Telomeric transposons are pervasive in linear bacterial genomes.

Eukaryotes have linear DNA, and their telomeres are hotspots for transposons, which in some cases took over telomere maintenance. We identified several families of independently evolved telomeric transposons in linear chromosomes and plasmids of cyanobacteria and Streptomyces. Although these elements have one specific transposon end sequence, with the second boundary being the telomere, we can show that they move using two transposon ends, likely when transiently bridged by the telomere maintenance systems. Mobilization of the element and the associated telomere allows replacement of native telomeres, making the host cell dependent on the new transposon telomere system for genome maintenance. This work indicates how telomeric transposons can promote gene transfer both between and within genomes, substantially influencing the evolutionary dynamics of linear genomes. Editor's summary: Many bacteria maintain their genomic DNA as circular plasmids, but some species keep their chromosomes as linear molecules, similar to eukaryotes. The ends of linear chromosomes have adaptations called telomeres that are protected and maintained by enzymes. Hsieh et al. discovered a class of parasitic DNA elements called transposons that bias integration into chromosome ends. These telomeric transposons use special assembly and targeting mechanisms and have their own telomere maintenance systems that allow the element to control the chromosome end. These bacteria thus need to preserve the transposon, which ensures its survival and shapes how it exchanges genetic information. —Di Jiang INTRODUCTION: Eukaryotes have linear DNA with specialized telomere ends that are protected and maintained by dedicated proteins. Selfish mobile genetic elements called transposons are known to accumulate in gene-poor eukaryotic telomere regions and, in some cases, take control of these ends. Many bacteria maintain their DNA as circles, but multiple medically and industrially relevant species have linear DNA and their own distinct mechanisms of telomere maintenance. Transposons drive genetic exchange in bacteria and have evolved ingenious ways to target integration into permissive genomic sites, strategies that allow these genetic elements to preserve essential functions of the bacterial host. RATIONALE: To understand how transposons propagate in bacteria, a global view of bacterial genomes is required. However, bacteria are extremely diverse, and this diversity is difficult to explore because most species are recalcitrant to growth in the laboratory. Recently, DNA sequencing from natural samples has become a major means to understand microbial diversity by using huge databases of DNA sequence information from diverse environments. We investigated the variety of transposons from nonmodel bacteria and explored their distribution in relation to telomeres to better understand how these elements contribute to the maintenance and exchange of genetic information. RESULTS: We computationally screened large-sequence databases from bacteria that have linear genomes, looking for protein families that are found in transposons. The focus was on types of transposons that use multiple proteins to carefully control where they integrate. We investigated cyanobacteria that maintain their telomeres by looping the two complementary DNA strands as a hairpin. We identified transposons that are only present in telomeric regions and possess the enzyme called protelomerase, which is known to form hairpin DNA ends. Biochemical experiments showed that the protelomerase maintains the specific telomere sequence found with the telomeric transposon, indicating that the transposon controls this end of the host DNA. Reconstituting the transposon in genetically tractable bacteria showed that it can actively mobilize and bias integration to telomeres when the chromosome is linearized. Analysis of DNA sequences from Streptomyces bacteria revealed two additional families of telomeric transposons, which are estimated to populate about a third of these genomes. Streptomyces protect and maintain their telomeres by using proteins that are bound covalently to the DNA ends. These systems also partner with another enzyme that can exchange DNA between bacteria, facilitating evolution. Unlike known transposons that have specific terminal sequence repeats, telomeric transposons have one conserved transposon end and terminate with a telomere on the other side. We identified diverse modalities that allow telomeric transposons to exist as DNA ends. In all cases, these elements likely take control of telomeres, preventing the bacterial host from losing the transposon that now forms its chromosome ends. One subfamily of telomeric transposons co-opted a CRISPR system that is normally used for defense against invading DNA as a tool for the transposon to target chromosome ends, exploiting RNA guides to locate and target telomeric sequences. Population analysis suggests that telomeric transposons replace the telomeres not just from the host but also from other telomeric transposons. CONCLUSION: Transposons are major drivers of genetic exchange across bacteria. Target site selection has emerged as a key feature to ensure transposon spread while minimizing excessive damage to the host. In this work, we identified several families of transposons that populate bacterial telomeres, a striking parallel to the behavior of transposons found in eukaryotes. When these telomeric transposons commandeer a DNA end of the host, they also act as an "addiction" system, ensuring that they cannot be lost. Distinct adaptations allow these elements to spread across telomere ends in the host and horizontally between hosts. They also mobilize genes with new functions that likely benefit new bacterial hosts, profiting the transposon and host. Telomeric transposons occupy linear DNA ends in cyanobacteria and Streptomyces.: The elements possess a single transposon end and replace the target telomere with their own. In cyanobacteria, the telomeric transposons are associated with the protelomerase gene for maintaining their hairpin telomere. In Streptomyces, diverse telomeric transposons, including type I-E CASTs, belong to two families (Tn7-like and TnsBC) and are often associated with telomere maintenance genes. [ABSTRACT FROM AUTHOR]