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Definition of a third VLR gene in hagfish

Significance The jawless vertebrates (hagfish and lampreys) possess an alternative adaptive immune system in which variable lymphocyte receptors (VLRs) constructed of leucine-rich repeats are used to recognize foreign antigens. Three VLR genes have been identified in lampreys (VLRA, VLRB, and VLRC), but only two (VLRA and VLRB) have been found in hagfish. Here, we identified and characterized a third hagfish VLR gene. Our analysis indicates that the third hagfish VLR is the ortholog of lamprey VLRA, while the previously identified hagfish “VLRA” is the counterpart of lamprey VLRC. The demonstration of three orthologous VLR genes in hagfish and lampreys suggests that this anticipatory receptor system evolved in a common ancestor of the two jawless vertebrate lineages ∼480 Mya. Jawless vertebrates (cyclostomes) have an alternative adaptive immune system in which lymphocytes somatically diversify their variable lymphocyte receptors (VLR) through recombinatorial use of leucine-rich repeat cassettes during VLR gene assembly. Three types of these anticipatory receptors in lampreys (VLRA, VLRB, and VLRC) are expressed by separate lymphocyte lineages. However, only two VLR genes (VLRA and VLRB) have been found in hagfish. Here we have identified a third hagfish VLR, which undergoes somatic assembly to generate sufficient diversity to encode a large repertoire of anticipatory receptors. Sequence analysis, structural comparison, and phylogenetic analysis indicate that the unique hagfish VLR is the counterpart of lamprey VLRA and the previously identified hagfish “VLRA” is the lamprey VLRC counterpart. The demonstration of three orthologous VLR genes in both lampreys and hagfish suggests that this anticipatory receptor system evolved in a common ancestor of the two cyclostome lineages around 480 Mya.