1887

Abstract

Linear plasmids are extrachromosomal DNA elements that have been found in a small number of bacterial species. To date, the only linear plasmids described in the family belong to , first found in Typhi. Here, we describe a collection of 12 isolates of the species complex in which we identified linear plasmids. Screening of assembly graphs assembled from public read sets identified linear plasmid structures in a further 13 . species complex genomes. We used these 25 linear plasmid sequences to query all bacterial genome assemblies in the National Center for Biotechnology Information database, and discovered an additional 61 linear plasmid sequences in a variety of species. Gene content analysis divided these plasmids into five distinct phylogroups, with very few genes shared across more than two phylogroups. The majority of linear plasmid-encoded genes are of unknown function; however, each phylogroup carried its own unique toxin–antitoxin system and genes with homology to those encoding the ParAB plasmid stability system. Passage of the 12 linear plasmid-carrying isolates in our collection (which include representatives of all five phylogroups) indicated that these linear plasmids can be stably maintained, and our data suggest they can transmit between strains (including members of globally disseminated multidrug-resistant clones) and also between diverse species. The linear plasmid sequences, and representative isolates harbouring them, are made available as a resource to facilitate future studies on the evolution and function of these novel plasmids.

Funding
This study was supported by the:
  • Bill and Melinda Gates Foundation (Award OPP1175797)
    • Principle Award Recipient: KathrynE Holt
  • Sylvia and Charles Viertel Charitable Foundation (Award Senior Medical Research Fellowship)
    • Principle Award Recipient: KathrynE Holt
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000807
2022-04-13
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/4/mgen000807.html?itemId=/content/journal/mgen/10.1099/mgen.0.000807&mimeType=html&fmt=ahah

