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19 pages, 1679 KiB

Open AccessArticle

Abundance, Diversity and Role of ICEs and IMEs in the Adaptation of Streptococcus salivarius to the Environment

by Julie Lao, Gérard Guédon, Thomas Lacroix, Florence Charron-Bourgoin, Virginie Libante, Valentin Loux, Hélène Chiapello, Sophie Payot and Nathalie Leblond-Bourget

Genes 2020, 11(9), 999; https://doi.org/10.3390/genes11090999 - 26 Aug 2020

Cited by 8 | Viewed by 2557

Abstract

Streptococcus salivarius is a significant contributor to the human oral, pharyngeal and gut microbiomes that contribute to the maintenance of health. The high genomic diversity observed in this species is mainly caused by horizontal gene transfer. This work aimed to evaluate the contribution [...] Read more.

Streptococcus salivarius is a significant contributor to the human oral, pharyngeal and gut microbiomes that contribute to the maintenance of health. The high genomic diversity observed in this species is mainly caused by horizontal gene transfer. This work aimed to evaluate the contribution of integrative and conjugative elements (ICEs) and integrative and mobilizable elements (IMEs) in S. salivarius genome diversity. For this purpose, we performed an in-depth analysis of 75 genomes of S. salivarius and searched for signature genes of conjugative and mobilizable elements. This analysis led to the retrieval of 69 ICEs, 165 IMEs and many decayed elements showing their high prevalence in S. salivarius genomes. The identification of almost all ICE and IME boundaries allowed the identification of the genes in which these elements are inserted. Furthermore, the exhaustive analysis of the adaptation genes carried by these elements showed that they encode numerous functions such as resistance to stress, to antibiotics or to toxic compounds, and numerous enzymes involved in diverse cellular metabolic pathways. These data support the idea that not only ICEs but also IMEs and decayed elements play an important role in S. salivarius adaptation to the environment. Full article

(This article belongs to the Special Issue Genomic Islands)

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15 pages, 2038 KiB

Open AccessArticle

Mobilization of IMEs Integrated in the oriT of ICEs Involves Their Own Relaxase Belonging to the Rep-Trans Family of Proteins

by Virginie Libante, Nazim Sarica, Abbas Mohamad Ali, Chloé Gapp, Anissa Oussalah, Gérard Guédon, Nathalie Leblond-Bourget and Sophie Payot

Genes 2020, 11(9), 1004; https://doi.org/10.3390/genes11091004 - 26 Aug 2020

Cited by 4 | Viewed by 3068

Abstract

Integrative mobilizable elements (IMEs) are widespread but very poorly studied integrated elements that can excise and hijack the transfer apparatus of co-resident conjugative elements to promote their own spreading. Sixty-four putative IMEs, harboring closely related mobilization and recombination modules, were found in 14 [...] Read more.

Integrative mobilizable elements (IMEs) are widespread but very poorly studied integrated elements that can excise and hijack the transfer apparatus of co-resident conjugative elements to promote their own spreading. Sixty-four putative IMEs, harboring closely related mobilization and recombination modules, were found in 14 Streptococcus species and in Staphylococcus aureus. Fifty-three are integrated into the origin of transfer (oriT) of a host integrative conjugative element (ICE), encoding a MobT relaxase and belonging to three distant families: ICESt3, Tn916, and ICE6013. The others are integrated into an unrelated IME or in chromosomal sites. After labeling by an antibiotic resistance gene, the conjugative transfer of one of these IMEs (named IME_oriTs) and its host ICE was measured. Although the IME is integrated in an ICE, it does not transfer as a part of the host ICE (no cis-mobilization). The IME excises and transfers separately from the ICE (without impacting its transfer rate) using its own relaxase, distantly related to all known MobT relaxases, and integrates in the oriT of the ICE after transfer. Overall, IME_oriTs use MobT-encoding ICEs both as hosts and as helpers for conjugative transfer. As half of them carry lsa(C), they actively participate in the dissemination of lincosamide–streptogramin A–pleuromutilin resistance among Firmicutes. Full article

(This article belongs to the Special Issue Genomic Islands)

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19 pages, 12605 KiB

Open AccessArticle

Insights into Mobile Genetic Elements of the Biocide-Degrading Bacterium Pseudomonas nitroreducens HBP-1

by Nicolas Carraro, Vladimir Sentchilo, Lenka Polák, Claire Bertelli and Jan Roelof van der Meer

Genes 2020, 11(8), 930; https://doi.org/10.3390/genes11080930 - 12 Aug 2020

Cited by 5 | Viewed by 3217

Abstract

The sewage sludge isolate Pseudomonas nitroreducens HBP-1 was the first bacterium known to completely degrade the fungicide 2-hydroxybiphenyl. PacBio and Illumina whole-genome sequencing revealed three circular DNA replicons: a chromosome and two plasmids. Plasmids were shown to code for putative adaptive functions such [...] Read more.

