Comparative study of overlapping genes in the genomes of Mycoplasma genitalium and Mycoplasma pneumoniae

Fukuda, Yoko; Washio, Takumi; Tomita, Masaru

doi:10.1093/nar/27.8.1847

Cited by 53 publications

(49 citation statements)

References 11 publications

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“…strain SJY1 (23,24). In S33, ndhA and ndhB overlap 4 bp, which is common for the genes of multiple subunits enzyme in microorganisms and is helpful for rapid cotranscription and translation and their regulation (62,63). Interestingly, there is a 26-kb distance between ndhAB-hno and pno-hsh, where 6 of 12 ORFs encode mobile element proteins, suggesting that these genes might come from other bacteria by the way of lateral gene transfer.…”

Section: Discussionmentioning

confidence: 99%

Nicotine Dehydrogenase Complexed with 6-Hydroxypseudooxynicotine Oxidase Involved in the Hybrid Nicotine-Degrading Pathway in Agrobacterium tumefaciens S33

Xie

et al. 2016

Appl Environ Microbiol

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c Nicotine, a major toxic alkaloid in tobacco wastes, is degraded by bacteria, mainly via pyridine and pyrrolidine pathways. Previously, we discovered a new hybrid of the pyridine and pyrrolidine pathways in Agrobacterium tumefaciens S33 and characterized its key enzyme 6-hydroxy-3-succinoylpyridine (HSP) hydroxylase. Here, we purified the nicotine dehydrogenase initializing the nicotine degradation from the strain and found that it forms a complex with a novel 6-hydroxypseudooxynicotine oxidase. The purified complex is composed of three different subunits encoded by ndhAB and pno, where ndhA and ndhB overlap by 4 bp and are ϳ26 kb away from pno. As predicted from the gene sequences and from chemical analyses, NdhA (82.4 kDa) and NdhB (17.1 kDa) harbor a molybdopterin cofactor and two [2Fe-2S] clusters, respectively, whereas Pno (73.3 kDa) harbors an flavin mononucleotide and a [4Fe-4S] cluster. Mutants with disrupted ndhA or ndhB genes did not grow on nicotine but grew well on 6-hydroxynicotine and HSP, whereas the pno mutant did not grow on nicotine or 6-hydroxynicotine but grew well on HSP, indicating that NdhA and NdhB are responsible for initialization of nicotine oxidation. We successfully expressed pno in Escherichia coli and found that the recombinant Pno presented 2,6-dichlorophenolindophenol reduction activity when it was coupled with 6-hydroxynicotine oxidation. The determination of reaction products catalyzed by the purified enzymes or mutants indicated that NdhAB catalyzed nicotine oxidation to 6-hydroxynicotine, whereas Pno oxidized 6-hydroxypseudooxynicotine to 6-hydroxy-3-succinoylsemialdehyde pyridine. These results provide new insights into this novel hybrid pathway of nicotine degradation in A. tumefaciens S33.A grobacterium tumefaciens is well known for its ability to induce crown gall tumors in dicotyledonous plants and mediate interkingdom genetic transfer, for that it is widely used in plant molecular biology and biotechnology (1). Interestingly, some strains of this species are also able to degrade xenobiotics such as cyanuric acid, iminodisuccinate, and methylene urea (2-4). We isolated A. tumefaciens strain S33, which has the strong ability to degrade the natural alkaloid nicotine from the rhizospheric soil of a tobacco plant (5, 6).Nicotine is a major alkaloid in tobacco, which causes tobacco addiction and may result in diseases such as pulmonary disease and cancer (7,8), and it is the primary toxic compound in tobacco wastes. The tobacco-manufacturing process and all activities using tobacco produce a large amount of solid or liquid waste containing high concentrations of nicotine, which are classified as "toxic and hazardous wastes" by the European Union (9). Therefore, detoxification of tobacco wastes is a major concern for public health and the environment. The discovery of nicotine degradation by microorganisms provides an alternative way to dispose of such wastes (10-12).Microbial degradation of nicotine attracts attention because it represents a method to treat the tobacco waste...

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Section: Discussionmentioning

confidence: 99%

Nicotine Dehydrogenase Complexed with 6-Hydroxypseudooxynicotine Oxidase Involved in the Hybrid Nicotine-Degrading Pathway in Agrobacterium tumefaciens S33

Xie

et al. 2016

Appl Environ Microbiol

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“…This has all the characteristics of an Internal Overlap: the Overlapping protein is thought to be younger than the much longer replicase (Keese and Gibbs 1992)-which we can confirm with our PDI measures for the two genes-and the overlap has arisen via a +1 frameshift. In bacteria, a comparative analyses of the genomes of Mycoplasma genitalium and Mycoplasma pneumoniae found some relatively long Terminal Overlaps, which appeared to be incidental elongations of the coding region by loss of the 3Ј stop codon (Fukuda et al 1999). The investigators found poor conservation of these elongated regions compared with homologs in other taxa, and suggested that these regions had little or no functional role at present; they appear to us to be other examples of gene overlap in the process of acquiring function.…”

Section: Discussionmentioning

confidence: 99%

The evolution of genome compression and genomic novelty in RNA viruses

Belshaw

Pybus²,

Rambaut³

2007

Genome Res.

154

176

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The genomes of RNA viruses are characterized by their extremely small size and extremely high mutation rates (typically 10 kb and 10 −4 /base/replication cycle, respectively), traits that are thought to be causally linked. One aspect of their small size is the genome compression caused by the use of overlapping genes (where some nucleotides code for two genes). Using a comparative analysis of all known RNA viral species, we show that viruses with larger genomes tend to have less gene overlap. We provide a numerical model to show how a high mutation rate could lead to gene overlap, and we discuss the factors that might explain the observed relationship between gene overlap and genome size. We also propose a model for the evolution of gene overlap based on the co-opting of previously unused ORFs, which gives rise to two types of overlap: (1) the creation of novel genes inside older genes, predominantly via +1 frameshifts, and (2) the incremental increase in overlap between originally contiguous genes, with no frameshift preference. Both types of overlap are viewed as the creation of genomic novelty under pressure for genome compression. Simulations based on our model generate the empirical size distributions of overlaps and explain the observed frameshift preferences. We suggest that RNA viruses are a good model system for the investigation of general evolutionary relationship between genome attributes such as mutational robustness, mutation rate, and size.

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“…Second, unlike genomic sequencing, where both strands are sequenced, RNA-Seq experiments are usually strand-specific. To be effective, transcriptome assemblers will need to take advantage of strand information to resolve overlapping sense and anti-sense transcripts [11][12][13][14] . Finally, it is generally difficult for short read assemblers to resolve repeat structures in a genome assembly; this problem is exacerbated during transcriptome assembly because transcript variants from the same gene can share many exons..…”

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confidence: 99%