Dataset Information

Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE).

ABSTRACT: BACKGROUND:In vertebrates, it has been repeatedly demonstrated that genes encoding proteins involved in pathogen-recognition by adaptive immunity (e.g. MHC) are subject to intensive diversifying selection. On the other hand, the role and the type of selection processes shaping the evolution of innate-immunity genes are currently far less clear. In this study we analysed the natural variation and the evolutionary processes acting on two genes involved in the innate-immunity recognition of Microbe-Associated Molecular Patterns (MAMPs). RESULTS:We sequenced genes encoding Toll-like receptor 4 (Tlr4) and 7 (Tlr7), two of the key bacterial- and viral-sensing receptors of innate immunity, across 23 species within the subfamily Murinae. Although we have shown that the phylogeny of both Tlr genes is largely congruent with the phylogeny of rodents based on a comparably sized non-immune sequence dataset, we also identified several potentially important discrepancies. The sequence analyses revealed that major parts of both Tlrs are evolving under strong purifying selection, likely due to functional constraints. Yet, also several signatures of positive selection have been found in both genes, with more intense signal in the bacterial-sensing Tlr4 than in the viral-sensing Tlr7. 92% and 100% of sites evolving under positive selection in Tlr4 and Tlr7, respectively, were located in the extracellular domain. Directly in the Ligand-Binding Region (LBR) of TLR4 we identified two rapidly evolving amino acid residues and one site under positive selection, all three likely involved in species-specific recognition of lipopolysaccharide of gram-negative bacteria. In contrast, all putative sites of LBRTLR7 involved in the detection of viral nucleic acids were highly conserved across rodents. Interspecific differences in the predicted 3D-structure of the LBR of both Tlrs were not related to phylogenetic history, while analyses of protein charges clearly discriminated Rattini and Murini clades. CONCLUSIONS:In consequence of the constraints given by the receptor protein function purifying selection has been a dominant force in evolution of Tlrs. Nevertheless, our results show that episodic diversifying parasite-mediated selection has shaped the present species-specific variability in rodent Tlrs. The intensity of diversifying selection was higher in Tlr4 than in Tlr7, presumably due to structural properties of their ligands.

SUBMITTER: Fornuskova A

PROVIDER: S-EPMC3848458 | biostudies-literature | 2013 Sep

REPOSITORIES: biostudies-literature

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Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE).

Fornůsková Alena A Vinkler Michal M Pagès Marie M Galan Maxime M Jousselin Emmanuelle E Cerqueira Frederique F Morand Serge S Charbonnel Nathalie N Bryja Josef J Cosson Jean-François JF

BMC evolutionary biology 20130912

<h4>Background</h4>In vertebrates, it has been repeatedly demonstrated that genes encoding proteins involved in pathogen-recognition by adaptive immunity (e.g. MHC) are subject to intensive diversifying selection. On the other hand, the role and the type of selection processes shaping the evolution of innate-immunity genes are currently far less clear. In this study we analysed the natural variation and the evolutionary processes acting on two genes involved in the innate-immunity recognition of ...[more]

PMID: 24028551

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Project description:Small rodents serve as intermediate or paratenic hosts for a variety of parasites and may participate in the transmission of these parasites into synanthropic cycles. Parasites with neuroinvasive stages, such as Toxoplasma gondii or Toxocara canis, can cause detrimental damage in the brain of intermediate or paratenic hosts. Therefore, the occurrence of neuroinvasive parasite stages was evaluated in brains of wild rodents captured in the city of Leipzig, Germany. In addition, a few specimens from the cities of Hanover, Germany, and Vienna, Austria were included, resulting in a total of 716 rodents collected between 2011 and 2016. Brains were investigated for parasitic stages by microscopic examination of native tissue, artificially digested tissue as well as Giemsa-stained digestion solution to verify positive results. Infective stages of zoonotic ascarids or other helminths were not detected in any sample, while coccidian cysts were found in 10.1% (95% CI: 7.9-12.5%; 72/716) of examined brains. The most abundant rodent species in the study was the bank vole (Myodes glareolus; Arvicolinae), showing an infection rate with cerebral cysts of 13.9% (95% CI: 11.0-17.8%; 62/445), while 2.7% (95% CI: 1.0-5.8%; 6/222) of yellow-necked mice (Apodemus flavicollis; Murinae) were infected. Generalized linear modelling revealed a statistically significant difference in prevalence between M. glareolus and A. flavicollis, significant local differences as well as an effect of increasing body mass on cyst prevalence. Coccidian cysts were differentiated by amplification of the 18S rRNA gene and subsequent sequencing. The majority of identifiable cysts (97.9%) were determined as Frenkelia glareoli, a coccidian species mainly circulating between M. glareolus as intermediate and buzzards (Buteo spp.) as definitive hosts. The zoonotic pathogen Toxoplasma gondii was confirmed in one M. glareolus originating from the city of Leipzig. Overall, it can be concluded that neuroinvasion of zoonotic parasites seems to be rare in M. glareolus and A. flavicollis.

Project description:During the past decade, the kisspeptin system has been identified in various vertebrates, leading to the discovery of multiple genes encoding both peptides (Kiss) and receptors (Kissr). The investigation of recently published genomes from species of phylogenetic interest, such as a chondrichthyan, the elephant shark, an early sarcopterygian, the coelacanth, a non-teleost actinopterygian, the spotted gar, and an early teleost, the European eel, allowed us to get new insights into the molecular diversity and evolution of both Kiss and Kissr families. We identified four Kissr in the spotted gar and coelacanth genomes, providing the first evidence of four Kissr genes in vertebrates. We also found three Kiss in the coelacanth and elephant shark genomes revealing two new species, in addition to Xenopus, presenting three Kiss genes. Considering the increasing diversity of kisspeptin system, phylogenetic, and synteny analyses enabled us to clarify both Kiss and Kissr classifications. We also could trace back the evolution of both gene families from the early steps of vertebrate history. Four Kissr and four Kiss paralogs may have arisen via the two whole genome duplication rounds (1R and 2R) in early vertebrates. This would have been followed by multiple independent Kiss and Kissr gene losses in the sarcopterygian and actinopterygian lineages. In particular, no impact of the teleost-specific 3R could be recorded on the numbers of teleost Kissr or Kiss paralogs. The origin of their diversity via 1R and 2R, as well as the subsequent occurrence of multiple gene losses, represent common features of the evolutionary histories of Kiss and Kissr families in vertebrates. In contrast, comparisons also revealed un-matching numbers of Kiss and Kissr genes in some species, as well as a large variability of Kiss/Kissr couples according to species. These discrepancies support independent features of the Kiss and Kissr evolutionary histories across vertebrate radiation.

Dataset Information

Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE).

Publications

Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE).

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