Single-cell transcriptomic atlas reveals the evolution of immune cells and molecules across multiple vertebrate species
Ontology highlight
ABSTRACT:
ORGANISM(S): Mus musculus Rattus norvegicus Danio rerio Sus scrofa Homo sapiens Xenopus tropicalis Macaca mulatta
PROVIDER: GSE186158 | GEO | 2023/01/30
REPOSITORIES: GEO
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Project description:Single-cell transcriptomic atlas reveals the evolution of immune cells and molecules across multiple vertebrate species
| PRJNA772751 | ENA
Project description:IntroductionBoth innate and adaptive immune system undergo evolution from low to high vertebrates. Due to the limitation of conventional approaches in identifying broader spectrum of immune cells and molecules from various vertebrates, it remains unclear how immune molecules evolve among vertebrates.ObjectivesHere, we utilized carry out comparative transcriptome analysis in various immune cells across seven vertebrate species.MethodsSingle-cell RNA sequencing (scRNA-seq).ResultsWe uncovered both conserved and species-specific profiling of gene expression in innate and adaptive immunity. Macrophages exhibited highly-diversified genes and developed sophisticated molecular signaling networks along with evolution, indicating effective and versatile functions in higher species. In contrast, B cells conservatively evolved with less differentially-expressed genes in analyzed species. Interestingly, T cells represented a dominant immune cell populations in all species and unique T cell populations were identified in zebrafish and pig. We also revealed compensatory TCR cascade components utilized by different species. Inter-species comparison of core gene programs demonstrated mouse species has the highest similarity in immune transcriptomes to human.ConclusionsTherefore, our comparative study reveals gene transcription characteristics across multiple vertebrate species during the evolution of immune system, providing insights for species-specific immunity as well as the translation of animal studies to human physiology and disease.
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Project description:How species with similar repertoires of protein coding genes differ so dramatically at the phenotypic level is poorly understood. From comparing the transcriptomes of multiple organs from vertebrate species spanning ~350 million years of evolution, we observe significant differences in alternative splicing complexity between the main vertebrate lineages, with the highest complexity in the primate lineage. Moreover, within as little as six million years, the splicing profiles of physiologically-equivalent organs have diverged to the extent that they are more strongly related to the identity of a species than they are to organ type. Most vertebrate species-specific splicing patterns are governed by the highly variable use of a largely conserved cis-regulatory code. However, a smaller number of pronounced species-dependent splicing changes are predicted to remodel interactions involving factors acting at multiple steps in gene regulation. These events are expected to further contribute to the dramatic diversification of alternative splicing as well as to other gene regulatory changes that contribute to phenotypic differences among vertebrate species.
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Project description:Adaptive immunity and the five vertebrate NF-kB/Rel family members first appeared in cartilaginous fish, suggesting that NF-kB family expansion allowed the acquisition of new functions to regulate adaptive immune responses. Transcriptome profiling revealed that, even in macrophages, the NF-kB family member, c-Rel, most potently regulates a cytokine gene linked to adaptive immunity, Il12b, with limiting roles at key regulators of innate immunity. Neofunctionalization of c-Rel to regulate Il12b depends on its unique DNA-binding properties, which we examined using structural, biochemical, functional, and genomic approaches. Among our findings was functional c-Rel homodimer binding to motifs with little resemblance to canonical NF-kB motifs. To determine whether c-Rel’s unique binding properties drove c-Rel-RelA divergence, we compared binding properties in various vertebrate species. c-Rel-RelA binding properties diverged in mammals and amphibians but were comparable in earlier vertebrates, suggesting that divergent DNA binding emerged relatively late during vertebrate evolution to support increasing complexity of adaptive immune regulation.
