Thermovibrio ammonificans sp. nov., a thermophilic, chemolithotrophic, nitrate-ammonifying bacterium from deep-sea hydrothermal vents

Vetriani, Costantino; Speck, Mark; Ellor, Susan V.; Lutz, Richard A.; Starovoytov, Valentin

doi:10.1099/ijs.0.02781-0

Cited by 100 publications

(110 citation statements)

References 27 publications

(29 reference statements)

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“…This is consistent with data showing that ammonification is more prevalent than denitrification in nitrate-reducing thermophiles (Blochl et al, 1997;Vetriani et al, 2004;Perez-Rodriguez et al, 2012), and may be related to a possible decrease in nitrate concentrations as the hydrothermal fluid temperature increases. In line with this hypothesis, an increase in the significance of nitrate ammonification relative to denitrification as the concentration of nitrate decreased was observed in estuarine sediments (Dong et al, 2009).…”

Section: Discussionsupporting

confidence: 81%

“…During growth, these microorganisms reduce nitrate to dinitrogen (Takai et al, 2004;Nakagawa et al, 2005;Takai et al, 2006) or ammonium (Blochl et al, 1997;Vetriani et al, 2004;Voordeckers et al, 2008;Perez-Rodriguez et al, 2010, 2012. In most cases, nitrate reduction is coupled to the oxidation of molecular hydrogen (and less frequently of formate or thiosulfate), and these organisms have a shorter doubling time when nitrate, rather than sulfur, is supplemented as the terminal electron acceptor (Vetriani et al, 2004;Voordeckers et al, 2005;Perez-Rodriguez et al, 2010, 2012. In particular, most of the Epsilonproteobacteria isolated from deep-sea hydrothermal vents conserve energy by reducing nitrate (reviewed in Campbell et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Deep-sea hydrothermal ventEpsilonproteobacteriaencode a conserved and widespread nitrate reduction pathway (Nap)

et al. 2014

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Despite the frequent isolation of nitrate-respiring Epsilonproteobacteria from deep-sea hydrothermal vents, the genes coding for the nitrate reduction pathway in these organisms have not been investigated in depth. In this study we have shown that the gene cluster coding for the periplasmic nitrate reductase complex (nap) is highly conserved in chemolithoautotrophic, nitrate-reducing Epsilonproteobacteria from deep-sea hydrothermal vents. Furthermore, we have shown that the napA gene is expressed in pure cultures of vent Epsilonproteobacteria and it is highly conserved in microbial communities collected from deep-sea vents characterized by different temperature and redox regimes. The diversity of nitrate-reducing Epsilonproteobacteria was found to be higher in moderate temperature, diffuse flow vents than in high temperature black smokers or in low temperatures, substrate-associated communities. As NapA has a high affinity for nitrate compared with the membrane-bound enzyme, its occurrence in vent Epsilonproteobacteria may represent an adaptation of these organisms to the low nitrate concentrations typically found in vent fluids. Taken together, our findings indicate that nitrate reduction is widespread in vent Epsilonproteobacteria and provide insight on alternative energy metabolism in vent microorganisms. The occurrence of the nap cluster in vent, commensal and pathogenic Epsilonproteobacteria suggests that the ability of these bacteria to respire nitrate is important in habitats as different as the deep-sea vents and the human body.

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Section: Discussionsupporting

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Deep-sea hydrothermal ventEpsilonproteobacteriaencode a conserved and widespread nitrate reduction pathway (Nap)

et al. 2014

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“…Transmission electron micrographs were obtained as previously described (Vetriani et al, 2004). Cells of strain 1812E T were Gramstain-negative rods, approximately 1.05±0.11 µm in length and 0.40±0.05 µm in width (n=100), with a polar flagellum (Fig.…”

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confidence: 99%

Sulfurovum riftiae sp. nov., a mesophilic, thiosulfate-oxidizing, nitrate-reducing chemolithoautotrophic epsilonproteobacterium isolated from the tube of the deep-sea hydrothermal vent polychaete Riftia pachyptila

Giovannelli

Chung

Staley

et al. 2016

International Journal of Systematic and Evolutionary Microbiology

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An anaerobic, nitrate-reducing, sulfur-and thiosulfate-oxidizing bacterium, designated strain 1812E T , was isolated from the vent polychaete Riftia pachyptila, which was collected from a deep-sea hydrothermal vent on the East Pacific Rise. Cells were Gram-stain-negative rods, measuring approximately 1.05±0.11 µm by 0.40±0.05 µm. Strain 1812E T grew at 25 --45 C (optimum 35 C), with 1.5-4.0 % (w/v) NaCl (optimum 3.0 %) and at pH 5.0-8.0 (optimum pH 6.0). The generation time under optimal conditions was 3 h. Strain 1812E T was an anaerobic chemolithotroph that grew with either sulfur or thiosulfate as the energy source and carbon dioxide as the sole carbon source. Nitrate was used as a sole terminal electron acceptor. The predominant fatty acids were C 16 : 1 !7c, C 18 : 1 !7c and C 16 : 0 . The major polar lipids were phosphatidylethanolamine, diphosphatidylglycerol and phosphatidylglycerol. The major respiratory quinone was menaquinone MK-6 and the G+C content of the genomic DNA was 47.4 mol%. Phylogenetic analysis of the 16S rRNA gene of strain 1812E T showed that the isolate belonged to the Epsilonproteobacteria, and its closest relatives were Sulfurovum lithotrophicum 42BKT T and Sulfurovum aggregans Monchim 33 T (98.3 and 95.7 % sequence similarity, respectively). DNA-DNA relatedness between strain 1812E T and the type strain of S. lithotrophicum was 29.7 %, demonstrating that the two strains are not members of the same species. Based on the phylogenetic, molecular, chemotaxonomic and physiological evidence, strain 1812E T represents a novel species within the genus Sulfurovum, for which the name Sulfurovum riftiae sp. nov. is proposed. The type strain is 1812E T (=DSM 101780 T =JCM 30810 T ).

