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High Diversity and Variability of Pipolins Among a Wide Range Of bioRxiv preprint doi: https://doi.org/10.1101/2020.04.24.059261; this version posted April 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 2 High diversity and variability of pipolins among a wide range of 3 pathogenic Escherichia coli strains 4 5 Saskia-Camille Flament-Simon1*, María de Toro2*, Liubov Chuprikova4*, Miguel 6 Blanco1, Juan Moreno-González3, Margarita Salas3‡, Jorge Blanco1, and 7 Modesto Redrejo-Rodríguez3,4# 8 9 1 Laboratorio de Referencia de E. coli (LREC), Departamento de Microbiología y Parasitología, 10 Facultad de Veterinaria, Universidad de Santiago de Compostela (USC), Lugo, 27002,Spain. 11 12 2 Plataforma de Genómica y Bioinformática, CIBIR (Centro de Investigación Biomédica de La 13 Rioja), Logroño, 26006 La Rioja, Spain. 14 15 3 Centro de Biología Molecular Severo Ochoa (Consejo Superior de Investigaciones Científicas- 16 Universidad Autónoma de Madrid), 28049, Madrid, Spain. 17 18 4 Departamento de Bioquímica, Universidad Autónoma de Madrid (UAM), Instituto de 19 Investigaciones Biomédicas "Alberto Sols" CSIC-UAM, 28029, Madrid, Spain. 20 21 22 *Equal contribution 23 ‡Deceased 24 #Correspondence to [email protected] 25 26 27 4 Figures + 2 Tables 28 7 Supplementary Figures + 3 Supplementary Tables 29 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.24.059261; this version posted April 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 30 Abstract 31 32 Self-synthesizing transposons are integrative mobile genetic elements (MGEs) that 33 encode their own B-family DNA polymerase (PolB). Discovered a few years ago, they 34 are proposed as key players in the evolution of several groups of DNA viruses and 35 virus-host interaction machinery. Pipolins are the most recent addition to the group, are 36 integrated in the genomes of bacteria from diverse phyla and also present as circular 37 plasmids in mitochondria. Remarkably, pipolins-encoded PolBs are proficient DNA 38 polymerases endowed with DNA priming capacity, hence the name, primer- 39 independent PolB (piPolB). 40 We have now surveyed the presence of pipolins in a collection of 2238 human and 41 animal pathogenic Escherichia coli strains and found that, although detected in only 25 42 new isolates (1.1%), they are present in E. coli strains from a wide variety of 43 pathotypes, serotypes, phylogenetic groups and sequence types. Overall, the 44 pangenome of strains carrying pipolins is highly diverse, despite the fact that a 45 considerable number of strains belongs to only three clonal complexes (CC10, CC23 46 and CC32). Comparative analysis with a set of 67 additional pipolin-harboring strains 47 from GenBank further confirmed these results. The genetic structure of pipolins shows 48 great flexibility and variability, with the piPolB gene and the attachment sites being the 49 only common features. Most pipolins contain one or more recombinases that would be 50 involved in excision/integration of the element in the same conserved tRNA gene. This 51 mobilization mechanism might explain the apparent incompatibility of pipolins with 52 other integrative MGEs such as integrons. 53 In addition, analysis of cophylogeny between pipolins and pipolin-harboring strains 54 showed a lack of congruence between several pipolins and their host strains, in 55 agreement with horizontal transfer between hosts. Overall, these results indicate that 56 pipolins can serve as a vehicle for genetic transfer among circulating E. coli and 57 possibly also among other pathogenic bacteria. 58 59 296 words 60 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.24.059261; this version posted April 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 61 Introduction 62 63 Mobile genetic elements (MGE), comprising bacteriophages, transposons, plasmids, 64 and insertion sequences, contribute to the great plasticity of the bacterial genome, 65 resulting in an extremely large pangenomes that, in the case of Escherichia coli, can 66 amount to more than 16,000 genes [1]. Thus, MGEs dynamics is the main source of 67 horizontal gene transfer, which leads to the spread of antimicrobial resistance (AR) 68 among both E. coli and other commensals, thereby enlarging the spectrum of 69 resistance (the resistome) among circulating strains [2]. 70 Pipolins constitute a recently reported new group of integrative MGEs widespread 71 among diverse bacterial phyla and also identified in mitochondria as circular plasmids 72 [3]. The hallmark feature of the pipolins is a gene encoding for a replicative family B 73 DNA polymerases (PolB) with an intrinsic de novo primer synthesis capacity, called 74 primer-independent PolBs (piPolBs), hence their name (piPolB-encoding elements). 