scholarly journals Is the Evolution of Salmonella enterica subsp. enterica Linked to Restriction-Modification Systems?

mSystems ◽  
2016 ◽  
Vol 1 (3) ◽  
Author(s):  
Louise Roer ◽  
Rene S. Hendriksen ◽  
Pimlapas Leekitcharoenphon ◽  
Oksana Lukjancenko ◽  
Rolf Sommer Kaas ◽  
...  

ABSTRACT The evolution of bacterial pathogens, their plasticity and ability to rapidly change and adapt to new surroundings are crucial for understanding the epidemiology and public health. With the application of genomics, it became clear that horizontal gene transfer played a key role in evolution. To understand the evolution and diversification of pathogens, we need to understand the processes that drive the horizontal gene transfer. Restriction-modification systems are thought to cause rearrangements within the chromosome, as well as act as a barrier to horizontal gene transfer. However, here we show that the correlation between restriction-modification systems and evolution in other bacterial species does not apply to Salmonella enterica subsp. enterica. In summary, from this work, we conclude that other mechanisms might be involved in controlling and shaping the evolution of Salmonella enterica subsp. enterica. Salmonella enterica subsp. enterica bacteria are highly diverse foodborne pathogens that are subdivided into more than 1,500 serovars. The diversity is believed to result from mutational evolution, as well as intra- and interspecies recombination that potentially could be influenced by restriction-modification (RM) systems. The aim of this study was to investigate whether RM systems were linked to the evolution of Salmonella enterica subsp. enterica. The study included 221 Salmonella enterica genomes, of which 68 were de novo sequenced and 153 were public available genomes from ENA. The data set covered 97 different serovars of Salmonella enterica subsp. enterica and an additional five genomes from four other Salmonella subspecies as an outgroup for constructing the phylogenetic trees. The phylogenetic trees were constructed based on multiple alignment of core genes, as well as the presence or absence of pangenes. The topology of the trees was compared to the presence of RM systems, antimicrobial resistance (AMR) genes, Salmonella pathogenicity islands (SPIs), and plasmid replicons. We did not observe any correlation between evolution and the RM systems in S. enterica subsp. enterica. However, sublineage correlations and serovar-specific patterns were observed. Additionally, we conclude that plasmid replicons, SPIs, and AMR were all better correlated to serovars than to RM systems. This study suggests a limited influence of RM systems on the evolution of Salmonella enterica subsp. enterica, which could be due to the conjugational mode of horizontal gene transfer in Salmonella. Thus, we conclude that other factors must be involved in shaping the evolution of bacteria. IMPORTANCE The evolution of bacterial pathogens, their plasticity and ability to rapidly change and adapt to new surroundings are crucial for understanding the epidemiology and public health. With the application of genomics, it became clear that horizontal gene transfer played a key role in evolution. To understand the evolution and diversification of pathogens, we need to understand the processes that drive the horizontal gene transfer. Restriction-modification systems are thought to cause rearrangements within the chromosome, as well as act as a barrier to horizontal gene transfer. However, here we show that the correlation between restriction-modification systems and evolution in other bacterial species does not apply to Salmonella enterica subsp. enterica. In summary, from this work, we conclude that other mechanisms might be involved in controlling and shaping the evolution of Salmonella enterica subsp. enterica.

