A Nitrile Hydratase in the Eukaryote Monosiga brevicollis

European Molecular Biology Laboratory, Heidelberg, Germany.
PLoS ONE (Impact Factor: 3.23). 02/2008; 3(12):e3976. DOI: 10.1371/journal.pone.0003976
Source: PubMed


Bacterial nitrile hydratase (NHases) are important industrial catalysts and waste water remediation tools. In a global computational screening of conventional and metagenomic sequence data for NHases, we detected the two usually separated NHase subunits fused in one protein of the choanoflagellate Monosiga brevicollis, a recently sequenced unicellular model organism from the closest sister group of Metazoa. This is the first time that an NHase is found in eukaryotes and the first time it is observed as a fusion protein. The presence of an intron, subunit fusion and expressed sequence tags covering parts of the gene exclude contamination and suggest a functional gene. Phylogenetic analyses and genomic context imply a probable ancient horizontal gene transfer (HGT) from proteobacteria. The newly discovered NHase might open biotechnological routes due to its unconventional structure, its new type of host and its apparent integration into eukaryotic protein networks.

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    • "The additional sequence data presented here makes it unlikely that nitrile hydratase genes were transferred by an LGT event from prokaryotes directly to choanoflagellates, as proposed by Foerstner and colleagues [4]. An origin by LGT has been proposed for several other genes found in choanoflagellates [9]–[11]. "
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    ABSTRACT: Nitrile hydratases are enzymes involved in the conversion of nitrile-containing compounds into ammonia and organic acids. Although they are widespread in prokaryotes, nitrile hydratases have only been reported in two eukaryotes: the choanoflagellate Monosiga brevicollis and the stramenopile Aureococcus anophagefferens. The nitrile hydratase gene in M. brevicollis was believed to have arisen by lateral gene transfer from a prokaryote, and is a fusion of beta and alpha nitrile hydratase subunits. Only the alpha subunit has been reported in A. anophagefferens. Here we report the detection of nitrile hydratase genes in five eukaryotic supergroups: opisthokonts, amoebozoa, archaeplastids, CCTH and SAR. Beta-alpha subunit fusion genes are found in the choanoflagellates, ichthyosporeans, apusozoans, haptophytes, rhizarians and stramenopiles, and potentially also in the amoebozoans. An individual alpha subunit is found in a dinoflagellate and an individual beta subunit is found in a haptophyte. Phylogenetic analyses recover a clade of eukaryotic-type nitrile hydratases in the Opisthokonta, Amoebozoa, SAR and CCTH; this is supported by analyses of introns and gene architecture. Two nitrile hydratase sequences from an animal and a plant resolve in the prokaryotic nitrile hydratase clade. The evidence presented here demonstrates that nitrile hydratase genes are present in multiple eukaryotic supergroups, suggesting that a subunit fusion gene was present in the last common ancestor of all eukaryotes. The absence of nitrile hydratase from several sequenced species indicates that subunits were lost in multiple eukaryotic taxa. The presence of nitrile hydratases in many other eukaryotic groups is unresolved due to insufficient data and taxon sampling. The retention and expression of the gene in distantly related eukaryotic species suggests that it plays an important metabolic role. The novel family of eukaryotic nitrile hydratases presented in this paper represents a promising candidate for research into their molecular biology and possible biotechnological applications.
    PLoS ONE 04/2012; 7(4):e32867. DOI:10.1371/journal.pone.0032867 · 3.23 Impact Factor
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    • "Moreover, the fact that the lysA of M. brevicollis does have some introns argues against a contamination artifact from bacterial samples. Indeed, there has already been a report of an LGT from proteobacteria to M. brevicollis (Foerstner et al. 2008), which suggest that LGT from proteobacteria to choanoflagellates may not be so uncommon. Furthermore, the lysA homologs of N. gruberi, M. brevicollis, C. owczarzaki, and proteobacteria share a molecular synapomorphy, which is a 5 0 extension of a round 500 amino acids. "
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    ABSTRACT: Lysine biosynthesis occurs in two ways: the diaminopimelate (DAP) pathway and the alpha-aminoadipate (AAA) pathway. The former is present in eubacteria, plants, and algae, whereas the latter was understood to be almost exclusive to fungi. The recent finding of the alpha-aminoadipate reductase (AAR) gene, one of the core genes of the AAA pathway, in the marine protist Corallochytrium limacisporum was, therefore, believed to be a molecular synapomorphy of fungi and C. limacisporum. To test this hypothesis, we undertook a broader search for the AAR gene in eukaryotes, and also analyzed the distribution of the lysA gene, a core gene of the DAP pathway. We show that the evolutionary history of both genes, AAR and lysA, is much more complex than previously believed. Furthermore, the AAR gene is present in several unicellular opisthokonts, thus rebutting the theory that its presence is a molecular synapomorphy between C. limacisporum and fungi. AAR gene seems to be exclusive of Excavata and Unikonts, whereas the lysA gene is present in several unrelated taxa within all major eukaryotic lineages, indicating a role for several lateral gene transfer (LGT) events. Our data imply that the choanoflagellate Monosiga brevicollis and the "choanozoan" Capsaspora owczarzaki acquired their lysA copies from a proteobacterial ancestor. Overall, these observations represent new evidence that the role of LGT in the evolutionary history of eukaryotes may have been more significant than previously thought.
    Journal of Molecular Evolution 09/2009; 69(3):240-8. DOI:10.1007/s00239-009-9266-x · 1.68 Impact Factor
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