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Bacterial Adaptation by a Transposition Burst of an Invading IS Element.

ABSTRACT: The general importance of transposable elements (TEs) for adaptive evolution remains unclear. This in part reflects a poor understanding of the role of TEs for adaptation in nonmodel systems. Here, we investigated whether insertion sequence (IS) elements are a major source of beneficial mutations during 400 generations of laboratory evolution of the cyanobacterium Acaryochloris marina strain CCMEE 5410, which has experienced a recent or on-going IS element expansion and has among the highest transposase gene contents for a bacterial genome. Most mutations detected in the eight independent experimental populations were IS transposition events. Surprisingly, however, the majority of these involved the copy-and-paste activity of only a single copy of an unclassified element (ISAm1) that has recently invaded the strain CCMEE 5410 genome. ISAm1 transposition was largely responsible for the highly repeatable evolutionary dynamics observed among populations. Notably, this included mutations in multiple targets involved in the acquisition of inorganic carbon for photosynthesis that were exclusively due to ISAm1 activity. These mutations were associated with an increase in linear growth rate under conditions of reduced carbon availability but did not appear to impact fitness when carbon was readily available. Our study reveals that the activity of a single transposase can fuel adaptation for at least several hundred generations but may also potentially limit the rate of adaptation through clonal interference.

SUBMITTER: Miller SR

PROVIDER: S-EPMC8763236 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The genome of the cyanobacterium Synechocystis sp. strain PCC6803 has nine kinds of insertion sequence (IS) elements, of which ISY100 in 22 copies is the most abundant. A typical ISY100 member is 947 bp long and has imperfect terminal inverted repeat sequences. It has an open reading frame encoding a 282-amino-acid protein that appears to have partial homology with the transposase encoded by a bacterial IS, IS630, indicating that ISY100 belongs to the IS630 family. To determine whether ISY100 has transposition ability, we constructed a plasmid carrying the IPTG (isopropyl-beta-D-thiogalactopyranoside)-inducible transposase gene at one site and mini-ISY100 with the chloramphenicol resistance gene, substituted for the transposase gene of ISY100, at another site and introduced the plasmid into an Escherichia coli strain already harboring a target plasmid. Mini-ISY100 transposed to the target plasmid in the presence of IPTG at a very high frequency. Mini-ISY100 was inserted into the TA sequence and duplicated it upon transposition, as do IS630 family elements. Moreover, the mini-ISY100-carrying plasmid produced linear molecules of mini-ISY100 with the exact 3' ends of ISY100 and 5' ends lacking two nucleotides of the ISY100 sequence. No bacterial insertion elements have been shown to generate such molecules, whereas the eukaryotic Tc1/mariner family elements, Tc1 and Tc3, which transpose to the TA sequence, have. These findings suggest that ISY100 transposes to a new site through the formation of linear molecules, such as Tc1 and Tc3, by excision. Some Tc1/mariner family elements leave a footprint with an extra sequence at the site of excision. No footprints, however, were detected in the case of ISY100, suggesting that eukaryotes have a system that repairs a double strand break at the site of excision by an end-joining reaction, in which the gap is filled with a sequence of several base pairs, whereas prokaryotes do not have such a system. ISY100 transposes in E. coli, indicating that it transposes without any host factor other than the transposase encoded by itself. Therefore, it may be able to transpose in other biological systems.

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Bacterial Adaptation by a Transposition Burst of an Invading IS Element.

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