Discovery of integrons in Archaea: Platforms for cross-domain gene transfer

Ghaly, Timothy M.; Tetu, Sasha G.; Penesyan, Anahit; Qi, Qin; Rajabal, Vaheesan; Gillings, Michael R.

doi:10.1126/sciadv.abq6376

Cited by 21 publications

(14 citation statements)

References 83 publications

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“…Two adjacent attC sites were selected from each phage for their ability to integrate into attI1 ( Table 2 ). Using a previously described conjugation-based attC x attI1 recombination assay ( Bouvier et al, 2005 ; Nivina et al, 2020 ; Ghaly et al, 2022b ), we showed that gene cassette insertion can take place following the transfer of single-stranded suicide vector DNA with phage-borne attC sites (bottom strands) into an intI1 -expressing E . coli recipient strain that also harbours an attI1 site ( Figure 3A ).…”

Section: Resultsmentioning

confidence: 99%

“…The attC donor strains were then isolated on LB agar selective media containing kanamycin (Km) and diaminopimelic acid (DAP). To generate attC donor plasmids that deliver the top strands of the respective attC sites, the same pairs of overlapping long primers were annealed and ligated to the Xba I/ Bam HI restriction sites of the pJP5603rev vector with its oriT in an inverted orientation relative to that of the pJP5603 parental vector ( Ghaly et al, 2022b ).…”

Section: Methodsmentioning

confidence: 99%

“…An L-arabinose-inducible, intI1 -expressing E . coli recipient strain from a previous study ( Ghaly et al, 2022b ; UB5201 + pBAD24:: intI1 + pACYC184:: attI1 ; carbenicillin (Cb) and chloramphenicol (Cm) resistant) was individually filter-mated in DAP-supplemented LB broth with one of the seven attC donor strains (Km resistant; attC sequences shown in Supplementary Table S3 ). IntI1 expression was induced using L-arabinose at 2 mg/ml or suppressed with D-glucose at 10 mg/ml in the negative control set.…”

Section: Methodsmentioning

confidence: 99%

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Identification of integrons and gene cassette-associated recombination sites in bacteriophage genomes

Rajabal

Ghaly

et al. 2023

Front. Microbiol.

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Bacteriophages are versatile mobile genetic elements that play key roles in driving the evolution of their bacterial hosts through horizontal gene transfer. Phages co-evolve with their bacterial hosts and have plastic genomes with extensive mosaicism. In this study, we present bioinformatic and experimental evidence that temperate and virulent (lytic) phages carry integrons, including integron-integrase genes, attC/attI recombination sites and gene cassettes. Integrons are normally found in Bacteria, where they capture, express and re-arrange mobile gene cassettes via integron-integrase activity. We demonstrate experimentally that a panel of attC sites carried in virulent phage can be recognized by the bacterial class 1 integron-integrase (IntI1) and then integrated into the paradigmatic attI1 recombination site using an attC x attI recombination assay. With an increasing number of phage genomes projected to become available, more phage-associated integrons and their components will likely be identified in the future. The discovery of integron components in bacteriophages establishes a new route for lateral transfer of these elements and their cargo genes between bacterial host cells.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Identification of integrons and gene cassette-associated recombination sites in bacteriophage genomes

Rajabal

Ghaly

et al. 2023

Front. Microbiol.

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“…Obligatory association of Psyn with co-cultured bacteria might have favored the gene exchanges, possibly influencing microbial population structure under natural conditions 46 . Several different archaeal molecular mechanisms facilitating cross-domain DNA transfer, including integrons 47 ,have been described 48 , thus providing plausible means for HGT between Bacteria and Asgard. Finally, frequent HGTs between Psyn and different bacterial species might partially explain the apparent chimeric profiles of Asgard genomes 49 , which seemingly result from the frequent mixing of ancestral archaeal genes with laterally inherited bacterial ones.…”

