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Marie-jeanne Perrot-minnot - One of the best experts on this subject based on the ideXlab platform.
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Differential patterns of definitive host use by two fish Acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis.
International Journal for Parasitology: Parasites and Wildlife, 2019Co-Authors: Marie-jeanne Perrot-minnot, Emilie Guyonnet, Loïc Bollache, Clément LagrueAbstract:Parasites with complex life-cycles and trophic transmission are expected to show low specificity towards final hosts. However, testing this hypothesis may be hampered by low taxonomic resolution, particularly in helminths. We investigated this issue using two intestinal fish parasites with similar life-cycles and occurring in sympatry, Pomphorhynchus laevis and Pomphorhynchus tereticollis (Acanthocephala). We used species-specific ITS1 length polymorphism to discriminate parasite species from 910 adult Acanthocephalans collected in 174 individual hosts from 12 fish species. Both P. laevis and P. tereticollis exhibited restricted host range within the community of available fish host species, and transmission bias compared to their relative abundance in intermediate hosts. The two parasites also exhibited low niche overlap, primarily due to their contrasting use of bentho-pelagic (P. laevis) and benthic (P. tereticollis) fish. Furthermore, parasite prevalence in intermediate hosts appeared to increase with taxonomic specificity in definitive host use. Comparison of P. laevis and P. tereticollis adult size in the two main definitive hosts, barbel and chub, suggested lower compatibility towards the fish species with the lowest parasite abundance, in particular in P. laevis. The determinants of low niche overlap between these two sympatric Acanthocephalan species, and the contribution of definitive host range diversity to parasite transmission success, are discussed.
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Differential patterns of definitive host use by two fish Acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis
Elsevier, 2019Co-Authors: Marie-jeanne Perrot-minnot, Emilie Guyonnet, Loïc Bollache, Clément LagrueAbstract:Parasites with complex life-cycles and trophic transmission are expected to show low specificity towards final hosts. However, testing this hypothesis may be hampered by low taxonomic resolution, particularly in helminths. We investigated this issue using two intestinal fish parasites with similar life-cycles and occurring in sympatry, Pomphorhynchus laevis and Pomphorhynchus tereticollis (Acanthocephala). We used species-specific ITS1 length polymorphism to discriminate parasite species from 910 adult Acanthocephalans collected in 174 individual hosts from 12 fish species. Both P. laevis and P. tereticollis exhibited restricted host range within the community of available fish host species, and transmission bias compared to their relative abundance in intermediate hosts. The two parasites also exhibited low niche overlap, primarily due to their contrasting use of bentho-pelagic (P. laevis) and benthic (P. tereticollis) fish. Furthermore, parasite prevalence in intermediate hosts appeared to increase with taxonomic specificity in definitive host use. Comparison of P. laevis and P. tereticollis adult size in the two main definitive hosts, barbel and chub, suggested lower compatibility towards the fish species with the lowest parasite abundance, in particular in P. laevis. The determinants of low niche overlap between these two sympatric Acanthocephalan species, and the contribution of definitive host range diversity to parasite transmission success, are discussed. Keywords: Compatibility, Complex life-cycle, Freshwater, Host range, Index, Reproduction, Specificit
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Contrasting phylogeography of two Western Palaearctic fish parasites despite similar life cycles.
