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
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
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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38 citations
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
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: In the photosynthetic bacterium Rhodospirillum rubrum, the presence of carbon monoxide (CO) induces expression of several proteins, such as CODH and CO-tolerant hydrogenase as mentioned in this paper.
Abstract: In the photosynthetic bacterium Rhodospirillum rubrum, the presence of carbon monoxide (CO) induces expression of several proteins. These include carbon monoxide dehydrogenase (CODH) and a CO-tolerant hydrogenase. Together these enzymes catalyze the following conversion: CO + H2O --> CO2 + H2. This system enables R. rubrum to grow in the dark on CO as the sole energy source. Expression of this system has been shown previously to be regulated at the transcriptional level by CO. We have now identified the remainder of the CO-regulated genes encoded in a contiguous region of the R. rubrum genome. These genes, cooMKLXU, apparently encode proteins related to the function of the CO-induced hydrogenase. As seen before with the gene for the large subunit of the CO-induced hydrogenase (cooH), most of the proteins predicted by these additional genes show significant sequence similarity to subunits of Escherichia coli hydrogenase 3. In addition, all of the newly identified coo gene products show similarity to subunits of NADH-quinone oxidoreductase (energy-conserving NADH dehydrogenase I) from various eukaryotic and prokaryotic organisms. We have found that dicyclohexylcarbodiimide, an inhibitor of mitochondrial NADH dehydrogenase I (also called complex I), inhibits the CO-induced hydrogenase as well. We also show that expression of the cooMKLXUH operon is regulated by CO and the transcriptional activator CooA in a manner similar to that of the cooFSCTJ operon that encodes the subunits of CODH and related proteins.
184 citations
TL;DR: In this article, the Ech hydrogenase was purified to apparent homogeneity in a high yield, and the enzyme catalyzed the H2 dependent reduction of a M.barkeri 2[4Fe-4S] ferredoxin with a specific activity of 50 U·mg protein−1 at pH 7.0.
Abstract: Methanosarcina barkeri has recently been shown to produce a multisubunit membrane-bound [NiFe] hydrogenase designated Ech (Escherichia coli hydrogenase 3) hydrogenase. In the present study Ech hydrogenase was purified to apparent homogeneity in a high yield. The enzyme preparation obtained only contained the six polypeptides which had previously been shown to be encoded by the ech operon. The purified enzyme was found to contain 0.9 mol of Ni, 11.3 mol of nonheme-iron and 10.8 mol of acid-labile sulfur per mol of enzyme. Using the purified enzyme the kinetic parameters were determined. The enzyme catalyzed the H2 dependent reduction of a M. barkeri 2[4Fe-4S] ferredoxin with a specific activity of 50 U·mg protein−1 at pH 7.0 and exhibited an apparent Km for the ferredoxin of 1 µm. The enzyme also catalyzed hydrogen formation with the reduced ferredoxin as electron donor at a rate of 90 U·mg protein−1 at pH 7.0. The apparent Km for the reduced ferredoxin was 7.5 µm. Reduction or oxidation of the ferredoxin proceeded at similar rates as the reduction or oxidation of oxidized or reduced methylviologen, respectively. The apparent Km for H2 was 5 µm. The kinetic data strongly indicate that the ferredoxin is the physiological electron donor or acceptor of Ech hydrogenase. Ech hydrogenase amounts to about 3% of the total cell protein in acetate-grown, methanol-grown or H2/CO2-grown cells of M. barkeri, as calculated from quantitative Western blot experiments. The function of Ech hydrogenase is ascribed to ferredoxin-linked H2 production coupled to the oxidation of the carbonyl-group of acetyl-CoA to CO2 during growth on acetate, and to ferredoxin-linked H2 uptake coupled to the reduction of CO2 to the redox state of CO during growth on H2/CO2 or methanol.
155 citations
"Genome analyses of the carboxydotro..." refers background in this paper
...The genes in this cluster are similar to genes described to be involved in the H2 production from CO oxidation [38-41]....
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TL;DR: Evidence derived from the crystal structure of fumarate reductase suggests an electrogenic mechanism for the latter process, which appears to be an electroneutral process.
147 citations
"Genome analyses of the carboxydotro..." refers background in this paper
...This interaction could occur as described in Wolinella succinogenes, where fumarate can be used as an electron acceptor for growth on formate [47]....
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TL;DR: Since first discovered by J~eijerincl~ in 1895, the bacter ia have been found in di tch and canal mud and soil, and also found in ocean mud and sea sand, and other saline basins, sand and c lay of dunes and polders, springs, sewage, brines of oil wells and water a t the bo t tom of gasoline storage tanks.
