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. 2005 Nov;1(5):e65.
doi: 10.1371/journal.pgen.0010065. Epub 2005 Nov 25.

Life in Hot Carbon Monoxide: The Complete Genome Sequence of Carboxydothermus Hydrogenoformans Z-2901

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Free PMC article

Life in Hot Carbon Monoxide: The Complete Genome Sequence of Carboxydothermus Hydrogenoformans Z-2901

Martin Wu et al. PLoS Genet. .
Free PMC article

Erratum in

  • PLoS Genet. 2006 Apr;2(4):e60. Haft, Daniel H [added]

Abstract

We report here the sequencing and analysis of the genome of the thermophilic bacterium Carboxydothermus hydrogenoformans Z-2901. This species is a model for studies of hydrogenogens, which are diverse bacteria and archaea that grow anaerobically utilizing carbon monoxide (CO) as their sole carbon source and water as an electron acceptor, producing carbon dioxide and hydrogen as waste products. Organisms that make use of CO do so through carbon monoxide dehydrogenase complexes. Remarkably, analysis of the genome of C. hydrogenoformans reveals the presence of at least five highly differentiated anaerobic carbon monoxide dehydrogenase complexes, which may in part explain how this species is able to grow so much more rapidly on CO than many other species. Analysis of the genome also has provided many general insights into the metabolism of this organism which should make it easier to use it as a source of biologically produced hydrogen gas. One surprising finding is the presence of many genes previously found only in sporulating species in the Firmicutes Phylum. Although this species is also a Firmicutes, it was not known to sporulate previously. Here we show that it does sporulate and because it is missing many of the genes involved in sporulation in other species, this organism may serve as a "minimal" model for sporulation studies. In addition, using phylogenetic profile analysis, we have identified many uncharacterized gene families found in all known sporulating Firmicutes, but not in any non-sporulating bacteria, including a sigma factor not known to be involved in sporulation previously.

Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Genomic Organization of C. hydrogenoformans
From the outside inward the circles show: (1, 2) predicted protein-coding regions on the plus and minus strands (colors were assigned according to the color code of functional classes; (3) prophage (orange) and CRISPR (pink) regions; (4) χ2-square score of tri-nucleotide composition; (5) GC skew (blue indicates a positive value and red a negative value); (6) tRNAs (green); (7) rRNAs (blue) and structural RNAs (red).
Figure 2
Figure 2. Genome Tree of Representatives of Firmicutes
A maximum likelihood tree was built from concatenated protein sequences of 31 universal housekeeping genes and rooted by two outgroup Actinobacteria (high GC Gram-positives) species: Corynebacterium glutamicum and Streptomyces coelicolor. Bootstrap support values (out of 100 runs) for branches of interest are shown beside them. Each species' ability to sporulate and its number of putative orthologs of the 175 known B. subtilis sporulation genes are also shown.
Figure 3
Figure 3. Genome Locations of Genes Predicted to Encode Five CODH Complexes
The genome locations of the genes encoding the five CooS homologs (labelled CooS I-V) are shown. Also shown are neighboring genes that are predicted to encode the five distinct CODH complexes (CODH I-V) with each CooS homolog. Possible cellular roles for four of the five CODH complexes are indicated.
Figure 4
Figure 4. Phylogenetic Tree of CooS Homologs
The figure shows a maximum-likelihood tree of CooS homologs. The tree indicates the five CooS homologs in C. hydrogenoformans are not the result of recent duplications but instead are from distinct subfamilies. The other CooS homologs included in the tree were obtained from the NCBI nr database and include some from incomplete genome sequences generated by United States Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/).
Figure 5
Figure 5. Predicted Complete Acetyl-CoA Pathway of Carbon Fixation in C. hydrogenoformans
Genes predicted to encode each step in the acetyl-CoA pathway of carbon fixation were identified in the genome. The locus numbers are indicated on the figure.
Figure 6
Figure 6. An Electron Micrograph of a C. hydrogenoformans Endospore
The finding of homologs of many genes involved in sporulation in other species led us to test whether C. hydrogenoformans also could form an endospore. Under stressful growth conditions, endospore-like structures form. We note that even though homologs could not be found in the genome for many genes that in other species are involved in protective outer-layer (cortex, coat, and exosporium) formation, those structures seem to be visible and intact.
Figure 7
Figure 7. Phylogenetic Profile Analysis of Sporulation in C. hydrogenoformans
For each protein encoded by the C. hydrogenoformans genome, a profile was created of the presence or absence of orthologs of that protein in the predicted proteomes of all other complete genome sequences. Proteins were then clustered by the similarity of their profiles, thus allowing the grouping of proteins by their distribution patterns across species. Examination of the groupings showed one cluster consisting of mostly homologs of sporulation proteins. This cluster is shown with C. hydrogenoformans proteins in rows (and the prediced function and protein ID indicated on the right) and other species in columns with presence of a ortholog indicated in red and absence in black. The tree to the left represents the portion of the cluster diagram for these proteins. Note that most of these proteins are found only in a few species represented in red columns near the center of the diagram. The species corresponding to these columns are indicated. We also note that though most of the proteins in this cluster, for which functions can be predicted, are predicted to be involved in sporulation and some have no predictable functions (highlighted in blue). This indicates that functions of these proteins' homologs have not been characterized in other species. Since these proteins show similar distribution patterns to so many proteins with roles in sporulation, we predict that they represent novel sporulation functions.

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