The early phase of a bacterial insertion sequence infection

Bichsel, Manuel; Barbour, A. D.; Wagner, Andreas

doi:10.1016/j.tpb.2010.08.003

Cited by 28 publications

(36 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Our results support this suggestion and show that even purely detrimental ISs may persist and reach an IS count distribution similar to the one observed in IS5 in sequenced genomes, provided that the HGT rate is larger than the fitness cost induced by one IS in the genome of an infected cell. This is in agreement with our earlier result based on a stochastic infection model [Bichsel et al, 2010]. The HGT rate in turn is larger than the fitness cost of one IS only if the possible increase in the infectiousness of a cell is smaller than the increase in the fitness cost with an increasing IS count.…”

Section: Purely Detrimental Iss Can Persist If the Hgt Rate Is Largersupporting

confidence: 93%

“…We have shown in an earlier paper that regardless of whether ISs are moderately beneficial or detrimental, the chances of a successful IS infection are small [Bichsel et al, 2010]. Here we are interested in the longer-term fate of an IS infection.…”

Section: Discussionmentioning

confidence: 99%

“…While most authors agree that harboring ISs in the genome is in general detrimental to the cell, there is disagreement about whether ISs persist because they are occasionally beneficial to their hosts [Blot, 1994, Shapiro, 1999, Schneider and Lenski, 2004 or because HGT is sufficiently strong to overcome selection against ISs due to their detrimental effects on their hosts [Dawkins, 1976, Doolittle and Sapienza, 1980, Orgel and Crick, 1980, Charlesworth et al, 1994, Nuzhdin, 1999. In an earlier study, we used a stochastic, branching process model to show that even purely detrimental ISs can invade a host cell population and persist, provided that the HGT rate is larger than the fitness cost caused by the IS [Bichsel et al, 2010]. Based on our model, we showed that most IS infections do not persist and die out very quickly.…”

Section: Insert Table 1 Herementioning

confidence: 99%

See 2 more Smart Citations

Estimating the fitness effect of an insertion sequence

2012

Self Cite

View full text Add to dashboard Cite

Since its discovery, mobile DNA has fascinated researchers. In particular, many researchers have debated why insertion sequences persist in prokaryote genomes and populations. While some authors think that insertion sequences persist only because of occasional beneficial effects they have on their hosts, others argue that horizontal gene transfer is strong enough to overcome their generally detrimental effects. In this study, we model the long-term fate of a prokaryote cell population, of which a small proportion of cells has been infected with one insertion sequence per cell. Based on our model and the distribution of IS5, an insertion sequence for which sufficient data is available in 525 fully sequenced proteobacterial genomes, we show that the fitness cost of insertion sequences is so small that they are effectively neutral or only slightly detrimental. We also show that an insertion sequence infection can persist and reach the empirically observed distribution if the rate of horizontal gene transfer is at least as large as the fitness cost, and that this rate is well within the rates of horizontal gene transfer observed in nature. In addition, we show that the time needed to reach the observed prevalence of IS5 is unrealistically long for the fitness cost and horizontal gene transfer rate that we computed. Occasional beneficial effects may thus have played an important role in the fast spreading of insertion sequences like IS5. AbstractSince its discovery, mobile DNA has fascinated researchers. In particular, many researchers have debated why insertion sequences persist in prokaryote genomes and populations. While some authors think that insertion sequences persist only because of occasional beneficial effects they have on their hosts, others argue that horizontal gene transfer is strong enough to overcome their generally detrimental effects. In this study, we model the long-term fate of a prokaryote cell population, of which a small proportion of cells has been infected with one insertion sequence per cell. Based on our model and the distribution of IS5, an insertion sequence for which sufficient data is available in 525 fully sequenced proteobacterial genomes, we show that the fitness cost of insertion sequences is so small that they are effectively neutral or only slightly detrimental. We also show that an insertion sequence infection can persist and reach the empirically observed distribution if the rate of horizontal gene transfer is at least as large as the fitness cost, and that this rate is well within the rates of horizontal gene transfer observed in nature. In addition, we show that the time needed to reach the observed prevalence of IS5 is unrealistically long for the fitness cost and horizontal gene transfer rate that we computed. Occasional beneficial effects may thus have played an important role in the fast spreading of insertion sequences like IS5.

show abstract

Section: Purely Detrimental Iss Can Persist If the Hgt Rate Is Largersupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Insert Table 1 Herementioning

confidence: 99%

See 1 more Smart Citation

Estimating the fitness effect of an insertion sequence

2012

Self Cite

View full text Add to dashboard Cite

show abstract

“…The raison d’etre for transposons and related elements is to disproportionately increase their representation within a given host genome (and to disseminate horizontally wherever possible) 14 , 15 . However, extinction is the long-term fate of most transposons given that selection is relatively impotent when it comes to purging deleterious mutations in transposases.…”

Section: Repins and Raytsmentioning

confidence: 99%

Curiosities of REPINs and RAYTs

Bertels

Rainey

2011

Mobile Genetic Elements

View full text Add to dashboard Cite

Repetitive extragenic palindromic (REP) sequences are a ubiquitous feature of bacterial genomes. Recent work shows that REPs are remnants of a larger mobile genetic element termed a REPIN. REPINs consists of two REP sequences in inverted orientation separated by a spacer region and are thought to be non-autonomous mobile genetic elements that exploit the transposase encoded by REP-Associated tYrosine Transposases (RAYTs). Complimentarity between the two ends of the REPIN suggests that the element forms hairpin structures in single stranded DNA or RNA. In addition to REPINs, other more complex arrangements of REPs have been identified in bacterial genomes, including the genome of the model organism Pseudomonas fluorescens SBW25. Here, we summarize existing knowledge and present new data concerning REPIN diversity. We also consider factors affecting the evolution of REPIN diversity, the ease with which REPINs might be co-opted by host genomes and the consequences of REPIN activity for the structure of bacterial genomes.

show abstract

“…Under this scenario, periodic IS reintroductions in genomes mediated by lateral transfers are crucial for their long-term survival (Wagner 2006; Bichsel et al 2010). However, IS copy number is not directly correlated to the rate of lateral gene transfer in bacteria, suggesting that horizontal transfer may not be a major determinant of IS abundance in genomes (Touchon and Rocha 2007).…”

Section: Introductionmentioning

confidence: 99%

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

Cerveau

Leclercq

Leroy

et al. 2011

Genome Biology and Evolution

View full text Add to dashboard Cite

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.

show abstract

The early phase of a bacterial insertion sequence infection

Cited by 28 publications

References 45 publications

Estimating the fitness effect of an insertion sequence

Estimating the fitness effect of an insertion sequence

Curiosities of REPINs and RAYTs

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

Contact Info

Product

Resources

About