Sulfur Oxidizer

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Manabu Fukui - One of the best experts on this subject based on the ideXlab platform.

  • Sulfurimicrobium lacus gen. nov., sp. nov., a Sulfur Oxidizer isolated from lake water, and review of the family Sulfuricellaceae to show that it is not a later synonym of Gallionellaceae
    Archives of Microbiology, 2020
    Co-Authors: Hisaya Kojima, Mamoru Kanda, Kazuhiro Umezawa, Manabu Fukui
    Abstract:

    A facultatively anaerobic Sulfur-oxidizing bacterium, strain skT11^T, was isolated from anoxic lake water of a stratified freshwater lake. As electron donor for chemolithoautotrophic growth, strain skT11^T oxidized thiosulfate, tetrathionate, and elemental Sulfur under nitrate-reducing conditions. Oxygen-dependent growth was observed under microoxic conditions, but not under fully oxygenated conditions. Growth was observed at a temperature range of 5–37 °C, with optimum growth at 28 °C. Strain skT11^T grew at a pH range of 5.1–7.5, with optimum growth at pH 6.5–6.9. Heterotrophic growth was not observed. Major components in the cellular fatty acid profile were C_16:1 and C_16:0. The complete genome of strain skT11^T consisted of a circular chromosome with a size of 3.8 Mbp and G + C content of 60.2 mol%. Phylogenetic analysis based on the 16S rRNA gene sequences indicated that the strain skT11^T is related to Sulfur-oxidizing bacteria of the genera Sulfuricella , Sulfurirhabdus, and Sulfuriferula , with sequence identities of 95.4% or lower. The analysis also indicated that these three genera should be excluded from the family Gallionellaceae , as members of another family. On the basis of its genomic and phenotypic properties, strain skT11^T (= DSM 110711^ T = NBRC 114323^ T) is proposed as the type strain of a new species in a new genus, Sulfurimicrobium lacus gen. nov., sp. nov. In addition, emended descriptions of the families Gallionellaceae and Sulfuricellaceae are proposed to declare that Sulfuricellaceae is not a later synonym of Gallionellaceae .

  • Sulfuriferula nivalis sp nov a Sulfur Oxidizer isolated from snow and emended description of Sulfuriferula plumbiphila
    International Journal of Systematic and Evolutionary Microbiology, 2020
    Co-Authors: Hisaya Kojima, Jun Mochizuki, Manabu Fukui
    Abstract:

    A chemolithoautotrophic Sulfur-oxidizing bacterium, strain SGTMT was isolated from snow collected in Japan. As electron donors for growth, SGTMT oxidized thiosulfate, tetrathionate and elemental Sulfur. Heterotrophic growth was not observed. Growth of the novel isolate was observed at a temperature range of 5–28 °C, with optimum growth at 18 °C. SGTMT grew at a pH range of 4.3–7.4, with optimum growth at pH 6.1–7.1. Major components in the cellular fatty acid profile were summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c) and C16 : 0. The complete genome of SGTMT consisted of a circular chromosome of approximately 3.4 Mbp and two plasmids. Phylogenetic analysis based on the 16S rRNA gene indicated that SGTMT represented a member of the genus Sulfuriferula , and its closest relative is Sulfuriferula thiophila mst6T with a sequence identity of 98 %. A comparative genome analysis showed dissimilarity between the genomes of SGTMT and S. thiophila mst6T, as low values of average nucleotide identity (74.9 %) and digital DNA–DNA hybridization (20.4%). On the basis of its genomic and phenotypic properties, SGTMT (=DSM 109609T=BCRC 81185T) is proposed as the type strain of a novel species, Sulfuriferula nivalis sp. nov. Some characteristics of another species in the same genus, Sulfuriferula plumbiphila , were also investigated to revise and supplement its description. The type strain of S. plumbiphila can grow on thiosulfate, tetrathionate and elemental Sulfur. The strain showed optimum growth at pH 6.3–7.0 and shared major cellular fatty acids with the other species of the genus Sulfuriferula .