mBio ◽  
2012 ◽  
Vol 3 (5) ◽  
Author(s):  
Peter Jorth ◽  
Marvin Whiteley

ABSTRACTNatural transformation by competent bacteria is a primary means of horizontal gene transfer; however, evidence that competence drives bacterial diversity and evolution has remained elusive. To test this theory, we used a retrospective comparative genomic approach to analyze the evolutionary history ofAggregatibacter actinomycetemcomitans, a bacterial species with both competent and noncompetent sister strains. Through comparative genomic analyses, we reveal that competence is evolutionarily linked to genomic diversity and speciation. Competence loss occurs frequently during evolution and is followed by the loss of clustered regularly interspaced short palindromic repeats (CRISPRs), bacterial adaptive immune systems that protect against parasitic DNA. Relative to noncompetent strains, competent bacteria have larger genomes containing multiple rearrangements. In contrast, noncompetent bacterial genomes are extremely stable but paradoxically susceptible to infective DNA elements, which contribute to noncompetent strain genetic diversity. Moreover, incomplete noncompetent strain CRISPR immune systems are enriched for self-targeting elements, which suggests that the CRISPRs have been co-opted for bacterial gene regulation, similar to eukaryotic microRNAs derived from the antiviral RNA interference pathway.IMPORTANCEThe human microbiome is rich with thousands of diverse bacterial species. One mechanism driving this diversity is horizontal gene transfer by natural transformation, whereby naturally competent bacteria take up environmental DNA and incorporate new genes into their genomes. Competence is theorized to accelerate evolution; however, attempts to test this theory have proved difficult. Through genetic analyses of the human periodontal pathogenAggregatibacter actinomycetemcomitans, we have discovered an evolutionary connection between competence systems promoting gene acquisition and CRISPRs (clustered regularly interspaced short palindromic repeats), adaptive immune systems that protect bacteria against genetic parasites. We show that competentA. actinomycetemcomitansstrains have numerous redundant CRISPR immune systems, while noncompetent bacteria have lost their CRISPR immune systems because of inactivating mutations. Together, the evolutionary data linking the evolution of competence and CRISPRs reveals unique mechanisms promoting genetic heterogeneity and the rise of new bacterial species, providing insight into complex mechanisms underlying bacterial diversity in the human body.


2018 ◽  
Vol 62 (9) ◽  
Author(s):  
Eva Hong ◽  
Ala-Eddine Deghmane ◽  
Muhamed-Kheir Taha

ABSTRACT We report the detection in France of a beta-lactamase-producing invasive meningococcal isolate. Whole-genome sequencing of the isolate revealed a ROB-1-type beta-lactamase gene that is frequently encountered in Haemophilus influenzae, suggesting horizontal transfer between isolates of these bacterial species. Beta-lactamases are exceptional in meningococci, with no reports for more than 2 decades. This report is worrying, as the expansion of such isolates may jeopardize the effective treatment against invasive meningococcal disease.


2018 ◽  
Vol 84 (23) ◽  
Author(s):  
Ximin Zeng ◽  
Zuowei Wu ◽  
Qijing Zhang ◽  
Jun Lin

ABSTRACTConjugation is an important mechanism for horizontal gene transfer inCampylobacter jejuni, the leading cause of human bacterial gastroenteritis in developed countries. However, to date, the factors that significantly influence conjugation efficiency inCampylobacterspp. are still largely unknown. Given that multiple recombinant loci could independently occur within one recipient cell during natural transformation, the genetic materials from a high-frequency conjugation (HFC)C. jejunistrain may be cotransformed with a selection marker into a low-frequency conjugation (LFC) recipient strain, creating new HFC transformants suitable for the identification of conjugation factors using a comparative genomics approach. To test this, an erythromycin resistance selection marker was created in an HFCC. jejunistrain; subsequently, the DNA of this strain was naturally transformed into NCTC 11168, an LFCC. jejunistrain, leading to the isolation of NCTC 11168-derived HFC transformants. Whole-genome sequencing analysis and subsequent site-directed mutagenesis identified Cj1051c, a putative restriction-modification enzyme (akaCjeI) that could drastically reduce the conjugation efficiency of NCTC 11168 (>5,000-fold). Chromosomal complementation of three diverse HFCC. jejunistrains with CjeI also led to a dramatic reduction in conjugation efficiency (∼1,000-fold). The purified recombinant CjeI could effectively digest theEscherichia coli-derived shuttle vector pRY107. The endonuclease activity of CjeI was abolished upon short heat shock treatment at 50°C, which is consistent with our previous observation that heat shock enhanced conjugation efficiency inC. jejuni. Together, in this study, we successfully developed and utilized a unique cotransformation strategy to identify a restriction-modification enzyme that significantly influences conjugation efficiency inC. jejuni.IMPORTANCEConjugation is an important horizontal gene transfer mechanism contributing to the evolution of bacterial pathogenesis and antimicrobial resistance.Campylobacter jejuni, the leading foodborne bacterial organism, displays significant strain diversity due to horizontal gene transfer; however, the molecular components influencing conjugation efficiency inC. jejuniare still largely unknown. In this study, we developed a cotransformation strategy for comparative genomics analysis and successfully identified a restriction-modification enzyme that significantly influences conjugation efficiency inC. jejuni. The new cotransformation strategy developed in this study is also expected to be broadly applied in other naturally competent bacteria for functional comparative genomics research.