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“…Growth was also tested in artificial seawater (ASW) medium (l 21 : NaCl, 24 g; KCl, 0.7 g; MgCl 2 , 7.0 g; yeast extract, 3.0 g; peptone, 2.5 g), in low-strength ASW (LS ASW) medium (modified ASW containing 0.1 g yeast extract and 0.5 g peptone l 21 ) and in ASW minimal medium (ASW MM) (l 21 : NaCl, 23.6 g; KCl,0.64 Growth rates (m; h 21 ) were estimated as described previously (Vetriani et al, 2004). Unless specified otherwise, growth ranges and optimal growth conditions were determined in LS ASW medium.…”

mentioning

confidence: 99%

“…Catalase activity was determined as described previously (Vetriani et al, 2004) and the presence of cytochrome c, a component of the cytochrome oxidase system, was determined according to the protocol described by Kovacs (1956). Escherichia coli K-12 and Pseudomonas aeruginosa were used as negative and positive controls for the cytochrome oxidase test, respectively.…”

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confidence: 99%

Salinisphaera hydrothermalis sp. nov., a mesophilic, halotolerant, facultatively autotrophic, thiosulfate-oxidizing gammaproteobacterium from deep-sea hydrothermal vents, and emended description of the genus Salinisphaera

Crespo‐Medina

Chatziefthimiou

Cruz-Matos

et al. 2009

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

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A mesophilic, aerobic, facultatively chemolithoautotrophic bacterium, designated strain EPR70 T , was isolated from hydrothermal fluids from diffuse-flow vents on the East Pacific Rise at 96 509 N 1046 179 W. Cells were Gram-negative rods, approximately 0.8-1.0 mm long and 0.3-0.5 mm wide. Strain EPR70 T grew at 20-40 6C (optimum 30-35 6C), 1-25 % NaCl (optimum 2.5 %) and pH 5.0-7.5 (optimum pH 5.5). The shortest generation time observed for strain EPR70 T was 42 min. Growth occurred under aerobic chemolithoautotrophic conditions in the presence of thiosulfate and CO 2 . Strain EPR70 T grew heterotrophically with acetate or n-alkanes as sole carbon and energy sources, and in complex artificial seawater medium. Nitrate was not used as an electron acceptor. The G+C content of the genomic DNA was 64 mol%. Phylogenetic analysis of the 16S rRNA gene indicated that this organism is a member of the class Gammaproteobacteria, with Salinisphaera shabanensis E1L3A T as its closest relative (94 % sequence similarity). On the basis of phylogenetic analyses based on 16S rRNA, rbcL and alkB genes and physiological analysis, it is proposed that the organism represents a novel species within the genus Salinisphaera, for which the name Salinisphaera hydrothermalis sp. nov. is proposed. The type strain is EPR70 T (5DSM 21483 T 5JCM 15514 T ).Deep-sea hydrothermal vents are located in tectonically active areas of the sea floor and release either hightemperature fluids (focused-flow vents) or moderatetemperature fluids (diffuse-flow vents). At deep-sea vents, seawater interacts with volcanic rocks at high temperature and becomes enriched in a variety of reduced chemical species, which represent a constant flux of electron donors for microbial oxidations. In the absence of light, chemosynthetic micro-organisms oxidize these reduced chemical species (predominantly sulfur compounds) and mediate the primary production of organic carbon (Jannasch, 1995;McCollom & Shock, 1997).Typically, representatives of the genera Thiomicrospira and Thiobacillus have been isolated when diffuse-flow hydrothermal fluids were inoculated in culture media for the enrichment of chemosynthetic, aerobic, sulfide-, sulfur-and thiosulfate-oxidizing bacteria (Ruby et al., 1981;Ruby & Jannasch, 1982;Jannasch et al., 1985;Durand et al., 1993;Teske et al., 2000; Takai et al., 2004). Heterotrophic bacteria of the genera Marinobacter, Vibrio, Pseudoalteromonas and Halomonas, among others, have also been isolated routinely The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains EPR70 T , EPR72 and EPR71 are EU740416-EU740418. The accession numbers for the partial rbcL gene sequences from strains EPR70 T , EPR71 and EPR72 and S. shabanensis DSM 14853 T are EU740422-EU740425 and those for the partial alkB gene sequences of strain EPR70 T , S. shabanensis DSM 14853 T and strain EPR71 are EU740419-EU740421.Graphs showing the effects of temperature, pH and NaCl concentration on growth of strain EPR70 T and neighbour-joining trees based on amino a...

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Thermovibrio ammonificans sp. nov., a thermophilic, chemolithotrophic, nitrate-ammonifying bacterium from deep-sea hydrothermal vents

Cited by 100 publications

References 27 publications

Deep-sea hydrothermal ventEpsilonproteobacteriaencode a conserved and widespread nitrate reduction pathway (Nap)

Deep-sea hydrothermal ventEpsilonproteobacteriaencode a conserved and widespread nitrate reduction pathway (Nap)

Sulfurovum riftiae sp. nov., a mesophilic, thiosulfate-oxidizing, nitrate-reducing chemolithoautotrophic epsilonproteobacterium isolated from the tube of the deep-sea hydrothermal vent polychaete Riftia pachyptila

Salinisphaera hydrothermalis sp. nov., a mesophilic, halotolerant, facultatively autotrophic, thiosulfate-oxidizing gammaproteobacterium from deep-sea hydrothermal vents, and emended description of the genus Salinisphaera

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