Abstract
Thorny-headed worms (Acanthocephala) are endoparasites exploiting Mandibulata (Arthropoda) and Gnathostomata (Vertebrata). Despite their world-wide occurrence and economic relevance as a pest, genome and transcriptome assemblies have not been published before. However, such data might hold clues for a sustainable control of acanthocephalans in animal production. For this reason, we present the first draft of an acanthocephalan nuclear genome, besides the mitochondrial one, using the fish parasite Pomphorhynchus laevis (Palaeacanthocephala) as a model. Additionally, we have assembled and annotated the transcriptome of this species and the proteins encoded. A hybrid assembly of long and short reads resulted in a near-complete P. laevis draft genome of ca. 260 Mb, comprising a large repetitive portion of ca. 63%. Numbers of transcripts and translated proteins (35,683) were within the range of other members of the Rotifera-Acanthocephala clade. Our data additionally demonstrate a significant reorganization of the acanthocephalan gene repertoire. Thus, more than 20% of the usually conserved metazoan genes were lacking in P. laevis. Ontology analysis of the retained genes revealed many connections to the incorporation of carotinoids. These are probably taken up via the surface together with lipids, thus accounting for the orange coloration of P. laevis. Furthermore, we found transcripts and protein sequences to be more derived in P. laevis than in rotifers from Monogononta and Bdelloidea. This was especially the case in genes involved in energy metabolism, which might reflect the acanthocephalan ability to use the scarce oxygen in the host intestine for respiration and simultaneously carry out fermentation. Increased plasticity of the gene repertoire through the integration of foreign DNA into the nuclear genome seems to be another underpinning factor of the evolutionary success of acanthocephalans. In any case, energy-related genes and their proteins may be considered as candidate targets for the acanthocephalan control.
Highlights
Acanthocephala are endoparasites of jaw-bearing vertebrates (Gnathostomata) including humans [1,2,3,4]
Mitochondrial genomes of Pomphorhynchus laevis and other acanthocephalans The mitochondrial genome of P. laevis extends over 13,881 bp and contains the typical metazoan set of 36 genes on the heavy strand (Fig 1)
Protein-coding genes and ribosomal rDNAs were identically arranged in P. laevis and ten re-analyzed mitochondrial genomes from Archiacanthocephala, Eoacanthocephala, Palaeacanthocephala, and Polyacanthocephala
Summary
Acanthocephala (thorny-headed worms) are endoparasites of jaw-bearing vertebrates (Gnathostomata) including humans [1,2,3,4]. In their digestive tract, the worms usually grow to adults of several millimeters to a few centimeters in length, followed by heterosexual reproduction. The female produces large quantities of eggs containing a larval stage (acanthor). The eggs are released into the environment with the host’s excrements [5] and subsequently can be orally taken up by an intermediate host from Crustacea, Hexapoda or Myriapoda [1,6]. The acanthor grows to a stage, which can infect the definitive host, following oral uptake of an intermediate host [7]. Additional host types may occur, but only the two-host cycle detailed above is obligatory [8]
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