Plasmid Conjugation from Proteobacteria as Evidence for the Origin of Xenologous Genes in Cyanobacteria

Encinas, David; Garcillán-Barcia, M. Pilar; Santos-Merino, María; Delaye, Luis; Moya, Andrés; Cruz, Fernando de la

doi:10.1128/jb.01464-13

Cited by 16 publications

(11 citation statements)

References 62 publications

(58 reference statements)

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“…3). This finding was in accord with experimental data demonstrating that conjugation from E. coli to S. elongatus readily occurs by various proteobacterial conjugative plasmids (Encinas et al 2014).…”

Section: Xenologs In S Elongatus Exhibit Low Expression Levelssupporting

confidence: 89%

Identification of Xenologs and Their Characteristic Low Expression Levels in the Cyanobacterium Synechococcus elongatus

et al. 2015

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Horizontal gene transfer (HGT) is a central process in prokaryotic evolution. Once a gene is introduced into a genome by HGT, its contribution to the fitness of the recipient cell depends in part on its expression level. Here we show that in Synechococcus elongatus PCC 7942, xenologs derived from non-cyanobacterial sources exhibited lower expression levels than native genes in the genome. In accord with our observation, xenolog codon adaptation indexes also displayed relatively low expression values. These results are in agreement with previous reports that suggested the relative neutrality of most xenologs. However, we also demonstrated that some of the xenologs detected participated in cellular functions, including iron starvation acclimation and nitrate reduction, which corroborate the role of HGT in bacterial adaptation. For example, the expression levels of some of the xenologs detected are known to increase under iron-limiting conditions. We interpreted the overall pattern as an indication that there is a selection pressure against high expression levels of xenologs. However, when a xenolog protein product confers a selective advantage, natural selection can further modulate its expression level to meet the requirements of the recipient cell. In addition, we show that ORFans did not exhibit significantly lower expression levels than native genes in the genome, which suggested an origin other than xenology.

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Section: Xenologs In S Elongatus Exhibit Low Expression Levelssupporting

confidence: 89%

Identification of Xenologs and Their Characteristic Low Expression Levels in the Cyanobacterium Synechococcus elongatus

et al. 2015

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“…Smillie et al ( 2010 ) proposed that cyanobacteria may use an as-yet-uncharacterized system to conjugate because, within the phylum, the plasmids encoding relaxase and/or T4CP did not possess known T4SS or VirB4 (Table S1 ). Indeed, plasmid transfer from Proteobacteria to Cyanobacteria has been previously reported (Encinas et al, 2014 ). Further in-depth analyses and classification of Cyanobacteria plasmids are necessary to understand the spread of plasmids in this phylum.…”

Section: Plasmids In Cyanobacteriamentioning

confidence: 90%

Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy

2015

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Plasmids are important “vehicles” for the communication of genetic information between bacteria. The exchange of plasmids transmits pathogenically and environmentally relevant traits to the host bacteria, promoting their rapid evolution and adaptation to various environments. Over the past six decades, a large number of plasmids have been identified and isolated from different microbes. With the revolution of sequencing technology, more than 4600 complete sequences of plasmids found in bacteria, archaea, and eukaryotes have been determined. The classification of a wide variety of plasmids is not only important to understand their features, host ranges, and microbial evolution but is also necessary to effectively use them as genetic tools for microbial engineering. This review summarizes the current situation of the classification of fully sequenced plasmids based on their host taxonomy and their features of replication and conjugative transfer. The majority of the fully sequenced plasmids are found in bacteria in the Proteobacteria, Firmicutes, Spirochaetes, Actinobacteria, Cyanobacteria and Euryarcheota phyla, and key features of each phylum are included. Recent advances in the identification of novel types of plasmids and plasmid transfer by culture-independent methods using samples from natural environments are also discussed.

