Short- and Long-term Evolutionary Dynamics of Bacterial Insertion Sequences: Insights from Wolbachia Endosymbionts

Abstract

Transposable elements (TE) are one of the major driving forces of genome evolution, raising the question of the long-term dynamics underlying their evolutionary success. Long-term TE evolution can readily be reconstructed in eukaryotes, thanks to many degraded copies constituting genomic fossil records of past TE proliferations. By contrast, bacterial genomes usually experience high sequence turnover and short TE retention times, thereby obscuring ancient TE evolutionary patterns. We found that Wolbachia bacterial genomes contain 52–171 insertion sequence (IS) TEs. IS account for 11% of Wolbachia wRi, which is one of the highest IS genomic coverage reported in prokaryotes to date. We show that many IS groups are currently expanding in various Wolbachia genomes and that IS horizontal transfers are frequent among strains, which can explain the apparent synchronicity of these IS proliferations. Remarkably, >70% of Wolbachia IS are nonfunctional. They constitute an unusual bacterial IS genomic fossil record providing direct empirical evidence for a long-term IS evolutionary dynamics following successive periods of intense transpositional activity. Our results show that comprehensive IS annotations have the potential to provide new insights into prokaryote TE evolution and, more generally, prokaryote genome evolution. Indeed, the identification of an important IS genomic fossil record in Wolbachia demonstrates that IS elements are not always of recent origin, contrary to the conventional view of TE evolution in prokaryote genomes. Our results also raise the question whether the abundance of IS fossils is specific to Wolbachia or it may be a general, albeit overlooked, feature of prokaryote genomes.

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

“…Indeed, we only detected six IS copies (Supplemental Table S3), accounting for <0.5% of the genome, and no group II introns. This is in marked contrast with all other Wolbachia genomes, in which ISs (in wBm and insect strains) and group II introns (in insect strains only) are found in high abundance (Supplemental Table S4; Cerveau et al 2011;Leclercq et al 2011).…”

Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts

“…Most ISRpe1 copies may have been generated in at least two major periods of intense transpositional activity, one ancient and another recent. This could be a widespread feature as several IS families in Wolbachia were recently shown to have the same pattern of transpositional activity (Cerveau et al, 2011b). Endosymbiont IS, including ISRpe1, may thus experiment cyclic expansion separated by periods of low transpositional activity, possibly leading to extinction in some genomes, as previously suggested for diverse IS (Wagner, 2006;Wagner et al, 2007).…”

“…The constitution of their genomes is dynamic, with flexible gene content and rampant intra-generic recombination, indicating accelerated rates of diversification and adaptability (Wu et al, 2004;Klasson et al, 2008;Felsheim et al, 2009;Klasson et al, 2009;Gillespie et al, 2012;Penz et al, 2012;Duplouy et al, 2013). Remarkably, mobile genetic elements represent substantial fractions of these genomes (Bordenstein and Reznikoff, 2005;Wernegreen, 2005;Moran et al, 2008) as exemplified with insertion sequences (ISs), a group of genetically compact transposable elements encoding no functions other than an enzyme that catalyzes their own transposition (Felsheim et al, 2009;Cerveau et al, 2011b). These latter elements are fundamentally selfish DNA parasites, with the capacity to autonomously replicate, proliferating and jumping to other loci within, but also between, genomes (Chandler and Mahillon, 2002;Siguier et al, 2006a).…”

“…This is known as the 'intracellular arena' hypothesis (Bordensteinnd and Wernegreen, 2004;Kent and Bordenstein, 2010). That intra-generic IS transfers occur, and are thus a key factor in shaping endosymbiont evolution, is beyond doubt: phylogenetic evidence indicates that many IS have an extensive history of movement between Wolbachia strains Cerveau et al, 2011b). Inter-generic IS transfers have, however, rarely been reported (Felsheim et al, 2009) and thus thought to be rare within endosymbiont communities.…”

Population Genetics and Molecular Evolution of DNA Sequences in Transposable Elements. I. A Simulation Framework

“…However, these models focus only on the copy number dynamics and did not consider the sequences of TEs. To the best of our knowledge, the most notable exception is the retrotransposon model of Navarro-Quezada and Schoen (2002) (but see Ohta 1985, Slatkin 1985, Brookfield 1986, and Hudson and Kaplan 1986 for fundamental numerical approaches and Quesneville andAnxolabéhère 2001 andCerveau et al 2011 for simple models of DNA transposons). Navarro-Quezada and Schoen (2002) modified the simulation model of Charlesworth and Charlesworth (1983) such that each TE has a DNA sequence.…”