Local hopping mobile DNA implicated in pseudogene formation and reductive evolution in an obligate cyanobacteria-plant symbiosis.

Theoden Vigil-Stenman,John Larsson,Johan A A Nylander,Birgitta Bergman

doi:10.1186/s12864-015-1386-7

Abstract

BackgroundInsertion sequences (ISs) are approximately 1 kbp long “jumping” genes found in prokaryotes. ISs encode the protein Transposase, which facilitates the excision and reinsertion of ISs in genomes, making these sequences a type of class I (“cut-and-paste”) Mobile Genetic Elements. ISs are proposed to be involved in the reductive evolution of symbiotic prokaryotes. Our previous sequencing of the genome of the cyanobacterium ‘Nostoc azollae’ 0708, living in a tight perpetual symbiotic association with a plant (the water fern Azolla), revealed the presence of an eroding genome, with a high number of insertion sequences (ISs) together with an unprecedented large proportion of pseudogenes. To investigate the role of ISs in the reductive evolution of ‘Nostoc azollae’ 0708, and potentially in the formation of pseudogenes, a bioinformatic investigation of the IS identities and positions in 47 cyanobacterial genomes was conducted. To widen the scope, the IS contents were analysed qualitatively and quantitatively in 20 other genomes representing both free-living and symbiotic bacteria.ResultsInsertion Sequences were not randomly distributed in the bacterial genomes and were found to transpose short distances from their original location (“local hopping”) and pseudogenes were enriched in the vicinity of IS elements. In general, symbiotic organisms showed higher densities of IS elements and pseudogenes than non-symbiotic bacteria. A total of 1108 distinct repeated sequences over 500 bp were identified in the 67 genomes investigated. In the genome of ‘Nostoc azollae’ 0708, IS elements were apparent at 970 locations (14.3%), with 428 being full-length. Morphologically complex cyanobacteria with large genomes showed higher frequencies of IS elements, irrespective of life style.ConclusionsThe apparent co-location of IS elements and pseudogenes found in prokaryotic genomes implies earlier IS transpositions into genes. As transpositions tend to be local rather than genome wide this likely explains the proximity between IS elements and pseudogenes. These findings suggest that ISs facilitate the reductive evolution in for instance in the symbiotic cyanobacterium ‘Nostoc azollae’ 0708 and in other obligate prokaryotic symbionts.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1386-7) contains supplementary material, which is available to authorized users.

Highlights

Insertion sequences (ISs) are approximately 1 kbp long “jumping” genes found in prokaryotes
The results show that ‘Nostoc azollae’ 0708 (NoAz) has a high portion of its genome occupied by IS elements: 14.3%, which is just below the proportion in O. tsutsugamushi (14.7%), but higher than in any of the other symbiotic organism investigated
‘Onion yellows phytoplasma’ with the smallest genome, 0.85 Mbp, still diverted 7.7% of its genome to be occupied by IS elements and phages, and was the only organism with more phage remains than IS elements

Summary

Introduction

Insertion sequences (ISs) are approximately 1 kbp long “jumping” genes found in prokaryotes. ISs encode the protein Transposase, which facilitates the excision and reinsertion of ISs in genomes, making these sequences a type of class I (“cut-and-paste”) Mobile Genetic Elements. Insertion Sequences (ISs) are defined as genomic sequences of “cut-and-paste” mobile DNA, typically 8001300 bp in length, which encode the protein Transposase. Insertion sequences accumulate in genomes when the evolutionary pressure is low and when decreases in population size result in genetic drift. They are known to influence the evolution of an organism e.g. through gene activation and inactivation, repression, deletions, rearrangements, recombinations, and gene transfers [1]. In “recent” obligate bacterial symbionts the genome reduction is usually small, while the number of insertion sequences tends to be high. In ancient symbiosis the norm is bacterial symbionts with small genomes and few or no ISs [10]

Methods

Results

Discussion

Conclusion