  • Sulfurivermis fontis gen nov sp nov a Sulfur oxidizing autotroph and proposal of thioprofundaceae fam nov
    International Journal of Systematic and Evolutionary Microbiology, 2017
    Co-Authors: Hisaya Kojima, Miho Watanabe, Manabu Fukui
    Abstract:

    A novel Gram-stain-negative, chemolithoautotrophic Sulfur Oxidizer, strain JG42T, was isolated from a hot spring microbial mat. As an electron donor for autotrophic growth, strain JG42T utilized sulfide, thiosulfate, tetrathionate and elemental Sulfur. Cells of strain JG42T were oxidase-positive and catalase-negative. The G+C content of the genomic DNA was 65 mol%. The predominant cellular fatty acid was C16 : 0. Phylogenetic analysis of the 16S rRNA gene indicated that strain JG42T belonged to the order Chromatiales , but sequence similarities to the known species were less than 94 %. On the basis of its properties, strain JG42T (=DSM 104776T=NBRC 112696T) is proposed as the type strain of a novel species of a new genus, Sulfurivermis fontis gen. nov., sp. nov., which belongs to the family Thioalkalispiraceae. A new family, Thioprofundaceae fam. nov., is also proposed to accommodate the genus Thioprofundum , transferred from the family Thioalkalispiraceae .

  • Sulfuritortus calidifontis gen nov sp nov a Sulfur Oxidizer isolated from a hot spring microbial mat
    International Journal of Systematic and Evolutionary Microbiology, 2017
    Co-Authors: Hisaya Kojima, Miho Watanabe, Manabu Fukui
    Abstract:

    A novel Sulfur-oxidizing autotrophic bacterium, strain J1AT was isolated from a hot spring microbial mat. The cells were Gram-stain-negative, catalase-negative and oxidase-positive. As sole electron donor for chemolithoautotrophic growth, strain J1AT utilized sulfide, thiosulfate, elemental Sulfur, and tetrathionate. The G+C content of the genomic DNA was 66 mol%. Major cellular fatty acids (>40 % of total) were C16 : 0 and summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c). The predominant quinone was Q-8. Phylogenetic analysis of the 16S rRNA gene indicated that strain J1AT is a relative of species of the genus Thiobacillus , but shares only 93 % or lower sequence similarities with them. On the basis of its properties, strain J1AT represents a novel species of a new genus, for which the name Sulfuritortus calidifontis gen. nov., sp. nov. is proposed. The type strain of the type species is J1AT (=DSM 103923T=NBRC 112474T).

  • Sulfuricaulis limicola gen nov sp nov a Sulfur Oxidizer isolated from a lake
    International Journal of Systematic and Evolutionary Microbiology, 2016
    Co-Authors: Hisaya Kojima, Tomohiro Watanabe, Manabu Fukui
    Abstract:

    A novel Sulfur-oxidizing bacterium, strain HA5T, was isolated from sediment of a lake in Japan. The cells were rod-shaped (0.3-0.5 × 1.2-6.0 μm) and Gram-stain-negative. The G+C content of the genomic DNA was 63 mol%. The major components in the cellular fatty acid profile were C16 : 0 and summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c). The strain oxidized thiosulfate, tetrathionate and elemental Sulfur as electron donors to support autotrophic growth. Growth was observed at a temperature range of 8-37 °C, with optimum growth at 28-32 °C. The pH range for growth was pH 6.1-9.2. Optimum growth of the isolate was observed in medium without NaCl. Phylogenetic analysis based on 16S rRNA gene sequences indicated that the strain belongs to the family Acidiferrobacteraceae in the class Gammaproteobacteria. The closest relative was Sulfurifustis variabilis skN76T with the highest 16S rRNA gene sequence similarity of 93 %. On the basis of phylogenetic and phenotypic properties, strain HA5T is proposed to represent a novel species of a new genus, Sulfuricaulis limicola gen. nov., sp. nov. The type strain of the type species is HA5T ( = DSM 100373T = NBRC 110752T).

Hisaya Kojima - One of the best experts on this subject based on the ideXlab platform.