References

  1. Hayakawa T, Tanaka T, Sakaguchi K, Otake N, Yonehara H. A linear plasmid-like DNA in Streptomyces sp. producing lankacidin group antibiotics. J Gen Appl Microbiol 1979; 25:255–260 [View Article]
    [Google Scholar]
  2. Plasterk RHA, Simon MI, Barbour AG. Transposition of structural genes to an expression sequence on a linear plasmid causes antigenic variation in the bacterium Borrelia hermsii. Nature 1985; 318:257–263 [View Article] [PubMed]
    [Google Scholar]
  3. Meinhardt F, Schaffrath R, Larsen M. Microbial linear plasmids. Appl Microbiol Biotechnol 1997; 47:329–336 [View Article] [PubMed]
    [Google Scholar]
  4. Boumasmoud M, Haunreiter VD, Schweizer TA, Meyer L, Chakrakodi B et al. Genomic surveillance of vancomycin-resistant Enterococcus faecium reveals spread of a linear plasmid conferring a nutrient utilization advantage. bioRxiv 2021442932 [View Article]
    [Google Scholar]
  5. Baker S, Hardy J, Sanderson KE, Quail M, Goodhead I et al. A novel linear plasmid mediates flagellar variation in Salmonella Typhi. PLoS Pathog 2007; 3:e59 [View Article] [PubMed]
    [Google Scholar]
  6. Casjens SR, Gilcrease EB, Huang WM, Bunny KL, Pedulla ML et al. The pKO2 linear plasmid prophage of Klebsiella oxytoca. J Bacteriol 2004; 186:1818–1832 [View Article] [PubMed]
    [Google Scholar]
  7. Ravin V, Ravin N, Casjens S, Ford ME, Hatfull GF et al. Genomic sequence and analysis of the atypical temperate bacteriophage N15. J Mol Biol 2000; 299:53–73 [View Article] [PubMed]
    [Google Scholar]
  8. Hertwig S, Klein I, Lurz R, Lanka E, Appel B. PY54, a linear plasmid prophage of Yersinia enterocolitica with covalently closed ends. Mol Microbiol 2003; 48:989–1003 [View Article] [PubMed]
    [Google Scholar]
  9. Lucyshyn D, Huang SH, Kobryn K. Spring loading a pre-cleavage intermediate for hairpin telomere formation. Nucleic Acids Res 2015; 43:6062–6074 [View Article] [PubMed]
    [Google Scholar]
  10. Yang C-C, Tseng S-M, Chen CW. Telomere-associated proteins add deoxynucleotides to terminal proteins during replication of the telomeres of linear chromosomes and plasmids in Streptomyces. Nucleic Acids Res 2015; 43:6373–6383 [View Article] [PubMed]
    [Google Scholar]
  11. Robertson J, Lin J, Wren-Hedgus A, Arya G, Carrillo C et al. Development of a multi-locus typing scheme for an Enterobacteriaceae linear plasmid that mediates inter-species transfer of flagella. PLoS One 2019; 14:e0218638 [View Article] [PubMed]
    [Google Scholar]
  12. Gorrie CL, Mirceta M, Wick RR, Edwards DJ, Thomson NR et al. Gastrointestinal carriage is a major reservoir of K. pneumoniae infection in intensive care patients. Clin Infect Dis 2017; 65:208–215 [View Article] [PubMed]
    [Google Scholar]
  13. Gorrie CL, Mirceta M, Wick RR, Judd LM, Wyres KL et al. Antimicrobial-resistant Klebsiella pneumoniae carriage and infection in specialized geriatric care wards linked to acquisition in the referring hospital. Clin Infect Dis 2018; 67:161–170 [View Article] [PubMed]
    [Google Scholar]
  14. Bueno MFC, Francisco GR, O’Hara JA, de Oliveira Garcia D, Doi Y. Coproduction of 16S rRNA methyltransferase RmtD or RmtG with KPC-2 and CTX-M group extended-spectrum β-lactamases in Klebsiella pneumoniae. Antimicrob Agents Chemother 2013; 57:2397–2400 [View Article] [PubMed]
    [Google Scholar]
  15. Cerdeira L, Fernandes MR, Francisco GR, Bueno MFC, Ienne S et al. Draft genome sequence of a hospital-associated clone of Klebsiella pneumoniae ST340/CC258 coproducing RmtG and KPC-2 isolated from a pediatric patient. Genome Announc 2016; 4:e01130-16 [View Article] [PubMed]
    [Google Scholar]
  16. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  17. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2019btz848 [View Article] [PubMed]
    [Google Scholar]
  18. Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing. Microb Genom 2017; 3:e000132 [View Article] [PubMed]
    [Google Scholar]
  19. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
    [Google Scholar]
  20. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  21. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 2020; 21:180 [View Article] [PubMed]
    [Google Scholar]
  22. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article] [PubMed]
    [Google Scholar]
  23. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: Rapid Annotations using Subsystems Technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
    [Google Scholar]
  24. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 2014; 42:D206–D214 [View Article] [PubMed]
    [Google Scholar]
  25. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article] [PubMed]