Abstract: Since first discovered by J~eijerincl~ in 1895 (5) in di tch and canal mud and soil, the bacter ia have been repea ted ly recovered from the~e hab i ta t s and also found in ocean mud and sea sand, bo t tom deposits of the Black Sea, and other saline basins, sand and c lay of dunes and polders, springs, sewage, brines of oil wells and water a t the bo t tom of gasoline storage tanks . The b lack color of muds and c lay caused b y the precipi ta t ion of iron sulfide a t tes t s to their act ivi ty. The oxidat ion of this iron sulfide plays an impor tan t pa r t in the reclamat ion of the soils of the Dutch polder land (16). Von Wol. zogen Ki~hr ascribes to these bacter ia the corrosion of iron conduits under anaerobic conditions in ground containing considerable amounts of sulfate (37, 38). I t is believed t ha t t hey were concerned with an explosion of a gasoline storage t ank (39, 9), the corrosion of concrete (2) and the periodic destruct ion of large numbers of fish in waters of the South African coas~ (11). I t is even possible t ha t some deposits of mineral sulfides have been formed through the ac t iv i ty of the sulfate-reducing bacter ia (4). The distr ibut ion, importance and general characterist ics of the bacter ia have been so adequate ly discussed b y Bears (1) and others (8, 40, 3) during recent years tha t a detai led review is tmnecessary.
135 citations
"Genome analyses of the carboxydotro..." refers background in this paper
...Later, Starkey (1938) renamed it to “Sporovibrio desulfuricans” [3] before it was finally renamed as D. nigrificans [1]....
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TL;DR: On the basis of phylogenetic and physiological features, it is suggested that strain CO-1-SRB(T) represents a novel species within the genus Desulfotomaculum, for which the name Desulfotomyaculum carboxydivorans is proposed.
Abstract: A moderately thermophilic, anaerobic, chemolithoheterotrophic, sulfate-reducing bacterium, strain CO-1-SRB(T), was isolated from sludge from an anaerobic bioreactor treating paper mill wastewater. Cells were Gram-positive, motile, spore-forming rods. The temperature range for growth was 30-68 degrees C, with an optimum at 55 degrees C. The NaCl concentration range for growth was 0-17 g l(-1); there was no change in growth rate until the NaCl concentration reached 8 g l(-1). The pH range for growth was 6.0-8.0, with an optimum of 6.8-7.2. The bacterium could grow with 100% CO in the gas phase. With sulfate, CO was converted to H(2) and CO(2) and part of the H(2) was used for sulfate reduction; without sulfate, CO was completely converted to H(2) and CO(2). With sulfate, strain CO-1-SRB(T) utilized H(2)/CO(2), pyruvate, glucose, fructose, maltose, lactate, serine, alanine, ethanol and glycerol. The strain fermented pyruvate, lactate, glucose and fructose. Yeast extract was necessary for growth. Sulfate, thiosulfate and sulfite were used as electron acceptors, whereas elemental sulfur and nitrate were not. A phylogenetic analysis of 16S rRNA gene sequences placed strain CO-1-SRB(T) in the genus Desulfotomaculum, closely resembling Desulfotomaculum nigrificans DSM 574(T) and Desulfotomaculum sp. RHT-3 (99 and 100% similarity, respectively). However, the latter strains were completely inhibited above 20 and 50% CO in the gas phase, respectively, and were unable to ferment CO, lactate or glucose in the absence of sulfate. DNA-DNA hybridization of strain CO-1-SRB(T) with D. nigrificans and Desulfotomaculum sp. RHT-3 showed 53 and 60% relatedness, respectively. On the basis of phylogenetic and physiological features, it is suggested that strain CO-1-SRB(T) represents a novel species within the genus Desulfotomaculum, for which the name Desulfotomaculum carboxydivorans is proposed. This is the first description of a sulfate-reducing micro-organism that is capable of growth under an atmosphere of pure CO with and without sulfate. The type strain is CO-1-SRB(T) (=DSM 14880(T)=VKM B-2319(T)).
112 citations
"Genome analyses of the carboxydotro..." refers background in this paper
...carboxydivorans is able to grow in the absence of an electron acceptor with CO (100%), pyruvate, lactate, glucose and fructose [6]....
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...Sporulation oval, terminal or subterminal TAS [6]...
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...Carbon source 100% CO, with and without sulfate TAS [6]...
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...Energy source hydrogenogenic and heterotrophic g rowth TAS [6]...
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...carboxydivorans was isolated from sludge in an anaerobic bioreactor treating paper mill wastewater [6] and was described to be the first sulfate-reducing bacterium able to grow at 100% CO....
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