  • Sulfurimicrobium lacus gen. nov., sp. nov., a Sulfur Oxidizer isolated from lake water, and review of the family Sulfuricellaceae to show that it is not a later synonym of Gallionellaceae
    Archives of Microbiology, 2020
    Co-Authors: Hisaya Kojima, Mamoru Kanda, Kazuhiro Umezawa, Manabu Fukui
    Abstract:

    A facultatively anaerobic Sulfur-oxidizing bacterium, strain skT11^T, was isolated from anoxic lake water of a stratified freshwater lake. As electron donor for chemolithoautotrophic growth, strain skT11^T oxidized thiosulfate, tetrathionate, and elemental Sulfur under nitrate-reducing conditions. Oxygen-dependent growth was observed under microoxic conditions, but not under fully oxygenated conditions. Growth was observed at a temperature range of 5–37 °C, with optimum growth at 28 °C. Strain skT11^T grew at a pH range of 5.1–7.5, with optimum growth at pH 6.5–6.9. Heterotrophic growth was not observed. Major components in the cellular fatty acid profile were C_16:1 and C_16:0. The complete genome of strain skT11^T consisted of a circular chromosome with a size of 3.8 Mbp and G + C content of 60.2 mol%. Phylogenetic analysis based on the 16S rRNA gene sequences indicated that the strain skT11^T is related to Sulfur-oxidizing bacteria of the genera Sulfuricella , Sulfurirhabdus, and Sulfuriferula , with sequence identities of 95.4% or lower. The analysis also indicated that these three genera should be excluded from the family Gallionellaceae , as members of another family. On the basis of its genomic and phenotypic properties, strain skT11^T (= DSM 110711^ T = NBRC 114323^ T) is proposed as the type strain of a new species in a new genus, Sulfurimicrobium lacus gen. nov., sp. nov. In addition, emended descriptions of the families Gallionellaceae and Sulfuricellaceae are proposed to declare that Sulfuricellaceae is not a later synonym of Gallionellaceae .

  • Sulfuriferula nivalis sp nov a Sulfur Oxidizer isolated from snow and emended description of Sulfuriferula plumbiphila
    International Journal of Systematic and Evolutionary Microbiology, 2020
    Co-Authors: Hisaya Kojima, Jun Mochizuki, Manabu Fukui
    Abstract:

    A chemolithoautotrophic Sulfur-oxidizing bacterium, strain SGTMT was isolated from snow collected in Japan. As electron donors for growth, SGTMT oxidized thiosulfate, tetrathionate and elemental Sulfur. Heterotrophic growth was not observed. Growth of the novel isolate was observed at a temperature range of 5–28 °C, with optimum growth at 18 °C. SGTMT grew at a pH range of 4.3–7.4, with optimum growth at pH 6.1–7.1. Major components in the cellular fatty acid profile were summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c) and C16 : 0. The complete genome of SGTMT consisted of a circular chromosome of approximately 3.4 Mbp and two plasmids. Phylogenetic analysis based on the 16S rRNA gene indicated that SGTMT represented a member of the genus Sulfuriferula , and its closest relative is Sulfuriferula thiophila mst6T with a sequence identity of 98 %. A comparative genome analysis showed dissimilarity between the genomes of SGTMT and S. thiophila mst6T, as low values of average nucleotide identity (74.9 %) and digital DNA–DNA hybridization (20.4%). On the basis of its genomic and phenotypic properties, SGTMT (=DSM 109609T=BCRC 81185T) is proposed as the type strain of a novel species, Sulfuriferula nivalis sp. nov. Some characteristics of another species in the same genus, Sulfuriferula plumbiphila , were also investigated to revise and supplement its description. The type strain of S. plumbiphila can grow on thiosulfate, tetrathionate and elemental Sulfur. The strain showed optimum growth at pH 6.3–7.0 and shared major cellular fatty acids with the other species of the genus Sulfuriferula .

