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Journal ArticleDOI

Isolation and characterization of a new CO-utilizing strain, Thermoanaerobacter thermohydrosulfuricus subsp. carboxydovorans, isolated from a geothermal spring in Turkey

TL;DR: Strain TLO has the capability to ferment a wide variety of mono-, di-, and polysaccharides and proteinaceous substrates, producing mainly lactate, next to acetate, ethanol, alanine, H2, and CO2 and was able to grow in an atmosphere of up to 25% of CO as sole electron donor.
Abstract: A novel anaerobic, thermophilic, Gram-positive, spore-forming, and sugar-fermenting bacterium (strain TLO) was isolated from a geothermal spring in Ayas, Turkey. The cells were straight to curved rods, 0.4–0.6 μm in diameter and 3.5–10 μm in length. Spores were terminal and round. The temperature range for growth was 40–80°C, with an optimum at 70°C. The pH optimum was between 6.3 and 6.8. Strain TLO has the capability to ferment a wide variety of mono-, di-, and polysaccharides and proteinaceous substrates, producing mainly lactate, next to acetate, ethanol, alanine, H2, and CO2. Remarkably, the bacterium was able to grow in an atmosphere of up to 25% of CO as sole electron donor. CO oxidation was coupled to H2 and CO2 formation. The G + C content of the genomic DNA was 35.1 mol%. Based on 16S rRNA gene sequence analysis and the DNA–DNA hybridization data, this bacterium is most closely related to Thermoanaerobacter thermohydrosulfuricus and Thermoanaerobacter siderophilus (99% similarity for both). However, strain TLO differs from Thermoanaerobacter thermohydrosulfuricus in important aspects, such as CO-utilization and lipid composition. These differences led us to propose that strain TLO represents a subspecies of Thermoanaerobacter thermohydrosulfuricus, and we therefore name it Thermoanaerobacter thermohydrosulfuricus subsp. carboxydovorans.

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Journal ArticleDOI
TL;DR: Upon both acid and base hydrolyses of total cell material, the uncommon membrane-spanning lipid 13,16-dimethyl octacosanedioic acid (iso-diabolic acid) was released in substantial amounts (22 to 43% of the total fatty acids) from all of the acidobacteria studied.
Abstract: The distribution of membrane lipids of 17 different strains representing 13 species of subdivisions 1 and 3 of the phylum Acidobacteria, a highly diverse phylum of the Bacteria, were examined by hydrolysis and gas chromatography-mass spectrometry (MS) and by high-performance liquid chromatography-MS of intact polar lipids. Upon both acid and base hydrolyses of total cell material, the uncommon membrane-spanning lipid 13,16-dimethyl octacosanedioic acid (iso-diabolic acid) was released in substantial amounts (22 to 43% of the total fatty acids) from all of the acidobacteria studied. This lipid has previously been encountered only in thermophilic Thermoanaerobacter species but bears a structural resemblance to the alkyl chains of bacterial glycerol dialkyl glycerol tetraethers (GDGTs) that occur ubiquitously in peat and soil and are suspected to be produced by acidobacteria. As reported previously, most species also contained iso-C15 and C16:1ω7C as major fatty acids but the presence of iso-diabolic acid was unnoticed in previous studies, most probably because the complex lipid that contained this moiety was not extractable from the cells; it could only be released by hydrolysis. Direct analysis of intact polar lipids in the Bligh-Dyer extract of three acidobacterial strains, indeed, did not reveal any membrane-spanning lipids containing iso-diabolic acid. In 3 of the 17 strains, ether-bound iso-diabolic acid was detected after hydrolysis of the cells, including one branched GDGT containing iso-diabolic acid-derived alkyl chains. Since the GDGT distribution in soils is much more complex, branched GDGTs in soil likely also originate from other (acido)bacteria capable of biosynthesizing these components.

360 citations


Cites background from "Isolation and characterization of a..."