2020 ◽  
Vol 12 (4) ◽  
pp. 381-395
Author(s):  
Nilson Da Rocha Coimbra ◽  
Aristoteles Goes-Neto ◽  
Vasco Azevedo ◽  
Aïda Ouangraoua

Abstract Horizontal gene transfer is a common mechanism in Bacteria that has contributed to the genomic content of existing organisms. Traditional methods for estimating bacterial phylogeny, however, assume only vertical inheritance in the evolution of homologous genes, which may result in errors in the estimated phylogenies. We present a new method for estimating bacterial phylogeny that accounts for the presence of genes acquired by horizontal gene transfer between genomes. The method identifies and corrects putative transferred genes in gene families, before applying a gene tree-based summary method to estimate bacterial species trees. The method was applied to estimate the phylogeny of the order Corynebacteriales, which is the largest clade in the phylum Actinobacteria. We report a collection of 14 phylogenetic trees on 360 Corynebacteriales genomes. All estimated trees display each genus as a monophyletic clade. The trees also display several relationships proposed by past studies, as well as new relevant relationships between and within the main genera of Corynebacteriales: Corynebacterium, Mycobacterium, Nocardia, Rhodococcus, and Gordonia. An implementation of the method in Python is available on GitHub at https://github.com/UdeS-CoBIUS/EXECT (last accessed April 2, 2020).


Author(s):  
Erik Senneby ◽  
Björn Hallström ◽  
Magnus Rasmussen

Introduction. Streptococcus dysgalactiae subspecies equisimilis (SDSE) is becoming increasingly recognized as an important human pathogen. Recurrent bacteremia with SDSE has been described previously. Aim. The aims of the study were to establish the genetic relatedness of SDSE isolates with emm-type stG643 that had caused recurrent bacteraemia in three patients and to search for signs of horizontal gene transfer of the emm gene in a collection of SDSE stG643 genomes. Hypothesis. Recurring SDSE bacteremia is caused by the same clone in one patient. Methodology. Whole genome sequencing of 22 clinical SDSE stG643 isolates was performed, including three paired blood culture isolates and sixteen isolates from various sites. All assemblies were aligned to a reference assembly and SNPs were extracted. A total of 53 SDSE genomes were downloaded from GenBank. Two phylogenetic trees, including all 75 SDSE isolates, were created. One tree was based on the emm gene only and one tree was based on all variable positions in the genomes. Results. The genomes from the three pairs of SDSE isolates showed high sequence similarity (1–17 SNPs difference between the pairs), whereas the median SNP difference between the 22 isolates in our collection was 1694 (range 1–11257). The paired isolates were retrieved with 7–53 months between episodes. The 22 SDSE isolates from our collection formed a cluster in the phylogenetic tree based on the emm gene, while they were more scattered in the tree based on all variable positions. Conclusions. Our results show that the paired isolates were of the same clonal origin, which in turn supports carriage between bacteraemia episodes. The phylogenetic analysis indicates that horizontal gene transfer of the emm-gene between some of the SDSE isolates has occurred.


mBio ◽  
2011 ◽  
Vol 2 (3) ◽  
Author(s):  
William M. Shafer ◽  
Elizabeth A. Ohneck

ABSTRACTWhile horizontal gene transfer occurs frequently among bacterial species, evidence for the transfer of DNA from host to microbe is exceptionally rare. However, the recent report by Anderson and Seifert [mBio 2(1):e00005-11, 2011] provides evidence for such an event with the finding that 11% ofNeisseria gonorrhoeaestrains harbor a 685-bp sequence that is 98 to 100% identical to the human long interspersed nuclear element L1. While the function of this element in gonococci remains unclear, this finding significantly impacts our consideration of the coevolution of hosts and microbes, particularly that of humans and pathogens.


mBio ◽  
2011 ◽  
Vol 2 (2) ◽  
Author(s):  
Ana Babic ◽  
Melanie B. Berkmen ◽  
Catherine A. Lee ◽  
Alan D. Grossman

