Genomic analysis of the regulatory elements and links with intrinsic DNA structural properties in the shrunken genome of Buchnera

Lilia Brinza,Hubert Charles,Federica Calevro

doi:10.1186/1471-2164-14-73

Abstract

BackgroundBuchnera aphidicola is an obligate symbiotic bacterium, associated with most of the aphididae, whose genome has drastically shrunk during intracellular evolution. Gene regulation in Buchnera has been a matter of controversy in recent years as the combination of genomic information with the experimental results has been contradictory, refuting or arguing in favour of a functional and responsive transcription regulation in Buchnera.The goal of this study was to describe the gene transcription regulation capabilities of Buchnera based on the inventory of cis- and trans-regulators encoded in the genomes of five strains from different aphids (Acyrthosiphon pisum, Schizaphis graminum, Baizongia pistacea, Cinara cedri and Cinara tujafilina), as well as on the characterisation of some intrinsic structural properties of the DNA molecule in these bacteria.ResultsInteraction graph analysis shows that gene neighbourhoods are conserved between E. coli and Buchnera in structures called transcriptons, interactons and metabolons, indicating that selective pressures have acted on the evolution of transcriptional, protein-protein interaction and metabolic networks in Buchnera. The transcriptional regulatory network in Buchnera is composed of a few general DNA-topological regulators (Nucleoid Associated Proteins and topoisomerases), with the quasi-absence of any specific ones (except for multifunctional enzymes with a known gene expression regulatory role in Escherichia coli, such as AlaS, PepA and BolA, and the uncharacterized hypothetical regulators YchA and YrbA). The relative positioning of regulatory genes along the chromosome of Buchnera seems to have conserved its ancestral state, despite the genome erosion. Sigma-70 promoters with canonical thermodynamic sequence profiles were detected upstream of about 94% of the CDS of Buchnera in the different aphids. Based on Stress-Induced Duplex Destabilization (SIDD) measurements, unstable σ70 promoters were found specifically associated with the regulator and transporter genes.ConclusionsThis genomic analysis provides supporting evidence of a selection of functional regulatory structures and it has enabled us to propose hypotheses concerning possible links between these regulatory elements and the DNA-topology (i.e., supercoiling, curvature, flexibility and base-pair stability) in the regulation of gene expression in the shrunken genome of Buchnera.

Highlights

Buchnera aphidicola is an obligate symbiotic bacterium, associated with most of the aphididae, whose genome has drastically shrunk during intracellular evolution
Selective constraints acting on the regulatory structures and genome functional analysis in Buchnera In order to determine whether protein interactions exerted a selective pressure on the conservation of some
Among the 55 transcription unit (TU) composing the 38 transcriptons found in both BAp and E. coli, 16 are monocistronic, 13 are identical or similar TUs and 26 are TUs that were reorganised during genome evolution, i.e., formed from a fusion or split from different ancestral TUs

Summary

Introduction

Buchnera aphidicola is an obligate symbiotic bacterium, associated with most of the aphididae, whose genome has drastically shrunk during intracellular evolution. The Buchnera genomes from the five aphid species share certain properties: (1) a small size, from 416 kb for BCc to 641 kb for BAp [1,3,4,5,6]; (2) a low GC-content of about 25%; (3) a standard bacterial gene density of about 85% of coding DNA; (4) the conservation of most genes encoding enzymes from the biosynthesis of essential amino acids that Buchnera furnish to their hosts [7,8] The differences between these five aphid species are related to the physiology of the symbiotic interactions that created specific evolutionary constraints, contributing to the differentiation of the Buchnera gene repertoires [9]. BCc offers an example of evolution with an extremely reduced genome, probably linked to the presence in their aphid host of the co-primary endosymbiont “Candidatus Serratia symbiotica” with which they show a strong dependency and partially share genes of several amino acid biosynthetic pathways [10,11]

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