Dataset Information

Large-scale and significant expression from pseudogenes in Sodalis glossinidius - a facultative bacterial endosymbiont.

ABSTRACT: The majority of bacterial genomes have high coding efficiencies, but there are some genomes of intracellular bacteria that have low gene density. The genome of the endosymbiont Sodalis glossinidius contains almost 50?% pseudogenes containing mutations that putatively silence them at the genomic level. We have applied multiple 'omic' strategies, combining Illumina and Pacific Biosciences Single-Molecule Real-Time DNA sequencing and annotation, stranded RNA sequencing and proteome analysis to better understand the transcriptional and translational landscape of Sodalis pseudogenes, and potential mechanisms for their control. Between 53 and 74?% of the Sodalis transcriptome remains active in cell-free culture. The mean sense transcription from coding domain sequences (CDSs) is four times greater than that from pseudogenes. Comparative genomic analysis of six Illumina-sequenced Sodalis isolates from different host Glossina species shows pseudogenes make up ~40?% of the 2729 genes in the core genome, suggesting that they are stable and/or that Sodalis is a recent introduction across the genus Glossina as a facultative symbiont. These data shed further light on the importance of transcriptional and translational control in deciphering host-microbe interactions. The combination of genomics, transcriptomics and proteomics gives a multidimensional perspective for studying prokaryotic genomes with a view to elucidating evolutionary adaptation to novel environmental niches.

SUBMITTER: Goodhead I

PROVIDER: S-EPMC7067036 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Large-scale and significant expression from pseudogenes in <i>Sodalis glossinidius</i> - a facultative bacterial endosymbiont.

Goodhead Ian I Blow Frances F Brownridge Philip P Hughes Margaret M Kenny John J Krishna Ritesh R McLean Lynn L Pongchaikul Pisut P Beynon Rob R Darby Alistair C AC

Microbial genomics 20200101 1

The majority of bacterial genomes have high coding efficiencies, but there are some genomes of intracellular bacteria that have low gene density. The genome of the endosymbiont <i>Sodalis glossinidius</i> contains almost 50 % pseudogenes containing mutations that putatively silence them at the genomic level. We have applied multiple 'omic' strategies, combining Illumina and Pacific Biosciences Single-Molecule Real-Time DNA sequencing and annotation, stranded RNA sequencing and proteome analysis ...[more]

PMID: 31922467

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Project description:BackgroundSodalis glossinidius, a maternally transmitted bacterial endosymbiont of tsetse flies (Glossina spp.), uses an acylated homoserine lactone (AHL)-based quorum sensing system to modulate gene expression in accordance with bacterial cell density. The S. glossinidius quorum sensing system relies on the function of two regulatory proteins; SogI (a LuxI homolog) synthesizes a signaling molecule, characterized as N-(3-oxohexanoyl) homoserine lactone (OHHL), and SogR1 (a LuxR homolog) interacts with OHHL to modulate transcription of specific target genes.Methodology/principal findingsWe used a tiling microarray to analyze the S. glossinidius transcriptome in the presence and absence of exogenous OHHL. The major finding is that OHHL increases transcription of a large number of genes that are known to be involved in the oxidative stress response. We also show that the obligate symbiont of the rice weevil, Sitophilus oryzae (SOPE), maintains copies of the quorum sensing regulatory genes that are found in S. glossinidius. Molecular evolutionary analyses indicate that these sequences are evolving under stabilizing selection, consistent with the maintenance of their functions in the SOPE symbiosis. Finally, the expression studies in S. glossinidius also reveal that quorum sensing regulates the expression of a cryptic, degenerate gene (carA) that arose from an ancient deletion in the last common ancestor of S. glossinidius and SOPE.Conclusions/significanceThis oxidative stress response is likely mandated under conditions of dense intracellular symbiont infection, when intense metabolic activity is expected to generate a heavy oxidative burden. Such conditions are known to arise in the bacteriocytes of grain weevils, which harbor dense intracellular infections of symbiotic bacteria that are closely related to S. glossinidius. The presence of a degenerate carA sequence in S. glossinidius and SOPE indicates the potential for neofunctionalization to occur during the process of genome degeneration.

Project description:Tsetse flies (Glossina spp.) feed exclusively on vertebrate blood. After a blood meal, the enteric endosymbiont Sodalis glossinidius is exposed to various environmental stressors including high levels of heme. To investigate how S. glossinidius morsitans (Sgm), the Sodalis subspecies that resides within the gut of G. morsitans, tolerates the heme-induced oxidative environment of tsetse's midgut, we used RNAseq to identify bacterial genes that are differentially expressed in cells cultured in high versus lower heme environments. Our analysis identified 436 genes that were significantly differentially expressed (> or < 2-fold) in the presence of high heme [219 heme-induced genes (HIGs) and 217 heme-repressed genes (HRGs)]. HIGs were enriched in Gene Ontology (GO) terms related to regulation of a variety of biological functions, including gene expression and metabolic processes. We observed that 11 out of 13 Sgm genes that were heme regulated in vitro were similarly regulated in bacteria that resided within tsetse's midgut 24 hr (high heme environment) and 96 hr (low heme environment) after the flies had consumed a blood meal. We used intron mutagenesis to make insertion mutations in 12 Sgm HIGs and observed no significant change in growth in vitro in any of the mutant strains in high versus low heme conditions. However, Sgm strains that carried mutations in genes encoding a putative undefined phosphotransferase sugar (PTS) system component (SG2427), fucose transporter (SG0182), bacterioferritin (SG2280), and a DNA-binding protein (SGP1-0002), presented growth and/or survival defects in tsetse midguts as compared to normal Sgm. These findings suggest that the uptake up of sugars and storage of iron represent strategies that Sgm employs to successfully reside within the high heme environment of its tsetse host's midgut. Our results are of epidemiological relevance, as many hematophagous arthropods house gut-associated bacteria that mediate their host's competency as a vector of disease-causing pathogens.

Dataset Information

Large-scale and significant expression from pseudogenes in Sodalis glossinidius - a facultative bacterial endosymbiont.

Publications

Large-scale and significant expression from pseudogenes in <i>Sodalis glossinidius</i> - a facultative bacterial endosymbiont.

Similar Datasets

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