Journal of Biogeography, 2018Co-Authors: Marie-jeanne Perrot-minnot, Marta Špakulová, Rémi Wattier, Petr Kotlík, Serdar Düşen, Ali Aydoğdu, Christelle TougardAbstract:Aim We used comparative phylogeography of two intestinal parasites of freshwater fish to test whether similarity in life cycle translates into concordant phylogeographical history. The thorny-headed worms Pomphorhynchus laevis and P. tereticollis (Acanthocephala) were formerly considered as a single species with a broad geographical and host range within the Western Palaearctic. Location Central and eastern parts of Northern Mediterranean area, Western and Central Europe, Ponto-Caspian Europe. Methods A mitochondrial marker (COI) was sequenced for 111 P. laevis and 50 P. tereticollis individuals and nuclear ITS1 and ITS2 sequences were obtained for 37 P. laevis and 21 P. tereticollis. Genetic divergence, phylogenetic relationships and divergence time were estimated for various lineages within each species, and their phylogeographical patterns were compared to known palaeogeographical events in Western Palaearctic. Biogeographical histories of each species were inferred. Results The two species show very different phylogeographical patterns. Five lineages were identified in P. laevis, partially matching several major biogeographical regions defined in the European riverine fish fauna. The early stages of P. laevis diversification occurred in the peri-Mediterranean area, during the Late Miocene. Subsequent expansion across Western Europe and Russia was shaped by dispersal and vicariant events, from Middle Pliocene to Middle Pleistocene. By contrast, P. tereticollis has differentiated more recently within the Western and Central parts of Europe, and shows weak geographical and genetic structuring. Conclusion Our study highlights weak to moderate similarity in the phylogeographical pattern of these Acanthocephalan parasites compared to their amphipod and fish hosts. The observed differences in the timing of dispersion and migration routes taken may reflect the use of a range of final hosts with different ecologies and dispersal capabilities. By using a group underrepresented in phylogeographical studies, our study is a valuable contribution to revealing the biogeography of host–parasite interactions in continental freshwaters.
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Interspecific differences in carotenoid content and sensitivity to UVB radiation in three Acanthocephalan parasites exploiting a common intermediate host.
International Journal for Parasitology, 2011Co-Authors: Marie-jeanne Perrot-minnot, Maria Gaillard, Raphaël Dodet, Frank CézillyAbstract:Few endoparasite species are pigmented. Acanthocephalans are an exception however, with several species being characterised by yellow to orange colouration both at the immature (cystacanth) and adult stages. However, the functional and adaptive significance of carotenoid-based colourations in Acanthocephalans remains unclear. One possibility is that the carotenoid content of Acanthocephalan cystacanths acts as a protective device against ultra-violet radiation (UVR) passing through the translucent cuticle of their crustacean hosts. Indeed, Acanthocephalans often bring about behavioural changes in their aquatic intermediate hosts that can increase their exposure to light. Carotenoid composition and damage due to ultra-violet - B (UVB) radiation were investigated in three Acanthocephalan parasite species that induce contrasting behavioural alterations in their common intermediate host, the crustacean amphipod Gammarus pulex. The fish Acanthocephalans Pomphorhynchus laevis and Pomphorhynchus tereticollis both induce a positive phototaxis in gammarids, such that infected hosts spend more time out of shelters, while remaining benthic. The bird Acanthocephalan Polymorphus minutus, on the other hand, induces a negative geotaxis, such that infected hosts typically swim close to the water surface, becoming more exposed to UV radiation. We show that differences in cystacanth colouration between Acanthocephalan species directly reflect important differences in carotenoid content. The two fish parasites exhibit a contrasting pattern, with P. tereticollis harbouring a large diversity of carotenoid pigments, whereas P. laevis is characterised by a lower carotenoid content consisting mainly of lutein and astaxanthin. The highest carotenoid content is found in the bright orange P.minutus, with a predominance of esterified forms of astaxanthin. Exposure to UVB radiation revealed a higher susceptibility in P. laevis larvae compared with P. tereticollis and P. minutus, in terms of sublethality (decreased evagination rate) and of damage to DNA (increased cyclobutane pyrimidine dimers production). Although we found important and correlated interspecific differences in carotenoid composition and tolerance to high UVB radiation, our results do not fully support the hypothesis of adaptive carotenoid-based colourations in relation to UV protection. An alternative scenario for the evolution of carotenoid accumulation in Acanthocephalan parasites is discussed.
Bernard Marchand - One of the best experts on this subject based on the ideXlab platform.