  • ...thermohydrosulfuricus (3), iso-diabolic acid was also detected only after hydrolysis of total cell material....

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  • ...iso-Diabolic acid has previously been encountered only in thermophilic Thermoanaerobacter species (3, 24, 32), where it fulfills a role as a membranespanning lipid....

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Journal ArticleDOI
TL;DR: It is demonstrated that the presence of membrane spanning ether-lipids and methyl branches shows a striking relationship with the growth boundaries of archaea and bacteria.
Abstract: The cytoplasmic membrane of a prokaryotic cell consists of a lipid bilayer or a monolayer that shields the cellular content from the environment. In addition, the membrane contains proteins that are responsible for transport of proteins and metabolites as well as for signalling and energy transduction. Maintenance of the functionality of the membrane during changing environmental conditions relies on the cell’s potential to rapidly adjust the lipid composition of its membrane. Despite the fundamental chemical differences between bacterial ester lipids and archaeal ether lipids, both types are functional under a wide range of environmental conditions. We here provide an overview of archaeal and bacterial strategies of changing the lipid compositions of their membranes. Some molecular adjustments are unique for archaea or bacteria, whereas others are shared between the two domains. Strikingly, shared adjustments were predominantly observed near the growth boundaries of bacteria. Here, we demonstrate that the presence of membrane spanning ether-lipids and methyl branches shows a striking relationship with the growth boundaries of archaea and bacteria.

249 citations

Journal ArticleDOI
TL;DR: Three main types of fermentative CO metabolism can be distinguished: hydrogenogenesis, methanogenesis, and acetogenesis, generating hydrogen, methane and acetate, respectively, with emphasis on the potential enzymatic routes and bio-energetics involved.
Abstract: Carbon monoxide can act as a substrate for different modes of fermentative anaerobic metabolism. The trait of utilizing CO is spread among a diverse group of microorganisms, including members of bacteria as well as archaea. Over the last decade this metabolism has gained interest due to the potential of converting CO-rich gas, such as synthesis gas, into bio-based products. Three main types of fermentative CO metabolism can be distinguished: hydrogenogenesis, methanogenesis, and acetogenesis, generating hydrogen, methane and acetate, respectively. Here, we review the current knowledge on these three variants of microbial CO metabolism with an emphasis on the potential enzymatic routes and bio-energetics involved.

131 citations


Cites background from "Isolation and characterization of a..."

  • ...No growth Kluyver and Schnellen, 1947 Methanosaeta concillii Aceticlastic Enzyme assay N.D. N.D....

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  • ...Methanothermobacter thermoautotrophicus Hydrogenotrophic Cultivation/enzyme assay 50 kPa Methane, hydrogen ∼200 Daniels et al., 1977; Wasserfallen et al., 2000 Methanosarcina thermophila Aceticlastic Cultivation >2 kPa Hydrogen, Methane N.D. Zinder and Anguish, 1992 Methanothrix sp. Strain CALS-1 Aceticlastic Cultivation <2 kPa Methane No growth Zinder and Anguish, 1992 Archaeoglobus fulgidusB Sulfate reducer Cultivation >136 kPa Acetate, formate ∼10 Henstra et al., 2007a Not determined parameters are marked N.D. AForward arrows (>) indicate inhibitory levels have not been reached; numbers displayed are the maximal level tested....

