Abstract

Background

   Parasite evolution has been conceptualized as a process of genetic loss
   and simplification. Contrary to this model, there is evidence of
   expansion and conservation of gene families related to essential
   functions of parasitism in some parasite genomes, reminiscent of
   widespread mosaic evolution—where subregions of a genome have different
   rates of evolutionary change. We found evidence of mosaic genome
   evolution in the cnidarian Myxobolus honghuensis, a myxozoan parasite
   of fish, with extremely simple morphology.

Results

   We compared M. honghuensis with other myxozoans and free-living
   cnidarians, and determined that it has a relatively larger myxozoan
   genome (206 Mb), which is less reduced and less compact due to gene
   retention, large introns, transposon insertion, but not polyploidy.
   Relative to other metazoans, the M. honghuensis genome is depleted of
   neural genes and has only the simplest animal immune components.
   Conversely, it has relatively more genes involved in stress resistance,
   tissue invasion, energy metabolism, and cellular processes compared to
   other myxozoans and free-living cnidarians. We postulate that the
   expansion of these gene families is the result of evolutionary
   adaptations to endoparasitism. M. honghuensis retains genes found in
   free-living Cnidaria, including a reduced nervous system, myogenic
   components, ANTP class Homeobox genes, and components of the Wnt and
   Hedgehog pathways.

Conclusions

   Our analyses suggest that the M. honghuensis genome evolved as a mosaic
   of conservative, divergent, depleted, and enhanced genes and pathways.
   These findings illustrate that myxozoans are not as genetically simple
   as previously regarded, and the evolution of some myxozoans is driven
   by both genomic streamlining and expansion.

Supplementary Information

   The online version contains supplementary material available at
   10.1186/s12915-022-01249-8.

   Keywords: Evolutionary genomics, Parasite evolution, Genome
   streamlining, Cnidaria, Myxozoa, Myxobolus honghuensis

Background

   Parasite evolution is a focal issue in evolutionary biology and ecology
   [[35]1, [36]2]. Understanding the evolutionary processes of the
   transition of ancestral free-living organisms to parasitism is
   important for human health and agriculture and offers a new testing
   ground for evolutionary and ecological theory [[37]3, [38]4]. Relative
   to free-living species, parasite genomes are typically smaller and more
   tightly packed with protein-coding genes [[39]5, [40]6]. Parasite
   evolution is usually considered to be accompanied by loss of genetic
   complexity, as exploitation of host metabolic pathways releases
   selective constraints on parts of the parasite genome, resulting in
   loss of now-redundant functions (and associated genes) [[41]7].
   Accordingly, an appealing reductive theory of evolution has been
   developed to describe this loss of function and subsequent streamlining
   that governs parasite genome evolution [[42]8, [43]9]. However, there
   is evidence for conservation and even expansion of gene families
   associated with infection and survival in some parasite genomes [[44]6,
   [45]10]. The opposing characters of genomic streamlining and expansion
   are components of a pervasive process known as mosaic evolution, which
   is the tendency for a genome to evolve as a set of discrete units, each
   with its own evolutionary mode, rather than being dominated by a
   uniform trend [[46]11, [47]12]. Mosaic evolution is widely used to
   frame observed genomic changes in free-living taxa including mice,
   humans, and birds [[48]12–[49]15]. There is much less evidence of
   selective genetic expansion in parasites [[50]6, [51]10,
   [52]16–[53]18]; thus, mosaic evolution has rarely been emphasized in
   describing parasite evolutionary patterns. We propose that a more
   complete picture of parasite genome evolution should incorporate the
   opposing features of streamlining and novel complexity.

   Cnidarians are early-diverging metazoans and ideally suited for
   investigating the genomic changes that underlie parasitism, as the
   group includes both free-living (e.g., Medusozoa, Anthozoa) and
   parasitic taxa (Myxozoa and Polypodiozoa) [[54]19]. Myxozoa are
   microscopic, oligocellular endoparasites with simple body organization,
   but multiple morphologies in their complex life cycles [[55]20,
   [56]21]. The few sequenced myxozoan genomes are more compact and
   smaller than those of free-living cnidarians [[57]22], with some
   species having reduced metabolic capacity [[58]23], or having lost core
   animal features such as cytosine methylation [[59]24] or their
   mitochondrial genome [[60]25]. These findings support the view that
   evolutionary loss and simplification have played a major role in
   shaping the evolution of myxozoans [[61]22, [62]25, [63]26].

   Here we characterize the genome of Myxobolus honghuensis, a parasite of
   economically important gibel carp [[64]27]. We compare its genome with
   other myxozoans and free-living Cnidaria to reveal unique and conserved
   genomic features that characterize this cryptically complex parasite
   group.

Results

Genome assembly and annotation

   We sequenced the M. honghuensis genome with a PacBio RSII, yielding
   ~136× coverage and a 16-kilobase (kb) average read length (Additional
   file [65]1: Table S1). The final long-read data contained 2,030,357
   sequences with a mean length of 10.4 kb (Additional file [66]1: Table
   S2). The genome size was estimated by k-mer analysis using Jellyfish
   software (Additional file [67]2: Fig. S1) to be 206 megabases (Mb). The
   FALCON-assembled genome contained 1118 contigs (161 Mb, N50 1.3 Mb;
   Table [68]1). M. honghuensis has a relatively larger myxozoan genome
   (Additional file [69]1: Table S3). The assembly showed high integrity
   and quality, with >98.5% of Illumina genome survey reads mapped to the
   PacBio assembly (Additional file [70]1: Table S4), and successful
   reconstruction of the nuclear rRNAs. Core Eukaryotic Genes Mapping
   Approach (CEGMA) [[71]28] identified only 42.7% of CEGs; a low
   percentage also seen in another myxozoan [[72]25] and possibly due to
   fast-evolutionary rates rendering even common eukaryotic genes
   difficult to recognize.

Table 1.

   Comparison of myxozoan genome assembly quality
   Species name Myxobolus honghuensis Thelohanellus kitauei Myxobolus
   squamalis Henneguya salminicola Kudoa iwatai Enteromyxum leei
   Sphaeromyxa zaharoni
   Assembly size (kb) 161,092,274 150,348,159 43,671,844 61,443,780
   31,197,353 68,163,509 173,585,031
   Number of scaffolds 1118 5757 37,921 18,330 1639 69,053 70,914
   Number of contigs 1118 15,632 37,919 18,330 1646 69,178 70,935
   Contig N50 1,273,483 13,033 1286 7570 39,532 998 4474
   Scaffold N50 1,273,483 149,756 1286 7570 40,195 998 4474
   CEGs (complete) 42.7% 46.8% 37.5% 53.6% 73.0% 25.8% 39.1%
   %GC 22.8 37.5 27.3 29.0 23.6 33.5 28.0
   References Present study Yang et al., 2014 [[73]23] Yahalomi et al.,