75 Preliminary phylogenetic analyses indicated that piPolBs would form a third major 76 branch of PolB, besides the protein-primed PolBs (pPolBs), found in a wide range of 77 viruses and plasmids, and RNA-primed PolBs (rPolBs), which are the principal 78 replicative enzymes of archaea and eukaryotes, some archaea and many dsDNA 79 viruses [3]. 80 Because of the fact that pipolins encode the major protein required for their replication 81 (i.e., piPolB), they are included in the proposed class of self-synthesizing (or self- 82 replicating) MGEs, which also includes two other superfamilies of elements integrated 83 in various cellular genomes [4]. The first superfamily comprises eukaryotic virus-like 84 transposable elements, called Polintons (also known as Mavericks), which besides a 85 putative pPolB, encode retrovirus-like integrases and a set of proteins hypothesized to 86 be involved in the formation of viral particles [5-7]. The second superfamily of pPolB- 87 encoding elements, denoted as casposons, is present in a wide range of archaea and 88 also in a few bacteria [8]. Similar to the aforementioned self-replicating MGEs, most 89 pipolins are integrated within bacterial chromosomes, although they are also 90 occasionally detected as episomal plasmids. However, unlike polintons and 91 casposons, the integrated pipolins encode for one or more integrases of the tyrosine 92 recombinase superfamily, which could be responsible for pipolin excision and/or 93 integration [3]. 94 The widespread and patchy distribution of pipolins among bacteria is in agreement with 95 an ancient origin and horizontal dispersal of this MGE group. However, pipolins from 96 the same or related species seem closely related, as was the case for pipolins from E. 97 coli [3]. The great majority of pathogenic E. coli strains encode for virulence-associated 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.24.059261; this version posted April 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 98 cassettes and antibiotic resistance genes, which are usually carried by MGEs, such as 99 pathogenicity islands (PAIs), plasmids, integrons, etc [9-11]. However, the annotation 100 of pipolins from E. coli as well as from proteobacteria did not lead to the identification of 101 any antibiotic resistance genes or virulence factors [3]. 102 Therefore, whereas reported evidence of mobility of polintons and casposons is limited 103 and based on metagenomic data [12], pipolins provide the opportunity to analyze the 104 occurrence, diversity, and dynamics of self-replicative MGEs in well-characterized 105 commensal and pathogenic bacteria, not only in genomic or metagenomics data, but 106 also in circulating field isolates and pathogenic variants. In this work, we surveyed the 107 presence of pipolins in a wide collection of pathogenic strains from the Spanish E. coli 108 reference laboratory (LREC). We found that pipolins, although not very abundant, are 109 widespread among a great variety of human and animal strains belonging to different 110 pathotypes, serotypes and sequence types (STs). 111 Whole-genome sequencing of the new pipolin-harboring E. coli strains allowed us to 112 characterize in detail the pipolins’ hosts and also the genetic structure and phylogeny 113 of pipolins. Most pipolins contain att-like terminal direct repeats and they are integrated 114 in the same tRNA gene. Nevertheless, they encode a great diversity of proteins, many 115 of which are orphans with unpredictable function. The comparison of the new strains 116 from LREC dataset with a number of detected pathogenic E. coli pipolin-harboring 117 strains from the NCBI GenBank database further confirmed our results. Finally, 118 pangenome and cophylogeny analyses among pipolins and host strains, demonstrated 119 that, except for strains from the same clonal complex, there is an overall lack of 120 phylogenetic congruence between pipolins and host strains. Therefore, our results 121 support that pipolins are a novel group of active mobile elements that might serve as a 122 platform for horizontal gene transference among diverse pathogenic bacteria. 123 124 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.24.059261; this version posted April 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 125 RESULTS AND DISCUSSION 126 127 Limited prevalence of pipolins among E.
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