  • Sulfurivermis fontis gen nov sp nov a Sulfur oxidizing autotroph and proposal of thioprofundaceae fam nov
    International Journal of Systematic and Evolutionary Microbiology, 2017
    Co-Authors: Hisaya Kojima, Miho Watanabe, Manabu Fukui
    Abstract:

    A novel Gram-stain-negative, chemolithoautotrophic Sulfur Oxidizer, strain JG42T, was isolated from a hot spring microbial mat. As an electron donor for autotrophic growth, strain JG42T utilized sulfide, thiosulfate, tetrathionate and elemental Sulfur. Cells of strain JG42T were oxidase-positive and catalase-negative. The G+C content of the genomic DNA was 65 mol%. The predominant cellular fatty acid was C16 : 0. Phylogenetic analysis of the 16S rRNA gene indicated that strain JG42T belonged to the order Chromatiales , but sequence similarities to the known species were less than 94 %. On the basis of its properties, strain JG42T (=DSM 104776T=NBRC 112696T) is proposed as the type strain of a novel species of a new genus, Sulfurivermis fontis gen. nov., sp. nov., which belongs to the family Thioalkalispiraceae. A new family, Thioprofundaceae fam. nov., is also proposed to accommodate the genus Thioprofundum , transferred from the family Thioalkalispiraceae .

  • Sulfuritortus calidifontis gen nov sp nov a Sulfur Oxidizer isolated from a hot spring microbial mat
    International Journal of Systematic and Evolutionary Microbiology, 2017
    Co-Authors: Hisaya Kojima, Miho Watanabe, Manabu Fukui
    Abstract:

    A novel Sulfur-oxidizing autotrophic bacterium, strain J1AT was isolated from a hot spring microbial mat. The cells were Gram-stain-negative, catalase-negative and oxidase-positive. As sole electron donor for chemolithoautotrophic growth, strain J1AT utilized sulfide, thiosulfate, elemental Sulfur, and tetrathionate. The G+C content of the genomic DNA was 66 mol%. Major cellular fatty acids (>40 % of total) were C16 : 0 and summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c). The predominant quinone was Q-8. Phylogenetic analysis of the 16S rRNA gene indicated that strain J1AT is a relative of species of the genus Thiobacillus , but shares only 93 % or lower sequence similarities with them. On the basis of its properties, strain J1AT represents a novel species of a new genus, for which the name Sulfuritortus calidifontis gen. nov., sp. nov. is proposed. The type strain of the type species is J1AT (=DSM 103923T=NBRC 112474T).

  • Sulfuricaulis limicola gen nov sp nov a Sulfur Oxidizer isolated from a lake
    International Journal of Systematic and Evolutionary Microbiology, 2016
    Co-Authors: Hisaya Kojima, Tomohiro Watanabe, Manabu Fukui
    Abstract:

    A novel Sulfur-oxidizing bacterium, strain HA5T, was isolated from sediment of a lake in Japan. The cells were rod-shaped (0.3-0.5 × 1.2-6.0 μm) and Gram-stain-negative. The G+C content of the genomic DNA was 63 mol%. The major components in the cellular fatty acid profile were C16 : 0 and summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c). The strain oxidized thiosulfate, tetrathionate and elemental Sulfur as electron donors to support autotrophic growth. Growth was observed at a temperature range of 8-37 °C, with optimum growth at 28-32 °C. The pH range for growth was pH 6.1-9.2. Optimum growth of the isolate was observed in medium without NaCl. Phylogenetic analysis based on 16S rRNA gene sequences indicated that the strain belongs to the family Acidiferrobacteraceae in the class Gammaproteobacteria. The closest relative was Sulfurifustis variabilis skN76T with the highest 16S rRNA gene sequence similarity of 93 %. On the basis of phylogenetic and phenotypic properties, strain HA5T is proposed to represent a novel species of a new genus, Sulfuricaulis limicola gen. nov., sp. nov. The type strain of the type species is HA5T ( = DSM 100373T = NBRC 110752T).

Miho Watanabe - One of the best experts on this subject based on the ideXlab platform.