ABSTRACT Horizontal gene transfer contributes to evolution and the acquisition of new traits. In bacteria, horizontal gene transfer is often mediated by conjugative genetic elements that transfer directly from cell to cell. Integrative and conjugative elements (ICEs; also known as conjugative transposons) are mobile genetic elements that reside within a host genome but can excise to form a circle and transfer by conjugation to recipient cells. ICEs contribute to the spread of genes involved in pathogenesis, symbiosis, metabolism, and antibiotic resistance. Despite its importance, little is known about the mechanisms of conjugation in Gram-positive bacteria or how quickly or frequently transconjugants become donors. We visualized the transfer of the integrative and conjugative element ICEBs1 from a Bacillus subtilis donor to recipient cells in real time using fluorescence microscopy. We found that transfer of DNA from a donor to a recipient appeared to occur at a cell pole or along the lateral cell surface of either cell. Most importantly, we found that when acquired by 1 cell in a chain, ICEBs1 spread rapidly from cell to cell within the chain by additional sequential conjugation events. This intrachain conjugation is inherently more efficient than conjugation that is due to chance encounters between individual cells. Many bacterial species, including pathogenic, commensal, symbiotic, and nitrogen-fixing organisms, harbor ICEs and grow in chains, often as parts of microbial communities. It is likely that efficient intrachain spreading is a general feature of conjugative DNA transfer and serves to amplify the number of cells that acquire conjugative mobile genetic elements. IMPORTANCE Conjugative elements contribute to horizontal gene transfer and the acquisition of new traits. They are largely responsible for spreading antibiotic resistance in bacterial communities. To study the cell biology of conjugation, we visualized conjugative DNA transfer between Bacillus subtilis cells in real time using fluorescence microscopy. In contrast to previous predictions that transfer would occur preferentially from the donor cell pole, we found that transfer of DNA from a donor to a recipient appeared to occur at a cell pole or along the lateral cell surface of either cell. Most importantly, we found that when acquired by 1 cell in a chain, the conjugative DNA spread rapidly from cell to cell within the chain through sequential conjugation events. Since many bacterial species grow naturally in chains, this intrachain transfer is likely a common mechanism for accelerating the spread of conjugative elements within microbial communities.


2021 ◽  
Vol 7 (2) ◽  
Author(s):  
George H. Jones

Poly(A) polymerases (PAPs) and tRNA nucleotidyltransferases belong to a superfamily of nucleotidyltransferases and modify RNA 3′-ends. The product of the pcnB gene, PAP I, has been characterized in a few β-, γ- and δ- Proteobacteria . Using the PAP I signature sequence, putative PAPs were identified in bacterial species from the α- and ε- Proteobacteria and from four other bacterial phyla ( Firmicutes , Actinobacteria , Bacteroidetes and Aquificae ). Phylogenetic analysis, alien index and G+C content calculations strongly suggest that the PAPs in the species identified in this study arose by horizontal gene transfer from the β- and γ- Proteobacteria .


mSphere ◽  
2020 ◽  
Vol 5 (6) ◽  
Author(s):  
Roberto C. Molina-Quiroz ◽  
Triana N. Dalia ◽  
Andrew Camilli ◽  
Ankur B. Dalia ◽  
Cecilia A. Silva-Valenzuela

ABSTRACT Natural transformation is a broadly conserved mechanism of horizontal gene transfer (HGT) in bacteria that can shape their evolution through the acquisition of genes that promote virulence, antibiotic resistance, and other traits. Recent work has established that neighbor predation via type VI secretion systems, bacteriocins, and virulent phages plays an important role in promoting HGT. Here, we demonstrate that in chitin estuary microcosms, Vibrio cholerae K139 lysogens exhibit prophage-dependent neighbor predation of nonlysogens to enhance HGT. Through predation of nonlysogens, K139 lysogens also have a fitness advantage under these microcosm conditions. The ecological strategy revealed by our work provides a better understanding of the evolutionary mechanisms used by bacteria to adapt in their natural setting and contributes to our understanding of the selective pressures that may drive prophage maintenance in bacterial genomes. IMPORTANCE Prophages are nearly ubiquitous in bacterial species. These integrated phage elements have previously been implicated in horizontal gene transfer (HGT) largely through their ability to carry out transduction (generalized or specialized). Here, we show that prophage-encoded viral particles promote neighbor predation leading to enhanced HGT by natural transformation in the waterborne pathogen Vibrio cholerae. Our findings contribute to a comprehensive understanding of the dynamic forces involved in prophage maintenance which ultimately drive the evolution of naturally competent bacteria in their natural environment.


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