Different phylogenomic methods support monophyly of enigmatic ‘Mesozoa’ (Dicyemida + Orthonectida, Lophotrochozoa)

Abstract

Dicyemids and orthonectids were traditionally classified in a group called Mesozoa, but their placement in a single clade has been contested and their position(s) within Metazoa is uncertain. Here, we assembled a comprehensive matrix of Lophotrochozoa (Metazoa) and investigated the position of Dicyemida (= Rhombozoa) and Orthonectida, employing multiple phylogenomic approaches. We sequenced seven new transcriptomes and one draft genome from dicyemids ( Dicyema , Dicyemennea ) and two transcriptomes from orthonectids ( Rhopalura ). Using these and published data, we assembled and analysed contamination-filtered datasets with up to 987 genes. Our results recover Mesozoa monophyletic and as a close relative of Platyhelminthes or Gnathifera. Because of the tendency of the long-branch mesozoans to group with other long-branch taxa in our analyses, we explored the impact of approaches purported to help alleviate long-branch attraction (e.g. taxon removal, coalescent inference, gene targeting). None of these were able to break the association of Orthonectida with Dicyemida in the maximum-likelihood trees. Contrastingly, the Bayesian analysis and site-specific frequency model in maximum-likelihood did not recover a monophyletic Mesozoa (but only when using a specific 50 gene matrix). The classic hypothesis on monophyletic Mesozoa is possibly reborn and should be further tested.

Plasmodium structure of Intoshia linei (Orthonectida)

“…The close phylogenetic relationship between annelids and orthonectids was lately supported by phylogenetic analysis of mitochondrial and nuclear genes (Bondarenko et al, 2019; Mikhailov et al, 2016; Schiffer et al, 2018; Zverkov et al, 2019). At the same time, some recent phylogenetic surveys based on transcriptomic and genomic evidence have revived the classical hypothesis on monophyletic Mesozoa (Orthonectida + Dicyemida), and the phylum was positioned either sister to Gastrotricha (Lu et al, 2017), or to Platyhelminthes or Gnathifera (Drábková et al, 2022).…”

RNA‐seq analysis of parasitism by Intoshia linei (Orthonectida) reveals protein effectors of defence, communication, feeding and growth

“…Nearly one‐fourth of the plasmodium‐associated proteins detected in this study currently lack homology to any known species except Orthonectida and do not contain any known conserved domains, which is in accordance with the derived genetic nature of orthonectids (Mikhailov et al, 2016; Slyusarev et al, 2020). Orthonectids have been considered relatives to various phyla, and this uncertainty in recent phylogenetic analyses highlights their divergence from any existing group (Bondarenko et al, 2019; Drábková et al, 2022; Lu et al, 2017; Mikhailov et al, 2016; Schiffer et al, 2018; Zverkov et al, 2019). Orphan genes usually have a narrow phylogenetic distribution, evolve rapidly, and mediate lineage‐specific adaptations (Khalturin et al, 2009).…”

“…The exact phylogenetic position of orthonectids is still being discussed. Although many authors supported the close phylogenetic relationship between orthonectids and annelids (Bondarenko et al, 2019; Mikhailov et al, 2016; Schiffer et al, 2018; Zverkov et al, 2019), some recent phylogenetic surveys positioned orthonectids either sister to Gastrotricha (Lu et al, 2017), or to Platyhelminthes or Gnathifera (Drábková et al, 2022). Orthonectids underwent drastic compaction of their genomes and simplification of their body plan (Mikhailov et al, 2016; Slyusarev & Starunov, 2016; Slyusarev et al, 2019, 2022, 2023).…”

Acceleration of genome rearrangement in clitellate annelids

“…For the latter, raw data were downloaded from NCBI SRA (SRR6766626, SRR10997450, SRR6766627, SRR6766628, SRR6766630, SRR6766631, SRR6766632, SRR10997434, and SRR6766629) and assembled with Trinity v2.8.4 (Haas et al 2013) with the following optional flags: --trimmomatic --quality_trimming_params “ILLUMINACLIP:/kmk/scripts/trimmomatic/adapters.fasta:2:30:10 SLIDINGWINDOW:4:5 LEADING:5 TRAILING:5 MINLEN:25” --normalize_reads. Assembled transcriptomes were translated using TransDecoder (https://github.com/TransDecoder) following the approach used by (Kutschera et al 2013; Drábková et al 2022). Repeats in the genome assembly were annotated and softmasked with RepeatMasker and RepeatModeler (Flynn et al 2020) using rmblast for both programs (https://www.repeatmasker.org).…”