  • Sulfurivermis fontis gen nov sp nov a Sulfur oxidizing autotroph and proposal of thioprofundaceae fam nov
    International Journal of Systematic and Evolutionary Microbiology, 2017
    Co-Authors: Hisaya Kojima, Miho Watanabe, Manabu Fukui
    Abstract:

    A novel Gram-stain-negative, chemolithoautotrophic Sulfur Oxidizer, strain JG42T, was isolated from a hot spring microbial mat. As an electron donor for autotrophic growth, strain JG42T utilized sulfide, thiosulfate, tetrathionate and elemental Sulfur. Cells of strain JG42T were oxidase-positive and catalase-negative. The G+C content of the genomic DNA was 65 mol%. The predominant cellular fatty acid was C16 : 0. Phylogenetic analysis of the 16S rRNA gene indicated that strain JG42T belonged to the order Chromatiales , but sequence similarities to the known species were less than 94 %. On the basis of its properties, strain JG42T (=DSM 104776T=NBRC 112696T) is proposed as the type strain of a novel species of a new genus, Sulfurivermis fontis gen. nov., sp. nov., which belongs to the family Thioalkalispiraceae. A new family, Thioprofundaceae fam. nov., is also proposed to accommodate the genus Thioprofundum , transferred from the family Thioalkalispiraceae .

  • Sulfuritortus calidifontis gen nov sp nov a Sulfur Oxidizer isolated from a hot spring microbial mat
    International Journal of Systematic and Evolutionary Microbiology, 2017
    Co-Authors: Hisaya Kojima, Miho Watanabe, Manabu Fukui
    Abstract:

    A novel Sulfur-oxidizing autotrophic bacterium, strain J1AT was isolated from a hot spring microbial mat. The cells were Gram-stain-negative, catalase-negative and oxidase-positive. As sole electron donor for chemolithoautotrophic growth, strain J1AT utilized sulfide, thiosulfate, elemental Sulfur, and tetrathionate. The G+C content of the genomic DNA was 66 mol%. Major cellular fatty acids (>40 % of total) were C16 : 0 and summed feature 3 (C16 : 1ω7c and/or C16 : 1ω6c). The predominant quinone was Q-8. Phylogenetic analysis of the 16S rRNA gene indicated that strain J1AT is a relative of species of the genus Thiobacillus , but shares only 93 % or lower sequence similarities with them. On the basis of its properties, strain J1AT represents a novel species of a new genus, for which the name Sulfuritortus calidifontis gen. nov., sp. nov. is proposed. The type strain of the type species is J1AT (=DSM 103923T=NBRC 112474T).

Klaus Jurgens - One of the best experts on this subject based on the ideXlab platform.

  • sup05 dominates the gammaproteobacterial Sulfur Oxidizer assemblages in pelagic redoxclines of the central baltic and black seas
    Applied and Environmental Microbiology, 2013
    Co-Authors: Sabine Glaubitz, Katrin Kieslich, Christian Meeske, Matthias Labrenz, Klaus Jurgens
    Abstract:

    Gammaproteobacterial Sulfur Oxidizers (GSOs), particularly SUP05-related sequences, have been found worldwide in numerous oxygen-deficient marine environments. However, knowledge regarding their abundance, distribution, and ecological role is scarce. In this study, on the basis of phylogenetic analyses of 16S rRNA gene sequences originating from a Baltic Sea pelagic redoxcline, the in situ abundances of different GSO subgroups were quantified by CARD-FISH (catalyzed reporter fluorescence in situ hybridization) with oligonucleotide probes developed specifically for this purpose. Additionally, ribulose bisphosphate carboxylase/oxygenase form II (cbbM) gene transcript clone libraries were used to detect potential active chemolithoautotrophic GSOs in the Baltic Sea. Taken together, the results obtained by these two approaches demonstrated the existence of two major phylogenetic subclusters embedded within the GSO, one of them affiliated with sequences of the previously described SUP05 subgroup. CARD-FISH analyses revealed that only SUP05 occurred in relatively high numbers, reaching 10 to 30% of the total prokaryotes around the oxic-anoxic interface, where oxygen and sulfide concentrations are minimal. The applicability of the oligonucleotide probes was confirmed with samples from the Black Sea redoxcline, in which the SUP05 subgroup accounted for 10 to 13% of the total prokaryotic abundance. The cbbM transcripts presumably originating from SUP05 cells support previous evidence for the chemolithoautotrophic activity of this phylogenetic group. Our findings on the vertical distribution and high abundance of SUP05 suggest that this group plays an important role in marine redoxcline biogeochemistry, probably as anaerobic or aerobic Sulfur Oxidizers.