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  • ...Moorella thermoautotrophica EcH/ Cytochromes (H+) 7 (UM), 9 (DM) 33 (DM) 3.34 (UM) 2.53 (DM) 0.82 (DM) Savage and Drake, 1986; Savage et al., 1987; Collins et al., 1994 Moorella thermoacetica EcH/ Cytochromes (H+) 9 (DM) 16 (DM) 1.28 (UM) 0.46 (UM) Daniel et al., 1990; Collins et al., 1994; Pierce et al., 2008 Acetobacterium Woodii RnF (Na+ ) 13D (UM), 5.5A (UM + formate) 6.2A (UM) N.D. 1.05C (DM) Balch et al., 1977; Tschech and Pfennig, 1984; Genthner and Bryant, 1987; Hess et al., 2013; Bertsch and Müller, 2015 Blautia producta RnF (Na+ ) 1.5 (UM) 5 (UM) 2.13C (UM) 0.65C (UM) Lorowitz and Bryant, 1984; Geerligs et al., 1989 Clostridium aceticum RnF (N.D.) ∼10B (UM) 20 (UM) N.D. N.D. Braun et al., 1981; Sim et al., 2007...

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  • ...…2007 Thermosinus carboxydivorans Hot spring, Norris Basin 60 1.15 Sokolova et al., 2004a Thermoanaerobacter thermohydrosulfuricus ssp. carboxydovorans Geothermal spring, Turkey 70 N.D. Balk et al., 2009 Desulfotomaculum carboxydivorans Paper mill wastewater sludge 55 N.D. Parshina et al., 2005b...

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  • ...Methanobrevibacter arboriphilicus Hydrogenotrophic Enzyme assay N.D. N.D. N.D. Hammel et al., 1984 Methanosarcina acetivorans C2A Aceticlastic Cultivation/enzyme assay >150 kPa Methane, acetate, formate ∼20 Rother and Metcalf, 2004; Oelgeschläger and Rother, 2009 Methanosarcina barkeri Aceticlastic Cultivation/enzyme assay >100 kPa Hydrogen, Methane ∼65 O’Brien et al., 1984; Bott et al., 1986 Methanobacterium formicicum Hydrogenotrophic Cultivation N.D. N.D....

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Journal ArticleDOI
TL;DR: Examination of lipid composition of seven phylogenetically divergent strains of subdivision 4 of the Acidobacteria, a bacterial group that is commonly encountered in soil, found the presence of ether bonds in the membrane lipids does not seem to be an adaptation to temperature, because the five mesophilic isolates contained a larger amount of ether lipids than the thermophile “Ca. Chloracidobacterium thermophilum.”
Abstract: Recently, iso-diabolic acid (13,16-dimethyl octacosanedioic acid) has been identified as a major membrane-spanning lipid of subdivisions 1 and 3 of the Acidobacteria, a highly diverse phylum within the Bacteria. This finding pointed to the Acidobacteria as a potential source for the bacterial glycerol dialkyl glycerol tetraethers that occur ubiquitously in peat, soil, lakes, and hot springs. Here, we examined the lipid composition of seven phylogenetically divergent strains of subdivision 4 of the Acidobacteria, a bacterial group that is commonly encountered in soil. Acid hydrolysis of total cell material released iso-diabolic acid derivatives in substantial quantities (11 to 48% of all fatty acids). In contrast to subdivisions 1 and 3 of the Acidobacteria, 6 out of the 7 species of subdivision 4 (excepting “Candidatus Chloracidobacterium thermophilum”) contained iso-diabolic acid ether bound to a glycerol in larger fractional abundance than iso-diabolic acid itself. This is in agreement with the analysis of intact polar lipids (IPLs) by high-performance liquid chromatography-mass spectrometry (HPLC-MS), which showed the dominance of mixed ether-ester glycerides. iso-Diabolic acid-containing IPLs were not identified, because these IPLs are not released with a Bligh-Dyer extraction, as observed before when studying lipid compositions of subdivisions 1 and 3 of the Acidobacteria. The presence of ether bonds in the membrane lipids does not seem to be an adaptation to temperature, because the five mesophilic isolates contained a larger amount of ether lipids than the thermophile “Ca. Chloracidobacterium thermophilum.” Furthermore, experiments with Pyrinomonas methylaliphatogenes did not reveal a major influence of growth temperature over the 50 to 69°C range.

102 citations


Cites background from "Isolation and characterization of a..."

