Chthonomonas calidirosea gen. nov., sp. nov., an aerobic, pigmented, thermophilic micro-organism of a novel bacterial class, Chthonomonadetes classis nov., of the newly described phylum Armatimonadetes originally designated candidate division OP10
Abstract:An aerobic, saccharolytic, obligately thermophilic, motile, non-spore-forming bacterium, strain T49T, was isolated from geothermally heated soil at Hell’s Gate, Tikitere, New Zealand. On the basis of 16S rRNA gene sequence similarity, T49T is the first representative of a new class in the newly described phylum Armatimonadetes, formerly known as candidate division OP10. Cells of strain T49T stained Gram-negative and were catalase-positive and oxidase-negative. Cells possessed a highly corrugated outer membrane… Show more
“…Succinyl CoA is generated via isocitrate dehydrogenase and 2-oxoglutarate dehydrogenase complex. T49 T has previously been reported as exhibiting obligate chemoheterotrophic metabolism (Lee et al, 2011). In addition to these previous cultivation experiments, we predicted and experimentally confirmed its ability to utilise several less-common carbohydrates and associated derivatives, including sorbitol and galactan.…”
Section: Sigma Factorssupporting
confidence: 50%
“…The placement of T49 T within the phylum Armatimonadetes was previously investigated through 16S rRNA-based analysis (Lee et al, 2011). However, the 16S rRNA gene alone does not reliably resolve the relationships among deeply branching phyla (Delsuc et al, 2005).…”
Section: Phylogenetic Analysismentioning
confidence: 99%
“…Although phosphoenolpyruvate carboxylase is a critical enzyme for the first step of carbon fixation in C4 and crassulacean acid metabolism plants (O' Leary and Diaz, 1982), the role of phosphoenolpyruvate carboxylase here appears to be limited to an anaplerotic role in maintaining the balance of intermediary molecules within the tricarboxylic acid cycle (Dunn, 2011); this is logical as the fixation of carbon dioxide is energetically unfavourable compared with the organic carbon substrates from which C. calidirosea T49 T is capable of deriving energy. Nitrogen uptake by T49 T was experimentally determined to be via ammonia assimilation and/or amino acid uptake (Lee et al, 2011). It appears that ammonia can be assimilated via glutamate or glycine and modified by a complete tetrahydrofolate onecarbon pathway.…”
Section: Sigma Factorsmentioning
confidence: 99%
“…The first reported cultivated strains of candidate division OP10, strains T49 T and P488, were isolated from geothermally heated soils in New Zealand (Stott et al, 2008). To date, three species from the Armatimonadetes have been formally described: C. calidirosea T49 T (Lee et al, 2011), Fimbriimonas ginsengisoli GSoil348 T and the phylum type species, Armatimonas rosea YO-36 T (Tamaki et al, 2011). These strains are only distantly related, with 16S rRNA gene sequence similarities of o80% (Dunfield et al, 2012).…”
Section: Introductionmentioning
confidence: 99%
“…However, in contrast to the mesophilic and neutrophilic A. rosea and F. ginsengisoli, T49 T is a thermophile (T opt 68 1C, range: 50-73 1C) and a moderate acidophile (growth pH 5.3, range: pH 4.7-5.8). The three strains differ in mol% G þ C content, cell morphology, fatty acid content, quinone and salt tolerance (Lee et al, 2011, Tamaki et al, 2011). In addition, T49 T appears to have a much broader carbohydrate utilisation range, including a partially cellulolytic phenotype; it can hydrolyse amorphous polysaccharides but not linear polysaccharides (Lee et al, 2011).…”
Most of the lineages of bacteria have remained unknown beyond environmental surveys using molecular markers. Until the recent characterisation of several strains, the phylum Armatimonadetes (formerly known as 'candidate division OP10') was a dominant and globally-distributed lineage within this 'uncultured majority'. Here we report the first Armatimonadetes genome from the thermophile Chthonomonas calidirosea T49 T and its role as a saccharide scavenger in a geothermal steam-affected soil environment. Phylogenomic analysis indicates T49 T to be related closely to the phylum Chloroflexi. The predicted genes encoding for carbohydrate transporters (27 carbohydrate ATP-binding cassette transporter-related genes) and carbohydrate-metabolising enzymes (including at least 55 putative enzymes with glycosyl hydrolase domains) within the 3.43 Mb genome help explain its ability to utilise a wide range of carbohydrates as well as its inability to break down extracellular cellulose. The presence of only a single class of branched amino acid transporter appears to be the causative step for the requirement of isoleucine for growth. The genome lacks many commonly conserved operons (for example, lac and trp). Potential causes for this, such as dispersion of functionally related genes via horizontal gene transfer from distant taxa or recent genome recombination, were rejected. Evidence suggests T49 T relies on the relatively abundant r-factors, instead of operonic organisation, as the primary means of transcriptional regulation. Examination of the genome with physiological data and environmental dynamics (including interspecific interactions) reveals ecological factors behind the apparent elusiveness of T49 T to cultivation and, by extension, the remaining 'uncultured majority' that have so far evaded conventional microbiological techniques.
