The role of variable DNA tandem repeats in bacterial adaptation

Abstract

DNA tandem repeats (TRs), also designated as satellite DNA, are inter- or intragenic nucleotide sequences that are repeated two or more times in a head-to-tail manner. Because TR tracts are prone to strand-slippage replication and recombination events that cause the TR copy number to increase or decrease, loci containing TRs are hypermutable. An increasing number of examples illustrate that bacteria can exploit this instability of TRs to reversibly shut down or modulate the function of specific genes, allowing them to adapt to changing environments on short evolutionary time scales without an increased overall mutation rate. In this review, we discuss the prevalence and distribution of inter- and intragenic TRs in bacteria and the mechanisms of their instability. In addition, we review evidence demonstrating a role of TR variations in bacterial adaptation strategies, ranging from immune evasion and tissue tropism to the modulation of environmental stress tolerance. Nevertheless, while bioinformatic analysis reveals that most bacterial genomes contain a few up to several dozens of intra- and intergenic TRs, only a small fraction of these have been functionally studied to date.

Suppression of fabB Mutation by fabF1 Is Mediated by Transcription Read-through in Shewanella oneidensis

“…Since the suppressing mutations are exclusively the TGTTTT deletion, it is likely that the mutation occurs within a fragment that is hypermutable. An in silico analysis revealed that the fragment covering the Rho-independent transcription terminator is composed of multiple tandem repeats (TRs), nucleotide sequences which are prone to strand slippage replication and recombinant events (35). To test if these TRs are the reason for suppressing mutations, we introduced them into ⌬desA ⌬fabB vectors carrying either TR-containing or TR-free fragments within multiple-copy-number plasmid pHG101 (Fig.…”

“…To test if these TRs are the reason for suppressing mutations, we introduced them into ⌬desA ⌬fabB vectors carrying either TR-containing or TR-free fragments within multiple-copy-number plasmid pHG101 (Fig. 6), because it has been established that mutation rates increase exponentially with increasing numbers of repeat units (35). The copy number of pHG101, which is based on the RK2 replicon, is about 4 to 7 per cell in E. coli and is estimated to be in a similar range in S. oneidensis (26,36).…”

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

“…The distribution of repeats around a genome can give insights into the mechanism by which they propagate [i.e., DNA replication slippage for tandem and transposition/recombination for distributed repeats, respectively (58,61,62)]. Here, we compared the distribution of putative transposase genes and insertion sequences in the IMS101 genome to the top 10 intergenic regions containing the most abundant repeats identified in our pipeline (Table S1).…”

“…It has been shown in numerous systems that repeating elements (repeats and/or IS; Dataset S8) can be mediators of genomic plasticity (61,62,78); however, the direct impacts of these repeats are not always so clear. For example, high IS density in the genome of Lactobacillus acidophilus has been described (79), and despite the propensity of these elements to inactivate genes and facilitate recombination of genomic structure (61), the genome of this isolate still displays high levels of synteny with other sequenced Lactobacilli.…”

“…Because it has also been shown that partial IS sequences can inhibit transposition (78,80), it is possible that these repeats/pseudogenes have not been deleted because they are controlling transposition in the transposase-heavy IMS101. Others have hypothesized that the conserved repeat structures observed in some bacteria could function as recombinationdependent "promoter banks" for adaptation to new conditions, thereby allowing relatively quick "rewiring" of metabolism in subpopulations (59,62,81).…”