Section: Discussionmentioning

confidence: 99%

Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya

et al. 2023

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Asgard archaea include the closest known archaeal relatives of eukaryotes. Here, we investigate the evolution and function of Asgard thymidylate synthases and other folate-dependent enzymes required for the biosynthesis of DNA, RNA, amino acids and vitamins, as well as syntrophic amino acid utilization. Phylogenies of Asgard folate-dependent enzymes are consistent with their horizontal transmission from various bacterial groups. We experimentally validate the functionality of thymidylate synthase ThyX of the cultured ‘Candidatus Prometheoarchaeum syntrophicum’. The enzyme efficiently uses bacterial-like folates and is inhibited by mycobacterial ThyX inhibitors, even though the majority of experimentally tested archaea are known to use carbon carriers distinct from bacterial folates. Our phylogenetic analyses suggest that the eukaryotic thymidylate synthase, required for de novo DNA synthesis, is not closely related to archaeal enzymes and might have been transferred from bacteria to protoeukaryotes during eukaryogenesis. Altogether, our study suggests that the capacity of eukaryotic cells to duplicate their genetic material is a sum of archaeal (replisome) and bacterial (thymidylate synthase) characteristics. We also propose that recent prevalent lateral gene transfer from bacteria has markedly shaped the metabolism of Asgard archaea.

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“…Indeed, the true extent of integron distribution is likely much broader, with recent discoveries showing that integrons also occur in archaea. This suggests that they are evolutionarily ancient elements that could play a role in cross‐domain gene transfer (Ghaly, Tetu, et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Exploring the role of mobile genetic elements in shaping plant–bacterial interactions for sustainable agriculture and ecosystem health

Rajabal,

Ghaly,

Egidi

et al. 2023

Plants People Planet

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Societal Impact StatementPlants and bacteria interact in complex ways that are crucial to the health and productivity of native vegetation and croplands. While the range of characterised plant‐beneficial bacterial traits continues to grow, key questions remain regarding the distribution and mobility of genes associated with these traits. This work explores the diversity of mobile genetic elements carried by bacteria associated with plant root surfaces, assessing their capacity to help shape plant–bacterial interactions. The significance of this work lies in the potential to contribute to new strategies for enhancing plant health, promoting sustainable agriculture and managing plant diseases in an era when we must respond to environmental change.Summary Integrons are gene capture and expression systems that contribute to bacterial adaptation. Integron research has mainly focused on the role that these elements play in spreading antimicrobial resistance. However, their contribution to niche adaptation is potentially much broader because integrons can sample the vast repertoire of diverse functions encoded by integron gene cassettes. Integrons and gene cassettes have been identified in many bacterial lineages residing in soil and water across varied ecosystems, but there has been little investigation of integrons in plant‐associated bacteria. Bacteria and plants have complex, dynamic relationships that influence plant health and productivity. To investigate whether integrons contribute to adaptative processes in plant microbiomes, we examined gene cassette and microbial taxonomic profiles in rhizoplanes of four important crop species grown under controlled glasshouse conditions. We identified 38,546 unique gene cassettes, including elements carrying genes associated with antibiotic resistance, type II toxin–antitoxin systems and genes with putative functions associated with plant growth promotion, along with a larger set encoding genes of unknown functions. Rhizoplane microbiomes of different plant species showed more similarity in their community composition profiles than in their gene cassette profiles, with complex and distinct suites of gene cassettes associated with each plant species, suggesting that gene cassettes might have a role in specific plant–bacterial interactions. We show that rhizoplane microbiomes carry diverse integron gene cassettes that could play a role in establishing and maintaining rhizoplane communities.

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Discovery of integrons in Archaea: Platforms for cross-domain gene transfer

Cited by 21 publications

References 83 publications

Identification of integrons and gene cassette-associated recombination sites in bacteriophage genomes

Identification of integrons and gene cassette-associated recombination sites in bacteriophage genomes

Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya

Exploring the role of mobile genetic elements in shaping plant–bacterial interactions for sustainable agriculture and ecosystem health

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