The Phylogenetic Position of the Enigmatic, Polypodium hydriforme (Cnidaria, Polypodiozoa): Insights from Mitochondrial Genomes

Abstract

Polypodium hydriforme is an enigmatic parasite that belongs to the phylum Cnidaria. Its taxonomic position has been debated: while it was previously suggested to be part of Medusozoa, recent phylogenomic analyses based on nuclear genes support the view that P. hydriforme and Myxozoa form a clade called Endocnidozoa. Medusozoans have linear mitochondrial (mt) chromosomes while myxozoans, as most metazoan species, have circular chromosomes. In this work, we determined the structure of the mt genome of P. hydriforme, using Illumina and Oxford Nanopore Technologies reads, and showed that it is circular. This suggests that P. hydriforme is not nested within Medusozoa, as this would entail linearization followed by re-circulation. Instead, our results support the view that P. hydriforme is a sister clade to Myxozoa, and mt linearization in the lineage leading to medusozoans occurred after the divergence of Myxozoa + P. hydriforme. Detailed analyses of the assembled P. hydriforme mt genome show that: (1) It is encoded on a single circular chromosome with an estimated size of ∼93,000 base pairs, making it one of the largest metazoan mt genomes; (2) Around 78% of the genome encompasses a non-coding region composed of several repeat types; (3) Similar to Myxozoa, no mt tRNAs were identified; (4) The codon TGA is a stop codon and does not encode for tryptophan as in other cnidarians; (5) Similar to other myxozoan mt genomes, it is extremely fast-evolving.

Long-read Sequencing Data Reveals Dynamic Evolution of Mitochondrial Genome Size and the Phylogenetic Utility of Mitochondrial DNA in Hercules Beetles (Dynastes; Scarabaeidae)

“…Specifically, while the size of a circular animal mitogenome can be >40 kb, the size of most circular animal mitogenomes are <20 kb ( Desalles et al 2017 ). While a tube worm has the largest linear mitogenome reported to date (>80 kb; Stampar et al 2019 ), a recent study has reported a >90 kb circular mitogenome in a cnidarian species ( Novosolov et al 2022 ). In insects, the mitogenome size has often been reported to be around 15–16 kb ( Cameron 2014 ; Desalle et al 2017 ; but exceptionally large mitogenomes have been found in bark weevils; Boyce et al 1989 ).…”

“…Furthermore, tandem repeats have been an interesting evolutionary phenomenon in the control region of animal mitochondria not only because of their phylogenetic and systematic utilities ( Faber and Stepien 1997 ; Mundy and Helbig 2004 ; Wan et al 2012 ; Wang et al 2015 ; Novosolov et al 2022 ), but also because of their evolutionary dynamics and the implication on mitochondrial function ( Mundy and Helbig 2004 ; Saito et al 2005 ; Yuan et al 2015 ; Chen et al 2020 ; Kinkar et al 2021 ; Novosolov et al 2022 ). For example, we found that in Dynastes mitogenomes, the 206 bp tandem repeats were closely located both prior to and after the conserved sequence blocks.…”

“…For example, rapid evolution in tandem repeats has been reported in bark weevils that resulted in a mitogenome of unusually large size ( Boyce et al 1989 ). A recent study unraveled an excessive accumulation of tandem repeats in the mitogenome of a cnidarian species, which resulted in a circular mitogenome size >90 kb ( Novosolov et al 2022 ). The evolutionary insights from mitogenome evolution might go undetected should one only apply a short-read sequencing approach, which has been extensively applied in mitogenome assemblies in recent years ( Desalle et al 2017 ; Filipović et al 2021 ; Formenti et al 2021 ).…”

“…The evolutionary insights from mitogenome evolution might go undetected should one only apply a short-read sequencing approach, which has been extensively applied in mitogenome assemblies in recent years ( Desalle et al 2017 ; Filipović et al 2021 ; Formenti et al 2021 ). With recent advances in long-read sequencing technology, we may finally better investigate the evolution of the gene order and genome size of mitogenomes ( De Vivo et al 2022 ; Novosolov et al 2022 ).…”

Myxozoans (Cnidaria) do not Retain Key Oxygen-Sensing and Homeostasis Toolkit Genes

“…Cnidarians have been shown to harbor a wide-range of mt-genome phenotypes, including the “traditional” single circular chromosome, multiple circular chromosomes, a single linear chromosome, or a highly fragmented genome ( fig. 2 ) ( Bridge, et al 1992 ; Kayal, et al 2012 ; Novosolov, et al 2022 ; Osigus, et al 2013 ; Smith, et al 2012 ; Yahalomi, et al 2017 ). The mitochondrion is also typically described as being essential and omnipresent in contemporary eukaryotes, but mitochondrial genomes in “early-branching” eukaryotes are frequently reduced ( Santos, et al 2018 ), or lost altogether ( John, et al 2019 ; Karnkowska, et al 2016 ).…”