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. Mean sense transcription from Coding Domain Sequences (CDS) 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 2,729 genes in the core genome, suggesting that they are stable and/or Sodalis is a recent introduction across the Glossina genus as a facultative symbiont. These data further shed light on the importance of transcriptional and translational control in deciphering host-microbe interactions. The combination of genomics, transcriptomics and proteomics give a multidimensional perspective for studying prokaryotic genomes with a view to elucidating evolutionary adaptation to novel environmental niches.ImportanceBacterial genes are generally 1Kb in length, organized efficiently (i.e. with few gaps between genes or operons), and few open reading frames (ORFs) lack any predicted function. Intracellular bacteria have been removed from extracellular selection pressures acting on pathways of declining importance to fitness and thus, these bacteria tend to delete redundant genes in favour of smaller functional repertoires. In the genomes of endosymbionts with a recent evolutionary relationship with their host, however, this process of genome reduction is not complete; Genes and pathways may be at an intermediate stage, undergoing mutation linked to reduced selection and small population numbers being vertically transmitted from mother to offspring in their hosts, resulting in an increase in abundance of pseudogenes and reduced coding capacities. A greater knowledge of the genomic architecture of persistent pseudogenes, with respect to their DNA structure, mRNA transcription and even putative translation to protein products, will lead to a better understanding of the evolutionary trajectory of endosymbiont genomes, many of which have important roles in arthropod ecology.

Bee foraging preferences, microbiota and pathogens revealed by direct shotgun metagenomics of honey

“…Likewise, amino acid transport appears to occur frequently between the gut microbiome and honeybees (71). Sodalis glossinidius was enriched in functions related to transposition, consistent with a recent study that evaluated the genomic landscape of Sodalis glossonidius and showed that a large part of it encoded for transposition-related pseudogenes (72). Importantly, Sodalis praecaptivus is considered to be the only currently known free-living form of Sodalis bacteria (73), while…”

A Tale of Three Species: Adaptation of Sodalis glossinidius to Tsetse Biology, Wigglesworthia Metabolism, and Host Diet

“…It has been noted previously that argC is pseudogenized (29), but the new annotation indicates that this may not be the case. ArgC is also detected by proteomics, suggesting that this gene is indeed likely functional (47).…”

“…This is particularly relevant in symbiotic bacteria where the functionality of broken or fragmented genes is not certain. Indeed, a recent report implies that some S. glossinidius genes thought to be pseudogenized are in fact under transcriptional control (47).…”

A phylogenomic study quantifies competing mechanisms for pseudogenization in prokaryotes—The Mycobacterium leprae case

“…Thus, the high synteny and high expression levels of most PGs imply that they have not likely been gained through HGT, but are the result of degradation of native genes. Indeed, large scale pseudogenization that is due to such degradation appears to be characteristic to intracellular bacteria, as many of their genes become inactivated during the transition from an independent lifestyle to the more stable environment of their host [ 49 , 50 ].…”