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Mitochondrial Genomes of Two Thaparocleidus Species (Platyhelminthes: Monogenea) Reveal the First rRNA Gene Rearrangement among the Neodermata.

ABSTRACT: Phylogenetic framework for the closely related Ancylodiscoidinae and Ancyrocephalinae subfamilies remains contentious. As this issue was never studied using a large molecular marker, we sequenced the first two Ancylodiscoidinae mitogenomes: Thaparocleidus asoti and Thaparocleidus varicus. Both mitogenomes had two non-coding regions (NCRs) that contained a number of repetitive hairpin-forming elements (RHE). Due to these, the mitogenome of T. asoti (16,074 bp) is the longest among the Monogenea; especially large is its major NCR, with 3500 bp, approximately 1500 bp of which could not be sequenced (thus, the total mitogenome size is ? 17,600 bp). Although RHEs have been identified in other monopisthocotyleans, they appear to be independently derived in different taxa. The presence of RHEs may have contributed to the high gene order rearrangement rate observed in the two mitogenomes, including the first report of a transposition of rRNA genes within the Neodermata. Phylogenetic analyses using mitogenomic dataset produced Dactylogyrinae embedded within the Ancyrocephalinae (paraphyly), whereas Ancylodiscoidinae formed a sister-group with them. This was also supported by the gene order analysis. 28S rDNA dataset produced polyphyletic Dactylogyridae and Ancyrocephalinae. The phylogeny of the two subfamilies shall have to be further evaluated with more data.

SUBMITTER: Zhang D

PROVIDER: S-EPMC6747449 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Mitochondrial Genomes of Two Thaparocleidus Species (Platyhelminthes: Monogenea) Reveal the First rRNA Gene Rearrangement among the Neodermata.

Zhang Dong D Zou Hong H Jakovlić Ivan I Wu Shan G SG Li Ming M Zhang Jin J Chen Rong R Li Wen X WX Wang Gui T GT

International journal of molecular sciences 20190828 17

Phylogenetic framework for the closely related Ancylodiscoidinae and Ancyrocephalinae subfamilies remains contentious. As this issue was never studied using a large molecular marker, we sequenced the first two Ancylodiscoidinae mitogenomes: Thaparocleidus asoti and Thaparocleidus varicus. Both mitogenomes had two non-coding regions (NCRs) that contained a number of repetitive hairpin-forming elements (RHE). Due to these, the mitogenome of T. asoti (16,074 bp) is the longest ...[more]

PMID: 31466297

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Project description:BackgroundRecent mitochondrial phylogenomics studies have reported a sister-group relationship of the orders Capsalidea and Dactylogyridea, which is inconsistent with previous morphology- and molecular-based phylogenies. As Dactylogyridea mitochondrial genomes (mitogenomes) are currently represented by only one family, to improve the phylogenetic resolution, we sequenced and characterized two dactylogyridean parasites, Lamellodiscus spari and Lepidotrema longipenis, belonging to a non-represented family Diplectanidae.ResultsThe L. longipenis mitogenome (15,433 bp) contains the standard 36 flatworm mitochondrial genes (atp8 is absent), whereas we failed to detect trnS1, trnC and trnG in L. spari (14,614 bp). Both mitogenomes exhibit unique gene orders (among the Monogenea), with a number of tRNA rearrangements. Both long non-coding regions contain a number of different (partially overlapping) repeat sequences. Intriguingly, these include putative tRNA pseudogenes in a tandem array (17 trnV pseudogenes in L. longipenis, 13 trnY pseudogenes in L. spari). Combined nucleotide diversity, non-synonymous/synonymous substitutions ratio and average sequence identity analyses consistently showed that nad2, nad5 and nad4 were the most variable PCGs, whereas cox1, cox2 and cytb were the most conserved. Phylogenomic analysis showed that the newly sequenced species of the family Diplectanidae formed a sister-group with the Dactylogyridae + Capsalidae clade. Thus Dactylogyridea (represented by the Diplectanidae and Dactylogyridae) was rendered paraphyletic (with high statistical support) by the nested Capsalidea (represented by the Capsalidae) clade.ConclusionsOur results show that nad2, nad5 and nad4 (fast-evolving) would be better candidates than cox1 (slow-evolving) for species identification and population genetics studies in the Diplectanidae. The unique gene order pattern further suggests discontinuous evolution of mitogenomic gene order arrangement in the Class Monogenea. This first report of paraphyly of the Dactylogyridea highlights the need to generate more molecular data for monogenean parasites, in order to be able to clarify their relationships using large datasets, as single-gene markers appear to provide a phylogenetic resolution which is too low for the task.

