Evidence for Horizontal Gene Transfer of Anaerobic Carbon Monoxide Dehydrogenases

Abstract

Carbon monoxide (CO) is commonly known as a toxic gas, yet both cultivation studies and emerging genome sequences of bacteria and archaea establish that CO is a widely utilized microbial growth substrate. In this study, we determined the prevalence of anaerobic carbon monoxide dehydrogenases ([Ni,Fe]-CODHs) in currently available genomic sequence databases. Currently, 185 out of 2887, or 6% of sequenced bacterial and archaeal genomes possess at least one gene encoding [Ni,Fe]-CODH, the key enzyme for anaerobic CO utilization. Many genomes encode multiple copies of [Ni,Fe]-CODH genes whose functions and regulation are correlated with their associated gene clusters. The phylogenetic analysis of this extended protein family revealed six distinct clades; many clades consisted of [Ni,Fe]-CODHs that were encoded by microbes from disparate phylogenetic lineages, based on 16S rRNA sequences, and widely ranging physiology. To more clearly define if the branching patterns observed in the [Ni,Fe]-CODH trees are due to functional conservation vs. evolutionary lineage, the genomic context of the [Ni,Fe]-CODH gene clusters was examined, and superimposed on the phylogenetic trees. On the whole, there was a correlation between genomic contexts and the tree topology, but several functionally similar [Ni,Fe]-CODHs were found in different clades. In addition, some distantly related organisms have similar [Ni,Fe]-CODH genes. Thermosinus carboxydivorans was used to observe horizontal gene transfer (HGT) of [Ni,Fe]-CODH gene clusters by applying Kullback–Leibler divergence analysis methods. Divergent tetranucleotide frequency and codon usage showed that the gene cluster of T. carboxydivorans that encodes a [Ni,Fe]-CODH and an energy-converting hydrogenase is dissimilar to its whole genome but is similar to the genome of the phylogenetically distant Firmicute, Carboxydothermus hydrogenoformans. These results imply that T carboxydivorans acquired this gene cluster via HGT from a relative of C. hydrogenoformans.

Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea

“…Phylogenetic analyses of these proteins show they are affiliated with 'clade E' (Supplementary Fig. 6) 12 and related to other methanogenic Euryarchaeota. The CooF sequences of Thermococcus spp, which also belong to this clade, have the ability to couple anaerobic CO oxidation to hydrogen production using cooS genes 26 .…”

Genomic Analysis of Calderihabitans maritimus KKC1, a Thermophilic, Hydrogenogenic, Carboxydotrophic Bacterium Isolated from Marine Sediment

“…The highest number of cooS genes ever reported in a single genome is five (cooS-I to -V) in C. hydrogenoformans (10). Thus, C. maritimus KKC1 harboring six CooS genes (five cooS genes conserving all residues linked to metal clusters [49] and one frameshifted cooS within the cooS-ACS gene cluster) possessed the most CooS genes of microbes with sequenced genomes.…”

“…We retrieved CooS amino acid sequences by BLASTP searches against Ref_seq proteins. We also used some sequences of the Ni-CODH phylogenetic tree from Techtmann et al (10) as references. The sequences were aligned and trimmed, and used to build an ML tree (bootstrap ϭ 100) as described above.…”

Complete Genome Sequence of Geobacillus strain Y4.1MC1, a Novel CO-Utilizing Geobacillus thermoglucosidasius Strain Isolated from Bath Hot Spring in Yellowstone National Park

“…Microbial consortia found in hot springs utilize carbon monoxide to obtain energy and fix carbon (reviewed in [1,2]). The microbes of these consortia utilize the Wood-Ljungdahl pathway, a pathway distinct from the one utilized by the aerobic organisms that oxidize CO with molecular oxygen [3,4].…”