  • diversity of active chemolithoautotrophic prokaryotes in the sulfidic zone of a black sea pelagic redoxcline as determined by rrna based stable isotope probing
    FEMS Microbiology Ecology, 2010
    Co-Authors: Sabine Glaubitz, Matthias Labrenz, Gunter Jost, Klaus Jurgens
    Abstract:

    Marine pelagic redoxclines are characterized by pronounced activities of chemolithoautotrophic microorganisms. As evidenced by the high dark CO(2) fixation rates measured around the oxic-anoxic interface but also in the upper sulfidic zone, the accordant organisms participate in important biogeochemical transformations. Although Epsilonproteobacteria have been identified as an important chemoautotrophic group in these environments, detailed species-level information on the identity of actively involved prokaryotes is lacking. In the present study, active chemolithoautotrophic prokaryotic assemblages were identified in the sulfidic zone of a pelagic Black Sea redoxcline by applying rRNA-based stable isotope probing in combination with 16S rRNA gene single-strand conformation polymorphism analysis and 16S rRNA gene cloning. The results showed that a single epsilonproteobacterium, affiliated with the genus Sulfurimonas, and two different members of the gammaproteobacterial Sulfur Oxidizer (GSO) cluster were responsible for dark CO(2) fixation activities in the upper sulfidic layer of the Black Sea redoxcline. Phylogenetically, these organisms were closely related to microorganisms, distributed worldwide, that are thought to be key players in denitrification and sulfide oxidation. Together, these findings emphasize the importance of chemolithoautotrophic members of the Sulfurimonas and GSO groups in the carbon, nitrogen, and Sulfur cycles of oxic-anoxic pelagic transition zones.

Nicole Dubilier - One of the best experts on this subject based on the ideXlab platform.

  • genetic evidence for two carbon fixation pathways the calvin benson bassham cycle and the reverse tricarboxylic acid cycle in symbiotic and free living bacteria
    mSphere, 2019
    Co-Authors: Maxim Rubinblum, Nicole Dubilier, Manuel Kleiner
    Abstract:

    Very few bacteria are able to fix carbon via both the reverse tricarboxylic acid (rTCA) and the Calvin-Benson-Bassham (CBB) cycles, such as symbiotic, Sulfur-oxidizing bacteria that are the sole carbon source for the marine tubeworm Riftia pachyptila, the fastest-growing invertebrate. To date, the coexistence of these two carbon fixation pathways had not been found in a cultured bacterium and could thus not be studied in detail. Moreover, it was not clear if these two pathways were encoded in the same symbiont individual, or if two symbiont populations, each with one of the pathways, coexisted within tubeworms. With comparative genomics, we show that Thioflavicoccus mobilis, a cultured, free-living gammaproteobacterial Sulfur Oxidizer, possesses the genes for both carbon fixation pathways. Here, we also show that both the CBB and rTCA pathways are likely encoded in the genome of the Sulfur-oxidizing symbiont of the tubeworm Escarpia laminata from deep-sea asphalt volcanoes in the Gulf of Mexico. Finally, we provide genomic and transcriptomic data suggesting a potential electron flow toward the rTCA cycle carboxylase 2-oxoglutarate:ferredoxin oxidoreductase, via a rare variant of NADH dehydrogenase/heterodisulfide reductase in the E. laminata symbiont. This electron-bifurcating complex, together with NAD(P)+ transhydrogenase and Na+ translocating Rnf membrane complexes, may improve the efficiency of the rTCA cycle in both the symbiotic and the free-living Sulfur Oxidizer.IMPORTANCE Primary production on Earth is dependent on autotrophic carbon fixation, which leads to the incorporation of carbon dioxide into biomass. Multiple metabolic pathways have been described for autotrophic carbon fixation, but most autotrophic organisms were assumed to have the genes for only one of these pathways. Our finding of a cultivable bacterium with two carbon fixation pathways in its genome, the rTCA and the CBB cycle, opens the possibility to study the potential benefits of having these two pathways and the interplay between them. Additionally, this will allow the investigation of the unusual and potentially very efficient mechanism of electron flow that could drive the rTCA cycle in these autotrophs. Such studies will deepen our understanding of carbon fixation pathways and could provide new avenues for optimizing carbon fixation in biotechnological applications.