Project description:The phylogenetic relationships of dactylogyrids (Monogenea: Dactylogyridae) parasitising catfishes (Siluriformes) from the Neotropical region were investigated for the first time.Partial sequences of the 28S rRNA gene of 40 specimens representing 25 dactylogyrid species were analysed together with sequences from GenBank using Bayesian inference, Maximum likelihood and Parsimony methods. Monophyly of dactylogyrids infecting catfishes and the Ancyrocephalinae was evaluated using the Approximately Unbiased test.The Ancyrocephalinae is a paraphyletic group of species clustering in three main clades as follows: (i) clade A comprising freshwater dactylogyrids from the Holarctic parasitising perciforms clustering together with species (Ameloblastella, Unibarra and Vancleaveus) parasitising Neotropical catfishes; (ii) clade B including species of Dactylogyrus (Dactylogyrinae) and Pseudodactylogyrus (Pseudodactylogyrinae) along with Ancyrocephalus mogurndae, and marine dactylogyrids with cosmopolitan distribution, parasites of scorpaeniforms and perciforms, along with the freshwater Cichlidogyrus and Scutogyrus (infecting African cichlids [Cichlidae]) and (iii) clade C containing exclusively dactylogyrids of siluriforms, freshwater and marine, with Palaearctic, Ethiopian, Oriental and Neotropical distributions; species of Aphanoblastella and Dactylogyridae gen. sp. 4 from the Neotropical region clustering together with species allocated in the Ancylodiscoidinae, along with species of Cosmetocleithrum, Demidospermus and Dactylogyridae gen. spp.The position of the Ancylodiscoidinae within a larger clade of dactylogyrids (ancyrocephalines) indicates that this subfamily does not represent a natural group. Instead, species allocated to this clade (dactylogyrids of siluriforms along with species of the Ancylodiscoidinae) should be considered as a separate subfamily within the Dactylogyridae. The erection of this taxon requires the search for morphological diagnostic characters in addition to phylogenetic information. A similar strategy should be considered for a new classification of the paraphyletic Ancyrocephalinae. Members of the three clades do not seem to share obvious morphological synapomorphies nor clear patterns in host-parasite associations, zoogeographical distribution or ecology. Clade A should be considered as the Ancyrocephalinae sensu stricto since it includes the type species Ancyrocephalus paradoxus Creplin, 1839. A new subfamily should be proposed to accommodate species currently allocated to Ancyrocephalinae clustering within clade B. Future attempts to propose a new classification of the subfamilies in the Dactylogyridae should include the phylogenetically diverse Neotropical dactylogyrids.

