The draft genome of horseshoe crab Tachypleus tridentatus reveals its evolutionary scenario and well-developed innate immunity

Abstract

Background: Horseshoe crabs are ancient marine arthropods with a long evolutionary history extending back approximately 450 million years, which may benefit from their innate immune systems. However, the genetic mechanisms underlying their abilities of distinguishing and defending against invading microbes are still unclear. Results: Here, we describe the 2.06 Gbp genome assembly of Tachypleus tridentatus with 24,222 predicted protein-coding genes. Comparative genomics shows that T. tridentatus and the Atlantic horseshoe crab Limulus polyphemus have the most orthologues shared among two species, including genes involved in the immune-related JAK-STAT signalling pathway. Divergence time dating results show that the last common ancestor of Asian horseshoe crabs (including T. tridentatus and C. rotundicauda ) and L. polyphemus appeared approximately 130 Mya (121-141), and the split of the two Asian horseshoe crabs was dated to approximately 63 Mya (57-69). Hox gene analysis suggests two clusters in both horseshoe crab assemblies. Surprisingly, selective analysis of immune-related gene families revealed the high expansion of conserved pattern recognition receptors. Genes involved in the IMD and JAK-STAT signal transduction pathways also exhibited a certain degree of expansion in both genomes. Intact coagulation cascade-related genes were present in the T. tridentatus genome with a higher number of coagulation factor genes. Moreover, most reported antibacterial peptides have been identified in T. tridentatus with their potentially effective antimicrobial sites. Conclusions: The draft genome of T. tridentatus would would provide important evidence for further clarifying the taxonomy and evolutionary relationship of Chelicerata. The expansion of conserved immune signalling pathway genes, coagulation factors and intact antimicrobial peptides in T. tridentatus constitutes its robust and effective innate immunity for self-defence in marine environments with an enormous number of invading pathogens and may affect the quality of the adaptive properties with regard to complicated marine environments.

Chromosome‐level genome assembly of the coastal horseshoe crab (Tachypleus gigas)

“…Spiders and scorpions, on the other hand, possess two Hox clusters due to one round of whole‐genome duplication that occurred in their common ancestor (Schwager et al., 2017). Sequencing of the whole‐genome of T. tridentatus , a species closely related to T. gigas , showed that it contained two Hox clusters, suggesting one round of whole‐genome duplication in this lineage (Gong et al., 2019; Zhou et al., 2020). However, a recent study involving sequencing and analysis of the genome of C. rotundicauda revealed the presence of five Hox clusters (Shingate et al., 2020), which suggested at least two rounds of whole‐genome duplication.…”

Systemic paralogy and function of retinal determination network homologs in arachnids

“…The occurrence of RDGN gene duplications in Arachnopulmonata, in tandem with improving functional genetic toolkits in P. tepidariorum (e.g., [ 107 ]), offers a unique opportunity for studying the role of sub- and neofunctionalization during the development of their eyes, and a possible role for these processes in the diversification of number, position and structure of the eyes in an ancient group of arthropods [ 32 , 34 , 93 , 97 , 98 ]. Genomic resources for mites, ticks, and harvestmen [ 108 – 110 ] reveal that apulmonate arachnid orders have not undergone the genome duplication events exhibited by Arachnopulmonata [ 41 ] and separately by horseshoe crabs [ 111 – 113 ]. Future comparative studies focused on understanding the ancestral role of chelicerate RDGN genes should additionally prioritize single-copy orthologs in emerging model systems independent of the arachnopulmonate gene expansion, such as the harvestman Phalangium opilio [ 53 , 114 ].…”

Genomic resources and toolkits for developmental study of whip spiders (Amblypygi) provide insights into arachnid genome evolution and antenniform leg patterning

“…On the other hand, genome and Hox cluster duplications are considered rare in Arthropoda [80]. Complete Hox cluster duplication in the phylum has only been reported in horseshoe crabs (Xiphosura) [34,35,81,82], and in spiders and scorpions (presumed ancestral in Arachnopulmonata). The phylogenetic placement of Amblypygi makes this group an opportune system to test the downstream prediction that P. marginemaculatus retains and expresses Hox paralogs shared by spiders and scorpions.…”