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Patchy Distribution of GTPases of Immunity-Associated Proteins (GIMAP) within Cnidarians and Dinoflagellates Suggests a Complex Evolutionary History.

ABSTRACT: GTPases of Immunity-Associated Proteins (GIMAP) are a group of small GTP-binding proteins found in a variety of organisms, including vertebrates, invertebrates, and plants. These proteins are characterized by the highly conserved AIG1 domain, and in vertebrates, have been implicated in regulation of the immune system as well as apoptosis and autophagy, though their exact mechanism of action remains unclear. Recent work on cnidarian GIMAPs suggests a conserved role in immunity, apoptosis, and autophagy-three processes involved in coral bleaching, or the breakdown of cnidarian-dinoflagellate symbiosis. Therefore, to further understand the evolution of GIMAPs in this group of organisms, the purpose of this study was to characterize GIMAP or GIMAP-like sequences utilizing publicly available genomic and transcriptomic data in species across the cnidarian phylogeny. The results revealed a patchy distribution of GIMAPs in cnidarians, with three distinct types referred to as L-GIMAP, S-GIMAP, and GIMAP-like. Additionally, GIMAPs were present in most dinoflagellate species and formed seven well-supported clades. Overall, these results elucidate the distribution of GIMAPs within two distantly related eukaryotic groups and represent the first in-depth investigation on the evolution of these proteins within both protists and basal metazoans.

SUBMITTER: Coelho JC

PROVIDER: S-EPMC8857920 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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Patchy Distribution of GTPases of Immunity-Associated Proteins (GIMAP) within Cnidarians and Dinoflagellates Suggests a Complex Evolutionary History.

Coelho Jenny C JC Calhoun Ethan D ED Calhoun Grant N GN Poole Angela Z AZ

Genome biology and evolution 20220201 2

GTPases of Immunity-Associated Proteins (GIMAP) are a group of small GTP-binding proteins found in a variety of organisms, including vertebrates, invertebrates, and plants. These proteins are characterized by the highly conserved AIG1 domain, and in vertebrates, have been implicated in regulation of the immune system as well as apoptosis and autophagy, though their exact mechanism of action remains unclear. Recent work on cnidarian GIMAPs suggests a conserved role in immunity, apoptosis, and aut ...[more]

PMID: 35015849

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Project description:BackgroundWe recently described a mini-intein in the PRP8 gene of a strain of the basidiomycete Cryptococcus neoformans, an important fungal pathogen of humans. This was the second described intein in the nuclear genome of any eukaryote; the first nuclear encoded intein was found in the VMA gene of several saccharomycete yeasts. The evolution of eukaryote inteins is not well understood. In this report we describe additional PRP8 inteins (bringing the total of these to over 20). We compare and contrast the phylogenetic distribution and evolutionary history of the PRP8 intein and the saccharomycete VMA intein, in order to derive a broader understanding of eukaryote intein evolution. It has been suggested that eukaryote inteins undergo horizontal transfer and the present analysis explores this proposal.ResultsIn total, 22 PRP8 inteins have been detected in species from three different orders of euascomycetes, including Aspergillus nidulans and Aspergillus fumigatus (Eurotiales), Paracoccidiodes brasiliensis, Uncinocarpus reesii and Histoplasma capsulatum (Onygales) and Botrytis cinerea (Helotiales). These inteins are all at the same site in the PRP8 sequence as the original Cryptococcus neoformans intein. Some of the PRP8 inteins contain apparently intact homing endonuclease domains and are thus potentially mobile, while some lack the region corresponding to the homing endonuclease and are thus mini-inteins. In contrast, no mini-inteins have been reported in the VMA gene of yeast. There are several examples of pairs of closely related species where one species carries the PRP8 intein while the intein is absent from the other species. Bio-informatic and phylogenetic analyses suggest that many of the ascomycete PRP8 homing endonucleases are active. This contrasts with the VMA homing endonucleases, most of which are inactive.ConclusionPRP8 inteins are widespread in the euascomycetes (Pezizomycota) and apparently their homing endonucleases are active. There is no evidence for horizontal transfer within the euascomycetes. This suggests that the intein is of ancient origin and has been vertically transmitted amongst the euascomycetes. It is possible that horizontal transfer has occurred between the euascomycetes and members of the basidiomycete genus Cryptococcus.

Dataset Information

Patchy Distribution of GTPases of Immunity-Associated Proteins (GIMAP) within Cnidarians and Dinoflagellates Suggests a Complex Evolutionary History.

Publications

Patchy Distribution of GTPases of Immunity-Associated Proteins (GIMAP) within Cnidarians and Dinoflagellates Suggests a Complex Evolutionary History.

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