  • ...(61), Sarcina ventriculi (62), members of the 304 Thermotogales (2,57,63-65), Thermoanaerobacter species (58,59,62) and Acidobacteria of 305 SD 1, 3 (14), and 4 (this work), respectively....

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  • ...This lipid was identified 254 previously as an abundant lipid in Acidobacteria of SD 1 and 3 (14) and in thermophilic 255 Thermoanaerobacter species (58-60), in which they fulfill a role as membrane-spanning 256 lipids....

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Journal ArticleDOI
TL;DR: Recent advances in the isolation of novel phylogenetic groups utilizing formate or CO, the remarkable genetic engineering that enhances H2 productivity, and the practical implementation of H2 production from C1 substrates are focused on.

63 citations

References
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Journal ArticleDOI
TL;DR: The fact that T. ferrireducens contains c-type cytochromes and T. siderophilus lacks them confirms the operation of different mechanisms of ferric iron reduction in these species, and suggests that CO2 fixation in this organism involves the anaerobic acetyl-CoA pathway.
Abstract: Growth physiology of the iron-reducing bacteria Thermoterrabacterium ferrireducens and Thermoanaerobacter siderophilus was investigated. The stimulation of the organotrophic growth of T. ferrireducens and T. siderophilusin the presence of Fe(III) was shown to be due to the utilization of ferric iron as an electron acceptor in catabolic processes and not to the effect exerted on the metabolism by Fe(II) or by changes in the redox potential. It was established that Fe(III) reduction in T. ferrireducens is not a detoxication strategy. In T. siderophilus, this process is carried out to alleviate the inhibitory effect of hydrogen. T. ferrireducens was shown to be capable of lithoautotrophic growth with molecular hydrogen as an electron donor and amorphous ferric oxide as an electron acceptor, in the absence of any organic substances. The minimum threshold of H2 consumption was 3 × 10–5 vol % of H2. The presence of CO dehydrogenase activity in T. ferrireducens suggests that CO2 fixation in this organism involves the anaerobic acetyl-CoA pathway. T. siderophilus failed to grow under lithoautotrophic conditions. The fact that T. ferrireducens contains c-type cytochromes and T. siderophilus lacks them confirms the operation of different mechanisms of ferric iron reduction in these species.

14 citations

Journal ArticleDOI
TL;DR: The proposed structures of these novel lipid components were the ones in which two head groups were linked by the membrane spanning fatty acyl component (DME C30) and regular chain fatty acids on glycerol moiety of each head group.
Abstract: Novel membrane lipids containing the unusual very long chain fatty acid, α,ω-13,16-dimethyloctacosanedioate dimethyl ester (DME C30) was isolated and purified from thermophilic anaerobic eubacterium, Thermoanaerobacter ethanolicus. Structures of the lipids containing the bifunctional fatty acyl components were proposed by various analyses such as 1 H, 1 3 C, 3 1 P nuclear magnetic resonance (NMR), Fourier transform infrared (FrIR) spectroscopy, gas chromatography/mass spectrometry (GC/MS) and fast atom bombardment mass spectrometry (FAB/MS). Combined with the GC/MS, 1 H and 1 3 C NMR data, we confirmed that the head groups of the lipids contained the glycerol and/or glucosamine molecules. 3 1 P NMR spectrum also showed that the lipids contained phosphate in a phosphodiester linkage. The proposed structures of these novel lipid components were the ones in which two head groups were linked by the membrane spanning fatty acyl component (DME C30) and regular chain fatty acids on glycerol moiety of each head group.

9 citations


"Isolation and characterization of a..." refers background in this paper

  • ...Interestingly, in all three strains the uncommon membrane-spanning a,x13,16-dimethyl-octacosanedioic acid, previously detected in the phylogenetically related T. ethanolicus (Jung et al. 1994; Lee et al. 2002) was present in substantial amounts, especially in strain TLO....

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