Abstract

BackgroundThe bottlenose dolphin (Tursiops truncatus) is a mammal that belongs to the Cetartiodactyla and have lived in marine ecosystems for nearly 60 millions years. Despite its popularity, our knowledge about its adaptive immunity and evolution is very limited. Furthermore, nothing is known about the genomics and evolution of dolphin antigen receptor immunity.ResultsHere we report a evolutionary and expression study of Tursiops truncatus T cell receptor gamma (TRG) and alpha/delta (TRA/TRD) genes. We have identified in silico the TRG and TRA/TRD genes and analyzed the relevant mature transcripts in blood and in skin from four subjects.The dolphin TRG locus is the smallest and simplest of all mammalian loci as yet studied. It shows a genomic organization comprising two variable (V1 and V2), three joining (J1, J2 and J3) and a single constant (C), genes. Despite the fragmented nature of the genome assemblies, we deduced the TRA/TRD locus organization, with the recent TRDV1 subgroup genes duplications, as it is expected in artiodactyls.Expression analysis from blood of a subject allowed us to assign unambiguously eight TRAV genes to those annotated in the genomic sequence and to twelve new genes, belonging to five different subgroups. All transcripts were productive and no relevant biases towards TRAV-J rearrangements are observed.Blood and skin from four unrelated subjects expression data provide evidence for an unusual ratio of productive/unproductive transcripts which arise from the TRG V-J gene rearrangement and for a “public” gamma delta TR repertoire. The productive cDNA sequences, shared both in the same and in different individuals, include biases of the TRGV1 and TRGJ2 genes.The high frequency of TRGV1-J2/TRDV1- D1-J4 productive rearrangements in dolphins may represent an interesting oligo-clonal population comparable to that found in human with the TRGV9- JP/TRDV2-D-J T cells and in primates.ConclusionsAlthough the features of the TRG and TRA/TRD loci organization reflect those of the so far examined artiodactyls, genomic results highlight in dolphin an unusually simple TRG locus. The cDNA analysis reveal productive TRA/TRD transcripts and unusual ratios of productive/unproductive TRG transcripts. Comparing multiple different individuals, evidence is found for a “public” gamma delta TCR repertoire thus suggesting that in dolphins as in human the gamma delta TCR repertoire is accompanied by selection for public gamma chain.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2841-9) contains supplementary material, which is available to authorized users.

Highlights

  • The bottlenose dolphin (Tursiops truncatus) is a mammal that belongs to the Cetartiodactyla and have lived in marine ecosystems for nearly 60 millions years

  • We annotated all the identified dolphin T cell receptor gamma (TRG) genes using the human (GEDI ID: AF159056) and ovine (GEDI ID: DQ992075.1, DQ992074.1) TRG genomic sequences as a reference; the beginning and end of each coding exon were accurately identified by locating the splice sites and the flanking recombination signal (RS) sequences of the V and J genes (Fig. 1)

  • The genomic structure of the smallest TRG locus described in mammals, includes two TRGV, three TRGV and only one TRGC genes

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Summary

Introduction

The bottlenose dolphin (Tursiops truncatus) is a mammal that belongs to the Cetartiodactyla and have lived in marine ecosystems for nearly 60 millions years. Nothing is known about the genomics and evolution of dolphin antigen receptor immunity. Whales and hippos shared a common semiaquatic ancestor that branched off from other artiodactyls around 60 million years ago [3,4,5]. One of the two branches would evolve into cetaceans, possibly beginning about 52 million years ago, with the protowhale Pakicetus, which underwent aquatic adaptation into the completely aquatic cetaceans [3]. The only studies of antigen receptors immunity revealed that IgG are present in whales [6, 7] and IGHG and IGHA genes have been described in the Atlantic bottlenose dolphin [8]. The locus organization and expression of TRG and TRA/TRD genes have been characterized in ruminants; these species have been shown to possess a large TRG [9,10,11] and TRA/TRD [12,13,14] germline repertoire

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