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ultrastructural study of spermiogenesis and the spermatozoon of cavisoma magnum southwell 1927 Acanthocephala palaeAcanthocephala cavisomidae from siganus lineatus pisces teleostei siganidae valenciennes 1835 in new caledonia
Micron, 2012Co-Authors: Josephine Foata, Rodney A. Bray, Yann Quilichini, Jeanlou Justine, Bernard MarchandAbstract:This paper presents an ultrastructural study of Cavisoma magnum (Acanthocephala, Cavisomatidae) with a Transmission Electron Microscopy tool. This parasite of the fish Siganus lineatus is here reported for the first time from off New Caledonia, South Pacific. It is the first study describing the ultrastructure, spermiogenesis and spermatozoon of a species of the family Cavisomatidae. The young spermatid of C. magnum possesses a centriole constituted of doublets without a central element. After the elaboration of a flagellum of 9+2 pattern, the centriole migrates in a nuclear groove. Then the flagellum migration occurs and gives rise to a spermatozoon. The distribution and the size of the protein granules are reported and the posterior extremity appears like a chromatin lamina wave. Comparative ultrastructural data are presented on sperm and spermiogenesis of the Acanthocephala and Rotifers examined to date and the phylogenetic implications are discussed.
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Ultrastructure of spermiogenesis and the spermatozoon of Macracanthorhynchus hirudinaceus (Pallas, 1781) (Acanthocephala: ArchiAcanthocephala), a parasite of the wild boar Sus scrofa.
The Journal of Parasitology, 2005Co-Authors: Josephine Foata, Julia-laurence Culioli, Bernard MarchandAbstract:The present paper describes the ultrastructure of spermiogenesis and the spermatozoon of Macracanthorhynchus hirudinaceus, an Acanthocephalan parasite of the wild boar Sus scrofa. At the beginning of spermatogenesis, spermatocytes exhibit synaptonemal complexes and 2 centrioles. In the spermatid, only 1 centriole remains, generating a flagellum with a 9+2 pattern. Another ultrastructural feature observed during the spermiogenesis of M. hirudinaceus is the condensation of the chromatin, forming a "honeycomb" structure in the old spermatid and a homogeneous, electron-dense structure in the spermatozoon. The mature spermatozoon of M. hirudinaceus presents a reversed anatomy, as has been described previously in other species of the Acanthocephala. The spermatozoon is divided into 2 parts: an axoneme, and a nucleocytoplasmic derivative. The spermatozoon flagellum exhibits a 9+2 or 9+0 pattern. The process of spermiogenesis and the ultrastructural organization of the spermatozoon of M. hirudinaceus are compared with available data regarding other Acanthocephalan species.
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ultrastructure of spermiogenesis and spermatozoon of leptorhynchoides plagicephalus Acanthocephala palaeAcanthocephala a parasite of the sturgeon acipenser naccarii osteichthyes acipenseriformes
Parasitology Research, 2004Co-Authors: Josephine Foata, B S Dezfuli, Barbara Pinelli, Bernard MarchandAbstract:This paper describes the ultrastructure of spermiogenesis and the spermatozoon of Leptorhynchoides plagicephalus, an Acanthocephalan parasite of the sturgeon Acipenser naccarii, a species which is under the threat of extinction. At the beginning, spermiogenesis in L. plagicephalus is characterized by the presence of a single centriole in the early spermatid. This centriole generates a flagellum with a 9+0 pattern. Another ultrastructural feature observed during the spermiogenesis of L. plagicephalus is the condensation of chromatin to form an “intranuclear wall”. The mature spermatozoon of L. plagicephalus presents a reversed anatomy, as observed in other species of the Acanthocephala. The spermatozoon is divided into two parts: an axoneme and a nucleocytoplasmic derivative. The pattern of spermiogenesis and the ultrastructural organization of the spermatozoon of L. plagicephalus are compared with information available on other Acanthocephalan species. The appearance of an “intranuclear wall” observed during the present study represents the first record within the Acanthocephala and is unknown from other animal taxa.
Josephine Foata - One of the best experts on this subject based on the ideXlab platform.