The sewage sludge isolate Pseudomonas nitroreducens HBP-1 was the first bacterium known to completely degrade the fungicide 2-hydroxybiphenyl. PacBio and Illumina whole-genome sequencing revealed three circular DNA replicons: a chromosome and two plasmids. Plasmids were shown to code for putative adaptive functions such as heavy metal resistance, but with unclarified ability for self-transfer. About one-tenth of strain HBP-1′s chromosomal genes are likely of recent horizontal influx, being part of genomic islands, prophages and integrative and conjugative elements (ICEs). P. nitroreducens carries two large ICEs with different functional specialization, but with homologous core structures to the well-known ICEclc of Pseudomonas knackmussii B13. The variable regions of ICEPni1 (96 kb) code for, among others, heavy metal resistances and formaldehyde detoxification, whereas those of ICEPni2 (171 kb) encodes complete meta-cleavage pathways for catabolism of 2-hydroxybiphenyl and salicylate, a protocatechuate pathway and peripheral enzymes for 4-hydroxybenzoate, ferulate, vanillin and vanillate transformation. Both ICEs transferred at frequencies of 10⁻⁶–10⁻⁸ per P. nitroreducens HBP-1 donor into Pseudomonas putida, where they integrated site specifically into tRNA^Gly-gene targets, as expected. Our study highlights the underlying determinants and mechanisms driving dissemination of adaptive properties allowing bacterial strains to cope with polluted environments. Full article

(This article belongs to the Special Issue Genomic Islands)

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12 pages, 2383 KiB

Open AccessArticle

ICEs Are the Main Reservoirs of the Ciprofloxacin-Modifying crpP Gene in Pseudomonas aeruginosa

by João Botelho, Filipa Grosso and Luísa Peixe

Genes 2020, 11(8), 889; https://doi.org/10.3390/genes11080889 - 04 Aug 2020

Cited by 11 | Viewed by 2963

Abstract

The ciprofloxacin-modifying crpP gene was recently identified in a plasmid isolated from a Pseudomonas aeruginosa clinical isolate. Homologues of this gene were also identified in Escherichia coli, Klebsiella pneumoniae and Acinetobacter baumannii. We set out to explore the mobile elements involved [...] Read more.

The ciprofloxacin-modifying crpP gene was recently identified in a plasmid isolated from a Pseudomonas aeruginosa clinical isolate. Homologues of this gene were also identified in Escherichia coli, Klebsiella pneumoniae and Acinetobacter baumannii. We set out to explore the mobile elements involved in the acquisition and spread of this gene in publicly available and complete genomes of Pseudomonas spp. All Pseudomonas complete genomes were downloaded from NCBI’s Refseq library and were inspected for the presence of the crpP gene. The mobile elements carrying this gene were further characterized. The crpP gene was identified only in P. aeruginosa, in more than half of the complete chromosomes (61.9%, n = 133/215) belonging to 52 sequence types, of which the high-risk clone ST111 was the most frequent. We identified 136 crpP-harboring integrative and conjugative elements (ICEs), with 93.4% belonging to the mating-pair formation G (MPF_G) family. The ICEs were integrated at the end of a tRNA^Lys gene and were all flanked by highly conserved 45-bp direct repeats. The crpP-carrying ICEs contain 26 core genes (2.2% of all 1193 genes found in all the ICEs together), which are present in 99% or more of the crpP-harboring ICEs. The most frequently encoded traits on these ICEs include replication, transcription, intracellular trafficking and cell motility. Our work suggests that ICEs are the main vectors promoting the dissemination of the ciprofloxacin-modifying crpP gene in P. aeruginosa. Full article

(This article belongs to the Special Issue Genomic Islands)

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9 pages, 405 KiB

Open AccessCommunication

Antibiotic Resistance Is Associated with Integrative and Conjugative Elements and Genomic Islands in Naturally Circulating Streptococcus pneumoniae Isolates from Adults in Liverpool, UK

by Elissavet Nikolaou, Alasdair T. M. Hubbard, João Botelho, Taylor A. M. Marschall, Daniela M. Ferreira and Adam P. Roberts

Genes 2020, 11(6), 625; https://doi.org/10.3390/genes11060625 - 06 Jun 2020

Cited by 7 | Viewed by 3686

Abstract

Pneumonia is the sixth largest cause of death in the UK. It is usually caused by Streptococcus pneumoniae, which healthy individuals can carry in their nose without symptoms of disease. Antimicrobial resistance further increases mortality and morbidity associated with pneumococcal infection, although [...] Read more.

