Genome analyses of the carboxydotrophic sulfate-reducers Desulfotomaculum nigrificans and Desulfotomaculum carboxydivorans and reclassification of Desulfotomaculum caboxydivorans as a later synonym of Desulfotomaculum nigrificans
Wageningen University and Research Centre1, Russian Academy of Sciences2, University of Minho3, Universidade Nova de Lisboa4, University of Amsterdam5, Los Alamos National Laboratory6, Joint Genome Institute7, Saint Petersburg State University8, Saint Petersburg Academic University9, Leibniz Association10
TL;DR: The genomes of both strains were compared to reveal their differences and led to a reclassification of D. carboxydivorans as a later heterotypic synonym ofD.
Abstract: Desulfotomaculum nigrificans and D. carboxydivorans are moderately thermophilic members of the polyphyletic spore-forming genus Desulfotomaculum in the family Peptococcaceae. They are phylogenetically very closely related and belong to ‘subgroup a’ of the Desulfotomaculum cluster 1. D. nigrificans and D. carboxydivorans have a similar growth substrate spectrum; they can grow with glucose and fructose as electron donors in the presence of sulfate. Additionally, both species are able to ferment fructose, although fermentation of glucose is only reported for D. carboxydivorans. D. nigrificans is able to grow with 20% carbon monoxide (CO) coupled to sulfate reduction, while D. carboxydivorans can grow at 100% CO with and without sulfate. Hydrogen is produced during growth with CO by D. carboxydivorans. Here we present a summary of the features of D. nigrificans and D. carboxydivorans together with the description of the complete genome sequencing and annotation of both strains. Moreover, we compared the genomes of both strains to reveal their differences. This comparison led us to propose a reclassification of D. carboxydivorans as a later heterotypic synonym of D. nigrificans.
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TL;DR: The wealth of publications in this period is a testimony to the large environmental, biogeochemical and technological relevance of these organisms and how much the field has progressed in these years, although many important questions and applications remain to be explored.
Abstract: Dissimilatory sulphate reduction is the unifying and defining trait of sulphate-reducing prokaryotes (SRP). In their predominant habitats, sulphate-rich marine sediments, SRP have long been recognized to be major players in the carbon and sulphur cycles. Other, more recently appreciated, ecophysiological roles include activity in the deep biosphere, symbiotic relations, syntrophic associations, human microbiome/health and long-distance electron transfer. SRP include a high diversity of organisms, with large nutritional versatility and broad metabolic capacities, including anaerobic degradation of aromatic compounds and hydrocarbons. Elucidation of novel catabolic capacities as well as progress in the understanding of metabolic and regulatory networks, energy metabolism, evolutionary processes and adaptation to changing environmental conditions has greatly benefited from genomics, functional OMICS approaches and advances in genetic accessibility and biochemical studies. Important biotechnological roles of SRP range from (i) wastewater and off gas treatment, (ii) bioremediation of metals and hydrocarbons and (iii) bioelectrochemistry, to undesired impacts such as (iv) souring in oil reservoirs and other environments, and (v) corrosion of iron and concrete. Here we review recent advances in our understanding of SRPs focusing mainly on works published after 2000. The wealth of publications in this period, covering many diverse areas, is a testimony to the large environmental, biogeochemical and technological relevance of these organisms and how much the field has progressed in these years, although many important questions and applications remain to be explored.
224 citations
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TL;DR: The results of phylogenetic analysis demonstrated that the genus Desulfotomaculum already has lost the clustering monophyly and was segregated into some distinct groups with low sequence similarity.
Abstract: The genus
Desulfotomaculum
is a heterogeneous group of spore-forming sulfate-reducing bacteria. The type species of the genus is
Desulfotomaculum
nigrificans (Approved Lists 1980) emend. Visser et al. 2014. The results of phylogenetic analysis demonstrated that the genus
Desulfotomaculum
already has lost the clustering monophyly and was segregated into some distinct groups with low sequence similarity. Major features of the type strains in these groups were compared, and four novel genera, Desulfallas gen. nov., Desulfofundulus gen. nov., Desulfofarcimen gen. nov. and Desulfohalotomaculum gen. nov. were proposed to accommodate species transferred from the genus
Desulfotomaculum
.
41 citations
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TL;DR: The List of Changes in Taxonomic Opinion must be considered as a service to bacteriology and it has no ‘official character’, other than providing a centralized point for registering/indexing such changes in a way that makes them easily accessible to the scientific community.