    [Google Scholar]
  26. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011; 39:W29–W37 [View Article] [PubMed]
    [Google Scholar]
  27. Xie Y, Wei Y, Shen Y, Li X, Zhou H et al. TADB 2.0: an updated database of bacterial type II toxin–antitoxin loci. Nucleic Acids Res 2018; 46:D749–D753 [View Article] [PubMed]
    [Google Scholar]
  28. Akarsu H, Bordes P, Mansour M, Bigot D-J, Genevaux P et al. TASmania: a bacterial Toxin-Antitoxin Systems database. PLoS Comput Biol 2019; 15:e1006946 [View Article] [PubMed]
    [Google Scholar]
  29. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
    [Google Scholar]
  30. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet 2000; 16:276–277 [View Article] [PubMed]
    [Google Scholar]
  31. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article] [PubMed]
    [Google Scholar]
  32. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article] [PubMed]
    [Google Scholar]
  33. Wick RR, Judd LM, Wyres KL, Holt KE. Recovery of small plasmid sequences via Oxford Nanopore sequencing. Microb Genom 2021; 7:e000631 [View Article] [PubMed]
    [Google Scholar]
  34. Fraikin N, Goormaghtigh F, Van Melderen L. Type II toxin-antitoxin systems: evolution and revolutions. J Bacteriol 2020; 202:e00763-19 [View Article] [PubMed]
    [Google Scholar]
  35. Roberts MAJ, Wadhams GH, Hadfield KA, Tickner S, Armitage JP. ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes. Proc Natl Acad Sci USA 2012; 109:6698–6703 [View Article] [PubMed]
    [Google Scholar]
  36. Fitzgerald S, Kary SC, Alshabib EY, MacKenzie KD, Stoebel DM et al. Redefining the H-NS protein family: a diversity of specialized core and accessory forms exhibit hierarchical transcriptional network integration. Nucleic Acids Res 2020; 48:10184–10198 [View Article] [PubMed]
    [Google Scholar]
  37. Ishihama A, Shimada T. Hierarchy of transcription factor network in Escherichia coli K-12: H-NS-mediated silencing and anti-silencing by global regulators. FEMS Microbiol Rev 2021; 45:fuab032 [View Article] [PubMed]
    [Google Scholar]
  38. Ares MA, Fernández-Vázquez JL, Rosales-Reyes R, Jarillo-Quijada MD, von Bargen K et al. H-NS nucleoid protein controls virulence features of Klebsiella pneumoniae by regulating the expression of type 3 pili and the capsule polysaccharide. Front Cell Infect Microbiol 2016; 6:13 [View Article] [PubMed]
    [Google Scholar]
  39. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H et al. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 2006; 313:236–238 [View Article] [PubMed]
    [Google Scholar]
  40. Atlung T, Ingmer H. H‐NS: a modulator of environmentally regulated gene expression. Mol Microbiol 1997; 24:7–17 [View Article] [PubMed]
    [Google Scholar]
  41. Campanaro S, Treu L, Rodriguez-R LM, Kovalovszki A, Ziels RM et al. New insights from the biogas microbiome by comprehensive genome-resolved metagenomics of nearly 1600 species originating from multiple anaerobic digesters. Biotechnol Biofuels 2020; 13:25 [View Article] [PubMed]
    [Google Scholar]
  42. Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2017; 2:1533–1542 [View Article] [PubMed]
    [Google Scholar]
  43. Stoesser N, Batty EM, Eyre DW, Morgan M, Wyllie DH et al. Predicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence data. J Antimicrob Chemother 2013; 68:2234–2244 [View Article] [PubMed]
    [Google Scholar]
  44. Smit PW, Stoesser N, Pol S, van Kleef E, Oonsivilai M et al. Transmission dynamics of hyper-endemic multi-drug resistant Klebsiella pneumoniae in a Southeast Asian neonatal unit: a longitudinal study with whole genome sequencing. Front Microbiol 2018; 9:1197 [View Article] [PubMed]
    [Google Scholar]
  45. Davis GS, Waits K, Nordstrom L, Weaver B, Aziz M et al. Intermingled Klebsiella pneumoniae populations between retail meats and human urinary tract infections. Clin Infect Dis 2015; 61:892–899 [View Article] [PubMed]
    [Google Scholar]
  46. Henson SP, Boinett CJ, Ellington MJ, Kagia N, Mwarumba S et al. Molecular epidemiology of Klebsiella pneumoniae invasive infections over a decade at Kilifi County Hospital in Kenya. Int J Med Microbiol 2017; 307:422–429 [View Article] [PubMed]
    [Google Scholar]
  47. Moradigaravand D, Martin V, Peacock SJ, Parkhill J. Evolution and epidemiology of multidrug-resistant Klebsiella pneumoniae in the United Kingdom and Ireland. mBio 2017; 8:e01976-16 [View Article] [PubMed]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.000807
Loading
/content/journal/mgen/10.1099/mgen.0.000807
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error