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“…Plasmids RP4, R388, and pKM101, which belong to the IncP-1, IncW, and IncN groups, respectively, are well-characterized and so-called broad-host-range plasmids because both their replication and conjugation systems can function in nearly all proteobacterial strains (30). The host ranges of these conjugation systems have been further shown to be broader than those of the replication systems; the former systems can deliver DNA into the bacterial recipient strains where the latter systems are not functional (31). Our results in this study similarly showed that the NAH7 conjugation system has a broader host range than its replication system; the conjugation system has an ability to conjugatively mobilize DNA into the alphaproteobacterial and betaproteobacterial strains, in which the replication system is most probably nonfunctional (Table 3).…”

Section: Discussionmentioning

confidence: 99%

Host Range of the Conjugative Transfer System of IncP-9 Naphthalene-Catabolic Plasmid NAH7 and Characterization of Its oriT Region and Relaxase

Kishida

Irie

Ohtsubo

et al. 2017

Appl Environ Microbiol

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NAH7 and pWW0 from gammaproteobacterial Pseudomonas putida strains are IncP-9 conjugative plasmids that carry the genes for degradation of naphthalene and toluene, respectively. Although such genes on these plasmids are wellcharacterized, experimental investigation of their conjugation systems remains at a primitive level. To clarify these conjugation systems, in this study, we investigated the NAH7-encoded conjugation system by (i) analyzing the origin of its conjugative transfer (oriT)-containing region and its relaxase, which specifically nicks within the oriT region for initiation of transfer, and (ii) comparing the conjugation systems between NAH7 and pWW0. The NAH7 oriT (oriT N ) region was located within a 430-bp fragment, and the strand-specific nicking (nic) site and its upstream sequences that were important for efficient conjugation in the oriT N region were identified. Unlike many other relaxases, the NAH7 relaxase exhibited unique features in its ability to catalyze, in a conjugation-independent manner, the site-specific intramolecular recombination between two copies of the oriT N region, between two copies of the pWW0 oriT (oriT W ) region (which is clearly different from the oriT N region), and between the oriT N and oriT W regions. The pWW0 relaxase, which is also clearly different from the NAH7 relaxase, was strongly suggested to have the ability to conjugatively and efficiently mobilize the oriT Ncontaining plasmid. Such a plasmid was, in the presence of the NAH7Δnic derivative, conjugatively transferable to alphaproteobacterial and betaproteobacterial strains in which the NAH7 replication machinery is nonfunctional, indicating that the NAH7 conjugation system has a broader host range than its replication system. IMPORTANCE Various studies have strongly suggested an important contribution of conjugative transfer of catabolic plasmids to the rapid and wide dissemination of the plasmid-loaded degradation genes to microbial populations. Degradation genes on such plasmids are often loaded on transposons, which can be inserted into the genomes of the recipient bacterial strains where the transferred plasmids cannot replicate. The aim was to advance detailed molecular knowledge of the determinants of host range for plasmids. This aim is expected to be easily and comprehensively achieved using an experimental strategy in which the oriT region is connected with a plasmid that has a broad host range of replication. Using such a strategy in this study, we showed that (i) the NAH7 oriT-relaxase system has unique properties that are significantly different from other well-studied systems and (ii) the host range of the NAH7 conjugation system is broader than previously thought.KEYWORDS Pseudomonas, conjugation, oriT, plasmid, relaxase C onjugative transfer of plasmids that carry various genetic traits contributes greatly to the rapid adaptation and evolution of host bacteria (1). The conjugative transfer of plasmids in Gram-negative bacteria consists of DNA transfer and replication (Dtr) and

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Plasmid Conjugation from Proteobacteria as Evidence for the Origin of Xenologous Genes in Cyanobacteria

Cited by 16 publications

References 62 publications

Identification of Xenologs and Their Characteristic Low Expression Levels in the Cyanobacterium Synechococcus elongatus

Identification of Xenologs and Their Characteristic Low Expression Levels in the Cyanobacterium Synechococcus elongatus

Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy

Host Range of the Conjugative Transfer System of IncP-9 Naphthalene-Catabolic Plasmid NAH7 and Characterization of Its oriT Region and Relaxase

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