The draft genome of the parasitic nematode Trichinella spiralis

Abstract

Genome evolution studies for the phylum Nematoda have been limited by focusing on comparisons involving Caenorhabditis elegans. We report a draft genome sequence of Trichinella spiralis, a food-borne zoonotic parasite, which is the most common cause of human trichinellosis. This parasitic nematode is an extant member of a clade that diverged early in the evolution of the phylum, enabling identification of archetypical genes and molecular signatures exclusive to nematodes. We sequenced the 64-Mb nuclear genome, which is estimated to contain 15,808 protein-coding genes, at ∼35-fold coverage using whole-genome shotgun and hierarchal map-assisted sequencing. Comparative genome analyses support intrachromosomal rearrangements across the phylum, disproportionate numbers of protein family deaths over births in parasitic compared to a non-parasitic nematode and a preponderance of gene-loss and -gain events in nematodes relative to Drosophila melanogaster. This genome sequence and the identified pan-phylum characteristics will contribute to genome evolution studies of Nematoda as well as strategies to combat global parasites of humans, food animals and crops.

Fig. 1

Protein and gene family changes associated with the origin and evolution of the Nematoda. (a) Protein family changes. At the branch of each lineage, the ‘+’ number indicates family birth events and the ‘-’ number indicates family death events represented by all members indicated for that lineage. For example, there are 702 protein family births ancestral to the phylum Nematoda and 88 protein family deaths in common among the four nematodes by comparison to arthropods (represented by D. melanogaster). These events were reconstructed from 12,206 inter-specific orthologous families (63,273 proteins). (b) Gene duplications and losses over the evolution of the common protein families. The gene duplication and loss events were reconstructed using 858 orthologous multi-member protein families (containing 8,260 proteins) conserved among all 6 species. At the branch of each lineage, the ‘+’ number indicates the number of gene duplication events and the ‘-’ number indicates the number of gene loss events for that lineage.

Fig. 2

Comparison of orthologous protein families among nematodes that span the phylum. Orthologous families comprised of each of the three parasites and D. melanogaster and C. elegans are plotted separately. The size of the dot represents the size of the orthologous family; the position represents the composition of the family based on the three represented species. With the assumption that evolutionarily close species have similar orthologous family size (fewer duplications and deletions), these plots illustrate that T. spiralis is equally distinct from both C. elegans and D. melanogaster while the two other parasites share greater commonality with C. elegans. P-values (derived using Chi-square test in pair-wise plot comparison) indicate a greater number of families present in C. elegans compared to D. melanogaster, and show that significantly fewer families are biased to C. elegans when T. spiralis is present in the orthologous family

Fig. 3

Genes from T. spiralis show macrosyntenic relationships with predicted orthologs from other nematodes. (a) T. spiralis genes on the six largest ultracontigs with orthologs in C. elegans, colored to indicate the C. elegans chromosome on which the ortholog is located. The correlation was strong (R=0.95, R=0.76 and R=0.99), and even stronger when the X chromosome was excluded (R=0.97, R=0.97 and R=0.99). As example, R=0.95 indicates that both T. spiralis Ultracontigs 1 and 4 are strongly associated with one predominant C. elegans chromosome, Chr III, and not a result of random gene distribution. (b) Orthologous segments shared among nematode species shown on the C. elegans chromosomes. Red segments are considered to be ancestral orthologous segments among nematodes. The size of segments corresponds to the C. elegans orthologous segment that might be different than the orthologous segment in the other two species (Supplementary Table 7).

Fig. 4

Distribution of orthologous families among the four nematode representatives spanning the phylum Nematoda. The lineages represented in the Nematoda are: Rhabditida (C. elegans), Tylenchina (M. incognita), Spirurina (B. malayi) and Dorylaimia (T. spiralis). The trophic ecology of each of the 4 nematode species used in this study for pan-phylum analysis is indicated next to the species name. The 2,517 orthologous groups are conserved in all four nematodes. Sixty-four orthologous groups are conserved among the parasitic species, but not the free-living C. elegans. Enrichment of functional categories related to certain orthologous groups compared to the complete functional repertoire for the 4 nematode species is presented in Supplementary Table 8 and Supplementary Table 9.