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ultrastructural study of spermiogenesis and the spermatozoon of cavisoma magnum southwell 1927 Acanthocephala palaeAcanthocephala cavisomidae from siganus lineatus pisces teleostei siganidae valenciennes 1835 in new caledonia
Micron, 2012Co-Authors: Josephine Foata, Rodney A. Bray, Yann Quilichini, Jeanlou Justine, Bernard MarchandAbstract:This paper presents an ultrastructural study of Cavisoma magnum (Acanthocephala, Cavisomatidae) with a Transmission Electron Microscopy tool. This parasite of the fish Siganus lineatus is here reported for the first time from off New Caledonia, South Pacific. It is the first study describing the ultrastructure, spermiogenesis and spermatozoon of a species of the family Cavisomatidae. The young spermatid of C. magnum possesses a centriole constituted of doublets without a central element. After the elaboration of a flagellum of 9+2 pattern, the centriole migrates in a nuclear groove. Then the flagellum migration occurs and gives rise to a spermatozoon. The distribution and the size of the protein granules are reported and the posterior extremity appears like a chromatin lamina wave. Comparative ultrastructural data are presented on sperm and spermiogenesis of the Acanthocephala and Rotifers examined to date and the phylogenetic implications are discussed.
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Ultrastructure of spermiogenesis and the spermatozoon of Macracanthorhynchus hirudinaceus (Pallas, 1781) (Acanthocephala: ArchiAcanthocephala), a parasite of the wild boar Sus scrofa.
The Journal of Parasitology, 2005Co-Authors: Josephine Foata, Julia-laurence Culioli, Bernard MarchandAbstract:The present paper describes the ultrastructure of spermiogenesis and the spermatozoon of Macracanthorhynchus hirudinaceus, an Acanthocephalan parasite of the wild boar Sus scrofa. At the beginning of spermatogenesis, spermatocytes exhibit synaptonemal complexes and 2 centrioles. In the spermatid, only 1 centriole remains, generating a flagellum with a 9+2 pattern. Another ultrastructural feature observed during the spermiogenesis of M. hirudinaceus is the condensation of the chromatin, forming a "honeycomb" structure in the old spermatid and a homogeneous, electron-dense structure in the spermatozoon. The mature spermatozoon of M. hirudinaceus presents a reversed anatomy, as has been described previously in other species of the Acanthocephala. The spermatozoon is divided into 2 parts: an axoneme, and a nucleocytoplasmic derivative. The spermatozoon flagellum exhibits a 9+2 or 9+0 pattern. The process of spermiogenesis and the ultrastructural organization of the spermatozoon of M. hirudinaceus are compared with available data regarding other Acanthocephalan species.
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ultrastructure of spermiogenesis and spermatozoon of leptorhynchoides plagicephalus Acanthocephala palaeAcanthocephala a parasite of the sturgeon acipenser naccarii osteichthyes acipenseriformes
Parasitology Research, 2004Co-Authors: Josephine Foata, B S Dezfuli, Barbara Pinelli, Bernard MarchandAbstract:This paper describes the ultrastructure of spermiogenesis and the spermatozoon of Leptorhynchoides plagicephalus, an Acanthocephalan parasite of the sturgeon Acipenser naccarii, a species which is under the threat of extinction. At the beginning, spermiogenesis in L. plagicephalus is characterized by the presence of a single centriole in the early spermatid. This centriole generates a flagellum with a 9+0 pattern. Another ultrastructural feature observed during the spermiogenesis of L. plagicephalus is the condensation of chromatin to form an “intranuclear wall”. The mature spermatozoon of L. plagicephalus presents a reversed anatomy, as observed in other species of the Acanthocephala. The spermatozoon is divided into two parts: an axoneme and a nucleocytoplasmic derivative. The pattern of spermiogenesis and the ultrastructural organization of the spermatozoon of L. plagicephalus are compared with information available on other Acanthocephalan species. The appearance of an “intranuclear wall” observed during the present study represents the first record within the Acanthocephala and is unknown from other animal taxa.
Holger Herlyn - One of the best experts on this subject based on the ideXlab platform.
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The genome, transcriptome, and proteome of the fish parasite Pomphorhynchus laevis (Acanthocephala).
PLOS ONE, 2020Co-Authors: Katharina Mauer, Hans Zischler, Thomas Hankeln, Sören Lukas Hellmann, Marco Groth, Andreas C. Fröbius, Holger HerlynAbstract: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.
