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Evidence for Horizontal Gene Transfer of Anaerobic Carbon Monoxide Dehydrogenases

Journal Article · · Frontiers in Microbiology
 [1];  [2];  [3];  [2];  [4];  [4];  [5]
  1. Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States). Inst. of Marine and Environmental Technology; Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States). Dept. of Microbiology and Immunology; DOE/OSTI
  2. Russian Academy of Sciences (RAS), Moscow (Russian Federation). Winogradsky Inst. of Microbiology
  3. Univ. of Chicago, IL (United States). Dept. of Geophysical Sciences
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States). Inst. of Marine and Environmental Technology; Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States). Dept. of Microbiology and Immunology

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 energyconverting 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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1628055
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 3; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (50)

Structure of the Ni/Fe-S Protein Subcomponent of the Acetyl-CoA Decarbonylase/Synthase Complex from Methanosarcina thermophila at 26-Å Resolution journal December 1999
The structural genes encoding CO dehydrogenase subunits (cox L, M and S) in Pseudomonas carboxydovorans OM5 reside on plasmid pHCG3 and are, with the exception of Streptomyces thermoautotrophicus, conserved in carboxydotrophic bacteria journal February 1992
Carbon monoxide conversion by thermophilic sulfate-reducing bacteria in pure culture and in co-culture with Carboxydothermus hydrogenoformans journal January 2005
Sphingopyxis jiangsuensis sp. nov. Isolated From the Surface Water of the Yellow Sea journal June 2022
Basic local alignment search tool journal October 1990
Mechanism of CO oxidation by carbon monoxide dehydrogenase from Clostridium thermoaceticum and its inhibition by anions journal June 1995
The Ni-Containing Carbon Monoxide Dehydrogenase Family:  Light at the End of the Tunnel? journal January 2002
A Novel Binuclear [CuSMo] Cluster at the Active Site of Carbon Monoxide Dehydrogenase:  Characterization by X-ray Absorption Spectroscopy journal January 2003
Mechanism of Carbon Monoxide Oxidation by the Carbon Monoxide Dehydrogenase/Acetyl-CoA Synthase from Clostridium thermoaceticum :  Kinetic Characterization of the Intermediates journal September 1997
Carbon Monoxide Induced Decomposition of the Active Site [Ni−4Fe−5S] Cluster of CO Dehydrogenase journal May 2004
Lateral gene transfer and the nature of bacterial innovation journal May 2000
Distribution, diversity and ecology of aerobic CO-oxidizing bacteria journal February 2007
Genetic basis for the establishment of endosymbiosis in Paramecium journal January 2019
Structural bases for the catalytic mechanism of Ni-containing carbon monoxide dehydrogenases journal January 2005
Purification and catalytic properties of a CO-oxidizing:H2-evolving enzyme complex from Carboxydothermus hydrogenoformans: CO-oxidizing:H2-evolving enzyme complex journal October 2002
A functional Ni-Ni-[4Fe-4S] cluster in the monomeric acetyl-CoA synthase from Carboxydothermus hydrogenoformans journal December 2003
Shifting the genomic gold standard for the prokaryotic species definition journal October 2009
Anaerobic growth of a Rhodopseudomonas species in the dark with carbon monoxide as sole carbon and energy substrate. journal September 1976
Molecular archaeology of the Escherichia coli genome journal August 1998
Crystal structure and mechanism of CO dehydrogenase, a molybdo iron-sulfur flavoprotein containing S-selanylcysteine journal August 1999
Life with Carbon Monoxide journal January 2004
A Rapid Bootstrap Algorithm for the RAxML Web Servers journal October 2008
TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops journal November 2008
Local homology recognition and distance measures in linear time using compressed amino acid alphabets journal January 2004
Secondary structure effects on DNA hybridization kinetics: a solution versus surface comparison journal June 2006
Notes on the characterization of prokaryote strains for taxonomic purposes journal January 2010
Thermosinus carboxydivorans gen. nov., sp. nov., a new anaerobic, thermophilic, carbon-monoxide-oxidizing, hydrogenogenic bacterium from a hot pool of Yellowstone National Park
  • Sokolova, Tatyana G.; González, Juan M.; Kostrikina, Nadezhda A.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 54, Issue 6 https://doi.org/10.1099/ijs.0.63186-0
journal November 2004
Horizontal Gene Transfer in Bacterial and Archaeal Complete Genomes journal November 2000
Base-Calling of Automated Sequencer Traces Using Phred.  I. Accuracy Assessment journal March 1998
Base-Calling of Automated Sequencer Traces Using Phred. II. Error Probabilities journal March 1998
Consed: A Graphical Tool for Sequence Finishing journal March 1998
‘That which does not kill us only makes us stronger’: the role of carbon monoxide in thermophilic microbial consortia journal May 2009
Genetic analysis of Carboxydothermus hydrogenoformans carbon monoxide dehydrogenase genes cooF and cooS journal October 2000
Crystal Structure of a Carbon Monoxide Dehydrogenase Reveals a [Ni-4Fe-5S] Cluster journal August 2001
Environmental Genomics Reveals a Single-Species Ecosystem Deep Within Earth journal October 2008
Identification of a Novel Class of Membrane-Bound [NiFe]-Hydrogenases in Thermococcus onnurineus NA1 by In Silico Analysis journal July 2010
Uptake ofCarbon Monoxide and Hydrogen at Environmentally Relevant Concentrationsby Mycobacteria† journal December 2003
Molybdopterin in carbon monoxide oxidase from carboxydotrophic bacteria journal February 1984
Isolation of an enzyme complex with carbon monoxide dehydrogenase activity containing corrinoid and nickel from acetate-grown Methanosarcina thermophila. journal January 1986
Genetic and physiological characterization of the Rhodospirillum rubrum carbon monoxide dehydrogenase system. journal January 1992
Molecular characterization of the gene cluster coxMSL encoding the molybdenum-containing carbon monoxide dehydrogenase of Oligotropha carboxidovorans. journal January 1995
Two Membrane-Associated NiFeS-Carbon Monoxide Dehydrogenases from the Anaerobic Carbon-Monoxide-Utilizing Eubacterium Carboxydothermus hydrogenoformans journal September 2001
Biology of Aerobic Carbon Monoxide-Oxidizing Bacteria journal October 1983
Co Dehydrogenase journal October 1995
MUSCLE: a multiple sequence alignment method with reduced time and space complexity journal August 2004
BEAST: Bayesian evolutionary analysis by sampling trees journal January 2007
Enzymology of the Wood-Ljungdahl Pathway of Acetogenesis journal March 2008
Life in Hot Carbon Monoxide: The Complete Genome Sequence of Carboxydothermus hydrogenoformans Z-2901 journal January 2005
A Benchmark of Parametric Methods for Horizontal Transfers Detection journal April 2010
Regulation of Multiple Carbon Monoxide Consumption Pathways in Anaerobic Bacteria journal January 2011

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