Abstract: The Bacteriological Code deals with the nomenclature of prokaryotes. This may include existing names (the Approved Lists of Bacterial Names) as well as new names and new combinations. In this sense the Code is also dealing indirectly with taxonomic opinions. However, as with most codes of nomenclature there are no mechanisms for formally recording taxonomic opinions that do not involve the creation of new names or new combinations. In particular, it would be desirable for taxonomic opinions resulting from the creation of synonyms or emended descriptions to be made widely available to the public. In 2004, the Editorial Board of the International Journal of Systematic and Evolutionary Microbiology (IJSEM) agreed unanimously that it was desirable to cover such changes in taxonomic opinions (i.e. the creation of synonyms or the emendation of circumscriptions) previously published outside the IJSEM and to introduce a List of Changes in Taxonomic Opinion [Notification of changes in taxonomic opinion previously published outside the IJSEM; Euzeby et al. (2004). Int J Syst Evol Microbiol
54 , 1429–1430]. Scientists wishing to have changes in taxonomic opinion included in future lists should send one copy of the pertinent reprint or a photocopy or a PDF file thereof to the IJSEM Editorial Office or to the Lists Editor. It must be stressed that the date of proposed taxonomic changes is the date of the original publication not the date of publication of the list. Taxonomic opinions included in the List of Changes in Taxonomic Opinion cannot be considered as validly published nor, in any other way, approved by the International Committee on Systematics of Prokaryotes and its Judicial Commission. The names that are to be used are those that are the ‘correct names’ (in the sense of Principle 6) in the opinion of the bacteriologist, with a given circumscription, position and rank. A particular name, circumscription, position and rank does not have to be adopted in all circumstances. Consequently, the List of Changes in Taxonomic Opinion must be considered as a service to bacteriology and it has no ‘official character’, other than providing a centralized point for registering/indexing such changes in a way that makes them easily accessible to the scientific community.
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TL;DR: The first comprehensive genome analysis of a representative of the deep phylogenetic branch Clostridia Incertae Sedis, family V, provides insights into energy metabolism of C. thermautotrophica with an emphasis on its ecological implications.
Abstract: The genus Carboxydocella forms a deeply branching family in the class Clostridia and is currently represented by three physiologically diverse species of thermophilic prokaryotes. The type strain of the type species, Carboxydocella thermautotrophica 41T, is an obligate chemolithoautotroph growing exclusively by hydrogenogenic CO oxidation. Another strain, isolated from a hot spring at Uzon caldera, Kamchatka in the course of this work, is capable of coupling carboxydotrophy and dissimilatory reduction of Fe(III) from oxic and phyllosilicate minerals. The processes of carboxydotrophy and Fe(III) reduction appeared to be interdependent in this strain. The genomes of both isolates were sequenced, assembled into single chromosome sequences (for strain 41T a plasmid sequence was also assembled) and analyzed. Genome analysis revealed that each of the two strains possessed six genes encoding diverse Ni,Fe-containing CO dehydrogenases (maximum reported in complete prokaryotic genomes), indicating crucial role of carbon monoxide in C. thermautotrophica metabolism. Both strains possessed a set of 30 multiheme c-type cytochromes, but only the newly isolated Fe-reducing strain 019 had one extra gene of a 17-heme cytochrome, which is proposed to represent a novel determinant of dissimilatory iron reduction in prokaryotes. Mossbauer studies revealed that strain 019 induced reductive transformation of the abundant ferric/ferrous-mica mineral glauconite to siderite during carboxydotrophic growth. Reconstruction of the C. thermautotrophica strains energy metabolism is the first comprehensive genome analysis of a representative of the deep phylogenetic branch Clostridia Incertae Sedis, family V. Our data provide insights into energy metabolism of C. thermautotrophica with an emphasis on its ecological implications.
24 citations
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TL;DR: Analysis of the genome sequences revealed that three genes were missing from pantothenate and thiamine biosynthetic pathways, and five genes were absent from the pathway for biotin biosynthesis, raising questions whether alternative steps exist in biotin and thienine biosynthesis pathways in these acetogens.
Abstract: Clostridium autoethanogenum and Clostridium ljungdahlii are physiologically and genetically very similar strict anaerobic acetogens capable of growth on carbon monoxide as sole carbon source. While exact nutritional requirements have not been reported, we observed that for growth, the addition of vitamins to media already containing yeast extract was required, an indication that these are fastidious microorganisms. Elimination of complex components and individual vitamins from the medium revealed that the only organic compounds required for growth were pantothenate, biotin and thiamine. Analysis of the genome sequences revealed that three genes were missing from pantothenate and thiamine biosynthetic pathways, and five genes were absent from the pathway for biotin biosynthesis. Prototrophy in C. autoethanogenum and C. ljungdahlii for pantothenate was obtained by the introduction of plasmids carrying the heterologous gene clusters panBCD from Clostridium acetobutylicum, and for thiamine by the introduction of the thiC-purF operon from Clostridium ragsdalei. Integration of panBCD into the chromosome through allele-coupled exchange also conveyed prototrophy. C. autoethanogenum was converted to biotin prototrophy with gene sets bioBDF and bioHCA from Desulfotomaculum nigrificans strain CO-1-SRB, on plasmid and integrated in the chromosome. The genes could be used as auxotrophic selection markers in recombinant DNA technology. Additionally, transformation with a subset of the genes for pantothenate biosynthesis extended selection options with the pantothenate precursors pantolactone and/or beta-alanine. Similarly, growth was obtained with the biotin precursor pimelate combined with genes bioYDA from C. acetobutylicum. The work raises questions whether alternative steps exist in biotin and thiamine biosynthesis pathways in these acetogens.