  • Genetic Evidence for Two Carbon Fixation Pathways (the Calvin-Benson-Bassham Cycle and the Reverse Tricarboxylic Acid Cycle) in Symbiotic and Free-Living Bacteria
    American Society for Microbiology, 2019
    Co-Authors: Maxim Rubin-blum, Nicole Dubilier, Manuel Kleiner
    Abstract:

    Primary production on Earth is dependent on autotrophic carbon fixation, which leads to the incorporation of carbon dioxide into biomass. Multiple metabolic pathways have been described for autotrophic carbon fixation, but most autotrophic organisms were assumed to have the genes for only one of these pathways. Our finding of a cultivable bacterium with two carbon fixation pathways in its genome, the rTCA and the CBB cycle, opens the possibility to study the potential benefits of having these two pathways and the interplay between them. Additionally, this will allow the investigation of the unusual and potentially very efficient mechanism of electron flow that could drive the rTCA cycle in these autotrophs. Such studies will deepen our understanding of carbon fixation pathways and could provide new avenues for optimizing carbon fixation in biotechnological applications.Very few bacteria are able to fix carbon via both the reverse tricarboxylic acid (rTCA) and the Calvin-Benson-Bassham (CBB) cycles, such as symbiotic, Sulfur-oxidizing bacteria that are the sole carbon source for the marine tubeworm Riftia pachyptila, the fastest-growing invertebrate. To date, the coexistence of these two carbon fixation pathways had not been found in a cultured bacterium and could thus not be studied in detail. Moreover, it was not clear if these two pathways were encoded in the same symbiont individual, or if two symbiont populations, each with one of the pathways, coexisted within tubeworms. With comparative genomics, we show that Thioflavicoccus mobilis, a cultured, free-living gammaproteobacterial Sulfur Oxidizer, possesses the genes for both carbon fixation pathways. Here, we also show that both the CBB and rTCA pathways are likely encoded in the genome of the Sulfur-oxidizing symbiont of the tubeworm Escarpia laminata from deep-sea asphalt volcanoes in the Gulf of Mexico. Finally, we provide genomic and transcriptomic data suggesting a potential electron flow toward the rTCA cycle carboxylase 2-oxoglutarate:ferredoxin oxidoreductase, via a rare variant of NADH dehydrogenase/heterodisulfide reductase in the E. laminata symbiont. This electron-bifurcating complex, together with NAD(P)+ transhydrogenase and Na+ translocating Rnf membrane complexes, may improve the efficiency of the rTCA cycle in both the symbiotic and the free-living Sulfur Oxidizer

  • genetic evidence for two carbon fixation pathways in symbiotic and free living bacteria the calvin bassham cycle and the reverse tricarboxylic acid cycle
    bioRxiv, 2018
    Co-Authors: Maxim Rubinblum, Nicole Dubilier, Manuel Kleiner
    Abstract:

    Sulfide-oxidizing bacterial endosymbionts of marine tubeworms such as Riftia pachyptila are able to fix carbon via both the reverse tricarboxylic acid (rTCA) and the Calvin-Benson-Bassham (CBB) cycles. Until recently, this co-existence of two carbon fixation pathways was thought to be unique to tubeworm symbionts. However, it was not clear if these two pathways were encoded in the same symbiont individual, or if two symbiont populations, each with one of the pathways, co-existed within tubeworms. We show here that both the CBB and rTCA pathways are likely encoded in the genome of the Sulfur-oxidizing symbiont of the tubeworm Escarpia laminata from deep-sea asphalt volcanoes in the Gulf of Mexico. Furthermore, with comparative genomics, we show that Thioflavicoccus mobilis, a cultured, free-living gammaproteobacterial Sulfur Oxidizer, also possesses the genes for both carbon fixation pathways. Finally, we provide genomic and transcriptomic data suggesting a potential electron flow towards the rTCA cycle carboxylase 2-oxoglutarate:ferredoxin oxidoreductase, via a rare variant of NADH dehydrogenase/heterodisulfide reductase. This electron bifurcating complex, together with NAD(P)+ transhydrogenase and Na+ translocating Rnf membrane complexes may drive the rTCA cycle in both the symbiotic and the free-living Sulfur Oxidizer.

  • acquisition of a novel Sulfur oxidizing symbiont in the gutless marine worm inanidrilus exumae
    Applied and Environmental Microbiology, 2018
    Co-Authors: Claudia Bergin, Cecilia Wentrup, Christer Erseus, Nancy Brewig, Anna Blazejak, Olav Giere, Markus Schmid, P De Wit, Nicole Dubilier
    Abstract:

    ABSTRACT Gutless phallodrilines are marine annelid worms without a mouth or gut, which live in an obligate association with multiple bacterial endosymbionts that supply them with nutrition. In this study, we discovered an unusual symbiont community in the gutless phallodriline Inanidrilus exumae that differs markedly from the microbiomes of all 22 of the other host species examined. Comparative 16S rRNA gene sequence analysis and fluorescence in situ hybridization revealed that I. exumae harbors cooccurring gamma-, alpha-, and deltaproteobacterial symbionts, while all other known host species harbor gamma- and either alpha- or deltaproteobacterial symbionts. Surprisingly, the primary chemoautotrophic Sulfur Oxidizer “Candidatus Thiosymbion” that occurs in all other gutless phallodriline hosts does not appear to be present in I. exumae. Instead, I. exumae harbors a bacterial endosymbiont that resembles “ Ca . Thiosymbion” morphologically and metabolically but originates from a novel lineage within the class Gammaproteobacteria. This endosymbiont, named Gamma 4 symbiont here, had a 16S rRNA gene sequence that differed by at least 7% from those of other free-living and symbiotic bacteria and by 10% from that of “ Ca . Thiosymbion.” Sulfur globules in the Gamma 4 symbiont cells, as well as the presence of genes characteristic for autotrophy ( cbbL ) and Sulfur oxidation ( aprA ), indicate that this symbiont is a chemoautotrophic Sulfur Oxidizer. Our results suggest that a novel lineage of free-living bacteria was able to establish a stable and specific association with I. exumae and appears to have displaced the “ Ca . Thiosymbion” symbionts originally associated with these hosts. IMPORTANCE All 22 gutless marine phallodriline species examined to date live in a highly specific association with endosymbiotic, chemoautotrophic Sulfur Oxidizers called “ Ca . Thiosymbion.” These symbionts evolved from a single common ancestor and represent the ancestral trait for this host group. They are transmitted vertically and assumed to be in transition to becoming obligate endosymbionts. It is therefore surprising that despite this ancient, evolutionary relationship between phallodriline hosts and “ Ca . Thiosymbion,” these symbionts are apparently no longer present in Inanidrilus exumae. They appear to have been displaced by a novel lineage of Sulfur-oxidizing bacteria only very distantly related to “ Ca . Thiosymbion.” Thus, this study highlights the remarkable plasticity of both animals and bacteria in establishing beneficial associations: the phallodriline hosts were able to acquire and maintain symbionts from two very different lineages of bacteria, while Sulfur-oxidizing bacteria from two very distantly related lineages were able to independently establish symbiotic relationships with phallodriline hosts.