Pneumonia is the sixth largest cause of death in the UK. It is usually caused by Streptococcus pneumoniae, which healthy individuals can carry in their nose without symptoms of disease. Antimicrobial resistance further increases mortality and morbidity associated with pneumococcal infection, although few studies have analysed resistance in naturally circulating pneumococcal isolates in adult populations. Here, we report on the resistome and associated mobile genetic elements within circulating pneumococcus isolated from adult volunteers enrolled in the experimental human pneumococcal colonisation (EHPC) research program at the Liverpool School of Tropical Medicine, UK. Pneumococcal isolates collected from 30 healthy asymptomatic adults who had volunteered to take part in clinical research were screened for antibiotic susceptibility to erythromycin and tetracycline, and whole-genome sequenced. The genetic context of resistance to one or both antibiotics in four isolates was characterised bioinformatically, and any association of the resistance genes with mobile genetic elements was determined. Tetracycline and macrolide resistance genes [tet(M), erm(B), mef(A), msr(D)] were detected on known Tn916-like integrative and conjugative elements, namely Tn6002 and Tn2010, and tet(32) was found for the first time in S. pneumoniae located on a novel 50 kb genomic island. The widespread use of pneumococcal conjugate vaccines impacts on serotype prevalence and transmission within the community. It is therefore important to continue to monitor antimicrobial resistance (AMR) genes present in both vaccine types and non-vaccine types in response to contemporary antimicrobial therapies and characterise the genetic context of acquired resistance genes to continually optimise antibiotic therapies. Full article

(This article belongs to the Special Issue Genomic Islands)

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12 pages, 1913 KiB

Open AccessArticle

Detection of a Novel, and Likely Ancestral, Tn916-Like Element from a Human Saliva Metagenomic Library

by Liam J. Reynolds, Muna F. Anjum and Adam P. Roberts

Genes 2020, 11(5), 548; https://doi.org/10.3390/genes11050548 - 14 May 2020

Cited by 6 | Viewed by 2851

Abstract

Tn916 is a conjugative transposon (CTn) and the first reported and most well characterised of the Tn916/Tn1545 family of CTns. Tn916-like elements have a characteristic modular structure and different members of this family have been identified based [...] Read more.

Tn916 is a conjugative transposon (CTn) and the first reported and most well characterised of the Tn916/Tn1545 family of CTns. Tn916-like elements have a characteristic modular structure and different members of this family have been identified based on similarities and variations in these modules. In addition to carrying genes encoding proteins required for their conjugation, Tn916-like elements also carry accessory, antimicrobial resistance genes; most commonly the tetracycline resistance gene, tet(M). Our study aimed to identify and characterise tetracycline resistance genes from the human saliva metagenome using a functional metagenomic approach. We identified a tetracycline-resistant clone, TT31, the sequencing of which revealed it to encode both tet(M) and tet(L). Comparison of the TT31 sequence with the accessory, regulation, and recombination modules of other Tn916-like elements indicated that a partial Tn916-like element encoding a truncated orf9 was cloned in TT31. Analysis indicated that a previous insertion within the truncated orf9 created the full length orf9 found in most Tn916-like transposons; demonstrating that orf9 is, in fact, the result of a gene fusion event. Thus, we hypothesise that the Tn916-like element cloned in TT31 likely represents an ancestral Tn916. Full article

(This article belongs to the Special Issue Genomic Islands)

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12 pages, 1223 KiB

Open AccessArticle

A Novel Arsenate-Resistant Determinant Associated with ICEpMERPH, a Member of the SXT/R391 Group of Mobile Genetic Elements

by Michael P. Ryan, Shannon Slattery and J. Tony Pembroke

Genes 2019, 10(12), 1048; https://doi.org/10.3390/genes10121048 - 16 Dec 2019

Cited by 6 | Viewed by 3222

Abstract

ICEpMERPH, the first integrative conjugative element (ICE) of the SXT/R391 family isolated in the United Kingdom and Europe, was analyzed to determine the nature of its adaptive functions, its genetic structure, and its homology to related elements normally found in pathogenic Vibrio or [...] Read more.