24 citations
Cites methods from "Genome analyses of the carboxydotro..."
...Genomic DNA of Desulfotomaculum nigrificans CO-1SRB (Parshina et al. 2005; Visser et al. 2014) was obtained from DSMZ (DSM14880)....
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References
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TL;DR: This is the first completed genome sequence of a Desulfotomaculum species with validly published name and it is able to oxidize substrates completely to carbon dioxide with sulfate as the electron acceptor, which is reduced to hydrogen sulfide.
Abstract: Desulfotomaculum acetoxidans Widdel and Pfennig 1977 was one of the first sulfate-reducing bacteria known to grow with acetate as sole energy and carbon source. It is able to oxidize substrates completely to carbon dioxide with sulfate as the electron acceptor, which is reduced to hydrogen sulfide. All available data about this species are based on strain 5575T, isolated from piggery waste in Germany. Here we describe the features of this organism, together with the complete genome sequence and annotation. This is the first completed genome sequence of a Desulfotomaculum species with validly published name. The 4,545,624 bp long single replicon genome with its 4370 protein-coding and 100 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.
35 citations
"Genome analyses of the carboxydotro..." refers background in this paper
...A cluster of nitrogenase genes (Dtox_1023 to 1030) has been described in the genome of Desulfotomaculum acetoxidans [44]....
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TL;DR: This species is of interest because it represents one of the few sulfate-reducing bacteria that have been isolated from the rumen and was sequenced as part of the DOE Joint Genome Institute Community Sequencing Program 2009.
Abstract: Desulfotomaculum ruminis Campbell and Postgate 1965 is a member of the large genus Desulfotomaculum which contains 30 species and is contained in the family Peptococcaceae. This species is of interest because it represents one of the few sulfate-reducing bacteria that have been isolated from the rumen. Here we describe the features of D. ruminis together with the complete genome sequence and annotation. The 3,969,014 bp long chromosome with a total of 3,901 protein-coding and 85 RNA genes is the second completed genome sequence of a type strain of the genus Desulfotomaculum to be published, and was sequenced as part of the DOE Joint Genome Institute Community Sequencing Program 2009.
28 citations
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TL;DR: Results indicated that amino acids, supplied by the yeast extract or peptone in the fermentation medium, also contributed to the formation of acetate and carbon dioxide.
Abstract: Desulfotomaculum nigrificans degraded glucose to acetate, ethyl alcohol, and carbon dioxide. By use of 14C-glucose labeled at different carbon atoms, two pathways of glucose metabolism were detected. They were the Embden-Meyerhof and the Entner-Doudoroff schemes. Because the observed quantities of acetate and carbon dioxide, arising from glucose, were greater than the expected theoretical values, individual fermentations were conducted with 15 uniformly labeled 14C-amino acids. The results indicated that amino acids, supplied by the yeast extract or peptone in the fermentation medium, also contributed to the formation of acetate and carbon dioxide.
25 citations
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TL;DR: The features of A. missouriensis 431T are described, together with the complete genome sequence and annotation, and it is shown that members of Actinoplanes are prolific sources of novel antibiotics, enzymes, and other bioactive compounds.
Abstract: Actinoplanes missouriensis Couch 1963 is a well-characterized member of the genus Actinoplanes, which is of morphological interest because its members typically produce sporangia containing motile spores. The sporangiospores are motile by means of flagella and exhibit chemotactic properties. It is of further interest that members of Actinoplanes are prolific sources of novel antibiotics, enzymes, and other bioactive compounds. Here, we describe the features of A. missouriensis 431T, together with the complete genome sequence and annotation. The 8,773,466 bp genome contains 8,125 protein-coding and 79 RNA genes.
24 citations
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TL;DR: In this article, a strictly anaerobic, mesophilic, thiosulfate-reducing bacterium, that was sporeforming, rod-shaped and motile, was isolated from corroded aluminium alloy in an aircraft.
20 citations