MBE Advance Access published online on July 8, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn146
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Research Article |
Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification
Stres
* Swedish Agricultural University, Department of Microbiology, Uppsala, Sweden
University of Ljubljana, Biotechnical Faculty, Zootechnical Department, Groblje 3, 1230 Domzale, Slovenia
Uppsala University Hospital, Department of Radiology, Oncology, and Clinical Immunology, Uppsala, Sweden
Corresponding author: Christopher M. Jones, Box 7025, 750 07 Uppsala, Sweden, Phone: +4618673222, Fax: +4618673392. Email: Chris.Jones{at}mikrob.slu.se
Received for publication March 17, 2008. Revision received June 12, 2008. Accepted for publication June 25, 2008.
Denitrification is a facultative respiratory pathway in which nitrite (NO2-), nitric oxide (NO), and nitrous oxide (N2O) are successively reduced to nitrogen gas (N2), effectively closing the nitrogen cycle. The ability to denitrify is widely dispersed among prokaryotes, and this polyphyletic distribution has raised the possibility of horizontal gene transfer (HGT) having a substantial role in the evolution of denitrification. Comparisons of 16S rRNA and denitrification gene phylogenies in recent studies support this possibility, however these results remain speculative, as they are based on visual comparisons of phylogenies from partial sequences. We re-analyzed publicly available nirS, nirK, norB, and nosZ partial sequences using Bayesian and Maximum likelihood phylogenetic inference. Concomitant analysis of denitrification genes with 16S rRNA sequences from the same organisms showed substantial differences between the trees, which were supported by examining the posterior probability of monophyletic constraints at different taxonomic levels. While these differences suggest HGT of denitrification genes, the presence of structural variants for nirK, norB, and nosZ, makes it difficult to determine HGT from other evolutionary events. Additional analysis using phylogenetic networks and likelihood ratio tests of phylogenies based on full-length sequences retrieved from genomes also revealed significant differences in tree topologies among denitrification and 16S rRNA gene phylogenies, with the exception of the nosZ gene phylogeny within the dataset of the nirK-harboring genomes. However, inspection of codon usage and G+C content plots from complete genomes gave no evidence for recent HGT. Instead, the close proximity of denitrification gene copies in the genomes of several denitrifying bacteria suggests duplication. While HGT cannot be ruled out as a factor in the evolution of denitrification genes, our analysis suggests that other phenomena, such gene duplication/divergence and lineage sorting, may have differently influenced the evolution of each denitrification gene.
Key Words: Denitrification • phylogeny • nirK • nirS • norB • nosZ
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