2024-03-11 | GSE243011 | GEO
Project description:Adaptive immunity and the five vertebrate NF-kB/Rel family members first appeared in cartilaginous fish, suggesting that NF-kB family expansion allowed the acquisition of new functions to regulate adaptive immune responses. Transcriptome profiling revealed that, even in macrophages, the NF-kB family member, c-Rel, most potently regulates a cytokine gene linked to adaptive immunity, Il12b, with limiting roles at key regulators of innate immunity. Neofunctionalization of c-Rel to regulate Il12b depends on its unique DNA-binding properties, which we examined using structural, biochemical, functional, and genomic approaches. Among our findings was functional c-Rel homodimer binding to motifs with little resemblance to canonical NF-kB motifs. To determine whether c-Rel’s unique binding properties drove c-Rel-RelA divergence, we compared binding properties in various vertebrate species. c-Rel-RelA binding properties diverged in mammals and amphibians but were comparable in earlier vertebrates, suggesting that divergent DNA binding emerged relatively late during vertebrate evolution to support increasing complexity of adaptive immune regulation.
2023-11-29 | GSE243010 | GEO
Project description:The brain requires complex mechanisms of genome regulation to encode and store behavioural information. In mammals, DNA methylation deposited at non-CG dinucleotides characterises brain epigenomes. However, it is unclear to what extent this non-canonical form of DNA methylation is evolutionarily conserved. To test this we profile brain cytosine methylation across the major vertebrate lineages, amphioxus, honeybee and octopus, finding that non-CG methylation in adult brain methylomes is restricted to vertebrates. In vertebrates, the genomic patterns of non-CG do not recapitulate those of CG methylation, yet both patterns are deeply conserved. Whereas low levels of gene body CG methylation demarcate a set of developmental transcription factors across tissues and species, a distinct set of neurodevelopmental genes accumulate non-CG methylation in neural tissues. We further show that the establishment of this methylation context coincides with the origin of the “writer” of non-CG methylation, the methyltransferase DNMT3A, and the “reader”, the methyl-CpG binding protein 2 (MeCP2), fuelled by the ancestral whole genome duplication in vertebrates. Surprisingly, MeCP2 evolved in a stepwise process, from an ancestral MBD4 protein with a dual role in transcriptional regulation and DNA repair in chordates. In sum, we show how a novel neural epigenomic layer assembled at the root of vertebrates and gained new regulatory roles partly independent from CG methylation, which could have fostered the sophisticated cognitive repertoires found in the vertebrate lineage.
2020-10-26 | GSE141609 | GEO
Project description:Stepwise Neofunctionalization of c-Rel during Vertebrate Evolution
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Project description:Vertebrates have highly methylated genomes at CpG positions while most invertebrates have sparsely methylated genomes. Therefore, hypermethylation is considered a major innovation that shaped the genome and the regulatory roles of DNA methylation in vertebrates. However, here we report that the marine sponge Amphimedon queenslandica, belonging to one of the earliest branching animal lineages, has evolved a hypermethylated genome with remarkable similarities to that of a vertebrate. Despite major differences in genome size and architecture, independent acquisition of hypermethylation reveal common distribution patterns and repercussions for genome regulation between both lineages. Genome wide depletion of CpGs is counterbalanced by CpG enrichment at unmethylated promoters, mirroring CpG islands. Furthermore, a subset of CpG-bearing transcription factor motifs are enriched at Amphimedon unmethylated promoters. We find that the animal-specific transcription factor NRF has conserved methyl-sensitivity over 700 million years, indicating an ancient cross-talk between transcription factors and DNA methylation. Finally, the sponge shows vertebrate-like levels of 5-hydroxymethylcytosine, the oxidative derivative of cytosine methylation involved in active demethylation. Hydroxymethylation is concentrated in regions that are enriched for transcription factor motifs and show developmentally dynamic demethylation. Together, these findings push back the links between DNA methylation and its regulatory roles to the early steps of animal evolution. Thus, the Amphimedon methylome challenges the prior hypotheses about the origins of vertebrate genome hypermethylation and its implications for regulatory complexity.
2019-08-02 | GSE124016 | GEO
Project description:vertebrate gut metagenome Metagenome
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