“…Succinyl CoA is generated via isocitrate dehydrogenase and 2-oxoglutarate dehydrogenase complex. T49 T has previously been reported as exhibiting obligate chemoheterotrophic metabolism (Lee et al, 2011). In addition to these previous cultivation experiments, we predicted and experimentally confirmed its ability to utilise several less-common carbohydrates and associated derivatives, including sorbitol and galactan.…”
Section: Sigma Factorssupporting
confidence: 50%
“…The placement of T49 T within the phylum Armatimonadetes was previously investigated through 16S rRNA-based analysis (Lee et al, 2011). However, the 16S rRNA gene alone does not reliably resolve the relationships among deeply branching phyla (Delsuc et al, 2005).…”
Section: Phylogenetic Analysismentioning
confidence: 99%
“…Although phosphoenolpyruvate carboxylase is a critical enzyme for the first step of carbon fixation in C4 and crassulacean acid metabolism plants (O' Leary and Diaz, 1982), the role of phosphoenolpyruvate carboxylase here appears to be limited to an anaplerotic role in maintaining the balance of intermediary molecules within the tricarboxylic acid cycle (Dunn, 2011); this is logical as the fixation of carbon dioxide is energetically unfavourable compared with the organic carbon substrates from which C. calidirosea T49 T is capable of deriving energy. Nitrogen uptake by T49 T was experimentally determined to be via ammonia assimilation and/or amino acid uptake (Lee et al, 2011). It appears that ammonia can be assimilated via glutamate or glycine and modified by a complete tetrahydrofolate onecarbon pathway.…”
Section: Sigma Factorsmentioning
confidence: 99%
“…The first reported cultivated strains of candidate division OP10, strains T49 T and P488, were isolated from geothermally heated soils in New Zealand (Stott et al, 2008). To date, three species from the Armatimonadetes have been formally described: C. calidirosea T49 T (Lee et al, 2011), Fimbriimonas ginsengisoli GSoil348 T and the phylum type species, Armatimonas rosea YO-36 T (Tamaki et al, 2011). These strains are only distantly related, with 16S rRNA gene sequence similarities of o80% (Dunfield et al, 2012).…”
Section: Introductionmentioning
confidence: 99%
“…However, in contrast to the mesophilic and neutrophilic A. rosea and F. ginsengisoli, T49 T is a thermophile (T opt 68 1C, range: 50-73 1C) and a moderate acidophile (growth pH 5.3, range: pH 4.7-5.8). The three strains differ in mol% G þ C content, cell morphology, fatty acid content, quinone and salt tolerance (Lee et al, 2011, Tamaki et al, 2011). In addition, T49 T appears to have a much broader carbohydrate utilisation range, including a partially cellulolytic phenotype; it can hydrolyse amorphous polysaccharides but not linear polysaccharides (Lee et al, 2011).…”
Most of the lineages of bacteria have remained unknown beyond environmental surveys using molecular markers. Until the recent characterisation of several strains, the phylum Armatimonadetes (formerly known as 'candidate division OP10') was a dominant and globally-distributed lineage within this 'uncultured majority'. Here we report the first Armatimonadetes genome from the thermophile Chthonomonas calidirosea T49 T and its role as a saccharide scavenger in a geothermal steam-affected soil environment. Phylogenomic analysis indicates T49 T to be related closely to the phylum Chloroflexi. The predicted genes encoding for carbohydrate transporters (27 carbohydrate ATP-binding cassette transporter-related genes) and carbohydrate-metabolising enzymes (including at least 55 putative enzymes with glycosyl hydrolase domains) within the 3.43 Mb genome help explain its ability to utilise a wide range of carbohydrates as well as its inability to break down extracellular cellulose. The presence of only a single class of branched amino acid transporter appears to be the causative step for the requirement of isoleucine for growth. The genome lacks many commonly conserved operons (for example, lac and trp). Potential causes for this, such as dispersion of functionally related genes via horizontal gene transfer from distant taxa or recent genome recombination, were rejected. Evidence suggests T49 T relies on the relatively abundant r-factors, instead of operonic organisation, as the primary means of transcriptional regulation. Examination of the genome with physiological data and environmental dynamics (including interspecific interactions) reveals ecological factors behind the apparent elusiveness of T49 T to cultivation and, by extension, the remaining 'uncultured majority' that have so far evaded conventional microbiological techniques.
Chtho.no.mo.na.de'tes. N.L. fem. pl. n.
Chthonomonadetes
the class of the order
Chthonomonadales
.
Armatimonadetes / Chthonomonadetes
The class
Chthonomonadetes
was circumscribed for this volume on a phylogenetic basis via comparative 16S rRNA gene sequence analysis of a single isolated representative and uncultured representatives from multiple terrestrial and aquatic habitats; the class contains the order
Chthonomonadales
.
Type order
:
Chthonomonadales
Lee, Dunfield, Morgan, Crowe, Houghton, Vyssotski, Ryan, Lagutin, McDonald and Stott 2011, 2488
VP
.
Chtho.no.mo.na.da'ce.ae. N.L. fem. pl. n.
Chthonomonadaceae
the family of the genus
Chthonomonas
.
Armatimonadetes / Chthonomonadetes / Chthonomonadales / Chthonomonadaceae
The family
Chthonomonadaceae
was circumscribed for this volume on a phylogenetic basis via comparative 16S rRNA gene sequence analysis of a single isolated representative and uncultured representatives from multiple terrestrial and aquatic habitats; the family contains the genus
Chthonomonas
.
DNA G + C content (mol%)
: 54.4.
Type genus
:
Chthonomonas
Lee, Dunfield, Morgan, Crowe, Houghton, Vyssotski, Ryan, Lagutin, McDonald and Stott 2011, 2487
VP
.
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