alignments of protein sequences covering the full diversity including metagenome-derived genomic assemblies. Supplementary Data 5 – Phylogenetic reconstruction of protein sequences present in only complete genomes using ModelFinder with best model selection. Supplementary Data 6 – Phylogenetic reconstruction of protein sequences covering the full diversity including metagenome-derived genomic assemblies using ModelFinder with best model selection. Supplementary Data 7 – Phylogenetic reconstruction of protein sequences present in only complete genomes using the model LG+I+G4. Supplementary Data 8 – Phylogenetic reconstruction of protein sequences covering the full diversity including metagenome-derived genomic assemblies using the model LG+I+G4.       </p

Physiology, phylogeny, and LUCA

Genomes record their own history. But if we want to look all the way back to life’s beginnings some 4 billion years ago, the record of microbial evolution that is preserved in prokaryotic genomes is not easy to read. Microbiology has a lot in common with geology in that regard. Geologists know that plate tectonics and erosion have erased much of the geological record, with ancient rocks being truly rare. The same is true of microbes. Lateral gene transfer (LGT) and sequence divergence have erased much of the evolutionary record that was once written in genomes, and it is not obvious which genes among sequenced genomes are genuinely ancient. Which genes trace to the last universal ancestor, LUCA? The classical approach has been to look for genes that are universally distributed. Another approach is to make all trees for all genes, and sift out the trees where signals have been overwritten by LGT. What is left ought to be ancient. If we do that, what do we find

Physiology, phylogeny, and LUCA

Genomes record their own history. But if we want to look all the way back to life’s beginnings some 4 billion years ago, the record of microbial evolution that is preserved in prokaryotic genomes is not easy to read. Microbiology has a lot in common with geology in that regard. Geologists know that plate tectonics and erosion have erased much of the geological record, with ancient rocks being truly rare. The same is true of microbes. Lateral gene transfer (LGT) and sequence divergence have erased much of the evolutionary record that was once written in genomes, and it is not obvious which genes among sequenced genomes are genuinely ancient. Which genes trace to the last universal ancestor, LUCA? The classical approach has been to look for genes that are universally distributed. Another approach is to make all trees for all genes, and sift out the trees where signals have been overwritten by LGT. What is left ought to be ancient. If we do that, what do we find

The future of origin of life research: Bridging decades-old divisions

Research on the origin of life is highly heterogeneous. After a peculiar historical development, it still includes strongly opposed views which potentially hinder progress. In the 1st Interdisciplinary Origin of Life Meeting, early-career researchers gathered to explore the commonalities between theories and approaches, critical divergence points, and expectations for the future. We find that even though classical approaches and theories—e.g. bottom-up and top-down, RNA world vs. metabolism-first—have been prevalent in origin of life research, they are ceasing to be mutually exclusive and they can and should feed integrating approaches. Here we focus on pressing questions and recent developments that bridge the classical disciplines and approaches, and highlight expectations for future endeavours in origin of life research