Project description:BackgroundNew records of alien land planarians are regularly reported worldwide, and some correspond to undescribed species of unknown geographic origin. The description of new species of land planarians (Geoplanidae) should classically be based on both external morphology and histology of anatomical structures, especially the copulatory organs, ideally with the addition of molecular data.MethodsHere, we describe the morphology and reproductive anatomy of a species previously reported as Diversibipalium "black", and the morphology of a species previously reported as Diversibipalium "blue". Based on next generation sequencing, we obtained the complete mitogenome of five species of Bipaliinae, including these two species.ResultsThe new species Humbertium covidum n. sp. (syn: Diversibipalium "black" of Justine et al., 2018) is formally described on the basis of morphology, histology and mitogenome, and is assigned to Humbertium on the basis of its reproductive anatomy. The type-locality is Casier, Italy, and other localities are in the Department of Pyrénées-Atlantiques, France; some published or unpublished records suggest that this species might also be present in Russia, China, and Japan. The mitogenomic polymorphism of two geographically distinct specimens (Italy vs France) is described; the cox1 gene displayed 2.25% difference. The new species Diversibipalium mayottensis n. sp. (syn: Diversibipalium "blue" of Justine et al., 2018) is formally described on the basis of external morphology and complete mitogenome and is assigned to Diversibipalium on the basis of an absence of information on its reproductive anatomy. The type- and only known locality is the island of Mayotte in the Mozambique Channel off Africa. Phylogenies of bipaliine geoplanids were constructed on the basis of SSU, LSU, mitochondrial proteins and concatenated sequences of cox1, SSU and LSU. In all four phylogenies, D. mayottensis was the sister-group to all the other bipaliines. With the exception of D. multilineatum which could not be circularised, the complete mitogenomes of B. kewense, B. vagum, B. adventitium, H. covidum and D. mayottensis were colinear. The 16S gene in all bipaliine species was problematic because usual tools were unable to locate its exact position.ConclusionNext generation sequencing, which can provide complete mitochondrial genomes as well as traditionally used genes such as SSU, LSU and cox1, is a powerful tool for delineating and describing species of Bipaliinae when the reproductive structure cannot be studied, which is sometimes the case of asexually reproducing invasive species. The unexpected position of the new species D. mayottensis as sister-group to all other Bipaliinae in all phylogenetic analyses suggests that the species could belong to a new genus, yet to be described.

Project description:Mugil cephalus L., 1758 (flathead mullet) is a valuable commercial fish and a promising object of artificial breeding in the Black Sea and the Sea of Azov, and the study of its parasite fauna is important for fishery and mariculture. Monogeneans of the genus Ligophorus are common ectoparasites dwelling on the gills of mullets. Two representatives of this genus parasitise flathead mullet in the Azov-Black Sea region, namely Ligophorus mediterraneus Sarabeev, Balbuena et Euzet, 2005 and Ligophorus cephali Rubtsova, Balbuena, Sarabeev, Blasco- Costa et Euzet, 2006. Morphological identification of these species requires spending much time and a high level of experience in monogenean taxonomy. For quick and correct species identification of these parasites, we have developed a genotyping approach based on the polymerase chain reaction of allele-specific gene sites for various Monogenea species. A fragment of the 28S ribosomal gene, which includes conserved and variable sites, was chosen as a genetic marker. Three approaches were used as follows: amplified fragment length analysis, allelespecific PCR with endpoint detection and allele-specific real-time PCR using SYBR Green intercalating dye. The first approach was by obtaining PCR products of different lengths that were specific either to L. mediterraneus or to L. cephali. This approach was implemented due to the presence of several variable sites located at a distance from each other. The PCR mixture contained three primers: one forward and two reverse. The forward primer was complementary to the conserved site, which did not differ between species. Reverse primers were speciesspecific and, for each species, they were complementary to different DNA regions located 100 bp apart. As a result, L. mediterraneus was characterized by shorter amplicons than L. cephali. For the second and third approaches, a pair of primers was designed according to the following principle: the forward primer was complementary to both species, since it was selected for the conserved gene region. Reverse primers were species-specific and were designed for the 28S variable region. The two parasite species were distinguished by three-point mutations. Thus, one pair of primers was complementary to L. mediterraneus, the other, to L. cephali. The amplified fragment length analysis and the allele-specific real-time PCR demonstrated 100 % coincidence of genotyping results compared with Sanger sequencing. The developed genotyping protocols can be used not only to distinguish two species of Ligophorus from flathead mullet in ecological studies and veterinary practice but also for further development of similar approaches for other monogeneans, among which there are many pathogenic species.

Dataset Information

Mitochondrial Genomes of Two Thaparocleidus Species (Platyhelminthes: Monogenea) Reveal the First rRNA Gene Rearrangement among the Neodermata.

Publications

Mitochondrial Genomes of Two <i>Thaparocleidus</i> Species (Platyhelminthes: Monogenea) Reveal the First rRNA Gene Rearrangement among the Neodermata.

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