ICEpMERPH, the first integrative conjugative element (ICE) of the SXT/R391 family isolated in the United Kingdom and Europe, was analyzed to determine the nature of its adaptive functions, its genetic structure, and its homology to related elements normally found in pathogenic Vibrio or Proteus species. Whole genome sequencing of Escherichia coli (E. coli) isolate K802 (which contains the ICEpMERPH) was carried out using Illumina sequencing technology. ICEpMERPH has a size of 110 Kb and 112 putative open reading frames (ORFs). The “hotspot regions” of the element were found to contain putative restriction digestion systems, insertion sequences, and heavy metal resistance genes that encoded resistance to mercury, as previously reported, but also surprisingly to arsenate. A novel arsenate resistance system was identified in hotspot 4 of the element, unrelated to other SXT/R391 elements. This arsenate resistance system was potentially linked to two genes: orf69, encoding an organoarsenical efflux major facilitator superfamily (MFS) transporter-like protein related to ArsJ, and orf70, encoding nicotinamide adenine dinucleotide (NAD)-dependent glyceraldehyde-3-phosphate dehydrogenase. Phenotypic analysis using isogenic strains of Escherichia coli strain AB1157 with and without the ICEpMERPH revealed resistance to low levels of arsenate in the range of 1–5 mM. This novel, low-level resistance may have an important adaptive function in polluted environments, which often contain low levels of arsenate contamination. A bioinformatic analysis on the novel determinant and the phylogeny of ICEpMERPH was presented. Full article

(This article belongs to the Special Issue Genomic Islands)

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Review

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16 pages, 2966 KiB

Open AccessReview

Genomic Islands in Mycoplasmas

by Christine Citti, Eric Baranowski, Emilie Dordet-Frisoni, Marion Faucher and Laurent-Xavier Nouvel

Genes 2020, 11(8), 836; https://doi.org/10.3390/genes11080836 - 22 Jul 2020

Cited by 18 | Viewed by 3824

Abstract

Bacteria of the Mycoplasma genus are characterized by the lack of a cell-wall, the use of UGA as tryptophan codon instead of a universal stop, and their simplified metabolic pathways. Most of these features are due to the small-size and limited-content of their [...] Read more.

Bacteria of the Mycoplasma genus are characterized by the lack of a cell-wall, the use of UGA as tryptophan codon instead of a universal stop, and their simplified metabolic pathways. Most of these features are due to the small-size and limited-content of their genomes (580–1840 Kbp; 482–2050 CDS). Yet, the Mycoplasma genus encompasses over 200 species living in close contact with a wide range of animal hosts and man. These include pathogens, pathobionts, or commensals that have retained the full capacity to synthesize DNA, RNA, and all proteins required to sustain a parasitic life-style, with most being able to grow under laboratory conditions without host cells. Over the last 10 years, comparative genome analyses of multiple species and strains unveiled some of the dynamics of mycoplasma genomes. This review summarizes our current knowledge of genomic islands (GIs) found in mycoplasmas, with a focus on pathogenicity islands, integrative and conjugative elements (ICEs), and prophages. Here, we discuss how GIs contribute to the dynamics of mycoplasma genomes and how they participate in the evolution of these minimal organisms. Full article

(This article belongs to the Special Issue Genomic Islands)

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18 pages, 1541 KiB

Open AccessReview

Horizontally Acquired Homologs of Xenogeneic Silencers: Modulators of Gene Expression Encoded by Plasmids, Phages and Genomic Islands

by Alejandro Piña-Iturbe, Isidora D. Suazo, Guillermo Hoppe-Elsholz, Diego Ulloa-Allendes, Pablo A. González, Alexis M. Kalergis and Susan M. Bueno

Genes 2020, 11(2), 142; https://doi.org/10.3390/genes11020142 - 29 Jan 2020

Cited by 12 | Viewed by 3537

Abstract

Acquisition of mobile elements by horizontal gene transfer can play a major role in bacterial adaptation and genome evolution by providing traits that contribute to bacterial fitness. However, gaining foreign DNA can also impose significant fitness costs to the host bacteria and can [...] Read more.

Acquisition of mobile elements by horizontal gene transfer can play a major role in bacterial adaptation and genome evolution by providing traits that contribute to bacterial fitness. However, gaining foreign DNA can also impose significant fitness costs to the host bacteria and can even produce detrimental effects. The efficiency of horizontal acquisition of DNA is thought to be improved by the activity of xenogeneic silencers. These molecules are a functionally related group of proteins that possess affinity for the acquired DNA. Binding of xenogeneic silencers suppresses the otherwise uncontrolled expression of genes from the newly acquired nucleic acid, facilitating their integration to the bacterial regulatory networks. Even when the genes encoding for xenogeneic silencers are part of the core genome, homologs encoded by horizontally acquired elements have also been identified and studied. In this article, we discuss the current knowledge about horizontally acquired xenogeneic silencer homologs, focusing on those encoded by genomic islands, highlighting their distribution and the major traits that allow these proteins to become part of the host regulatory networks. Full article

(This article belongs to the Special Issue Genomic Islands)

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