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evolutionary anatomy of the muscular apparatus involved in the anchoring of Acanthocephala to the intestinal wall of their vertebrate hosts
Parasitology Research, 2017Co-Authors: Holger Herlyn, Horst TaraschewskiAbstract:Different conceptions exist regarding structure, function, and evolution of the muscles that move the Acanthocephalan presoma, including the proboscis, i.e., the usually hooked hold-fast anchoring these endoparasites to the intestinal wall of their vertebrate definitive hosts. In order to clarify the unresolved issues, we carried out a light microscopic analysis of series of semi-thin sections and whole mounts representing the three traditional Acanthocephalan classes: ArchiAcanthocephala (Macracanthorhynchus hirudinaceus), EoAcanthocephala (Paratenuisentis ambiguus, Tenuisentis niloticus), and PalaeAcanthocephala (Acanthocephalus anguillae, Echinorhynchus truttae, Pomphorhynchus laevis, Corynosoma sp.). Combining our data with published light, transmission electron, and scanning electron microscopic data, we demonstrate that receptacle protrusor and proboscis receptacle in Archi- and EoAcanthocephala are homologous to the outer and inner wall of the proboscis receptacle in PalaeAcanthocephala. Besides the proboscis receptacle and a “surrounding muscle,” the last common ancestor of Acanthocephala presumably possessed a proboscis retractor, receptacle retractor, neck retractor (continuous with lemnisci compressors), and retinacula. These muscles most probably evolved in the Acanthocephalan stem line. Moreover, the last common ancestor of Acanthocephala presumably possessed only a single layer of muscular cords under the presomal tegument while the metasomal body wall had circular and longitudinal strands. Two lateral receptacle flexors (also lateral receptacle protrusors), an apical muscle plate (surrounding one or two apical sensory organs), a midventral longitudinal muscle, and the differentiation of longitudinal body wall musculature at the base of the proboscis probably emerged within ArchiAcanthocephala. All muscles have a common organization principle: a peripheral layer of contractile filaments encloses the cytoplasm.
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Phylogeny of Syndermata (syn. Rotifera): Mitochondrial gene order verifies epizoic Seisonidea as sister to endoparasitic Acanthocephala within monophyletic Hemirotifera.
Molecular Phylogenetics and Evolution, 2016Co-Authors: Malte Sielaff, David B. Mark Welch, Thomas Hankeln, David Rosenkranz, Hanno Schmidt, Torsten H. Struck, Holger HerlynAbstract:A monophyletic origin of endoparasitic thorny-headed worms (Acanthocephala) and wheel-animals (Rotifera) is widely accepted. However, the phylogeny inside the clade, be it called Syndermata or Rotifera, has lacked validation by mitochondrial (mt) data. Herein, we present the first mt genome of the key taxon Seison and report conflicting results of phylogenetic analyses: while mt sequence-based topologies showed monophyletic Lemniscea (Bdelloidea+Acanthocephala), gene order analyses supported monophyly of Pararotatoria (Seisonidea+Acanthocephala) and Hemirotifera (Bdelloidea+Pararotatoria). Sequence-based analyses obviously suffered from substitution saturation, compositional bias, and branch length heterogeneity; however, we observed no compromising effects in gene order analyses. Moreover, gene order-based topologies were robust to changes in coding (genes vs. gene pairs, two-state vs. multistate, aligned vs. non-aligned), tree reconstruction methods, and the treatment of the two monogonont mt genomes. Thus, mt gene order verifies seisonids as sister to Acanthocephalans within monophyletic Hemirotifera, while deviating results of sequence-based analyses reflect artificial signal. This conclusion implies that the complex life cycle of extant Acanthocephalans evolved from a free-living state, as retained by most monogononts and bdelloids, via an epizoic state with a simple life cycle, as shown by seisonids. Hence, Acanthocephala represent a rare example where ancestral transitional stages have counterparts amongst the closest relatives.
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Transcriptome Data Reveal Syndermatan Relationships and Suggest the Evolution of Endoparasitism in Acanthocephala via an Epizoic Stage
PLoS ONE, 2014Co-Authors: Alexandra R. Wey-fabrizius, Alexander Witek, Holger Herlyn, David B. Mark Welch, Ingo Ebersberger, Benjamin Rieger, David Rosenkranz, Thomas HankelnAbstract:The taxon Syndermata comprises the biologically interesting wheel animals (“Rotifera”: Bdelloidea + Monogononta + Seisonidea) and thorny-headed worms (Acanthocephala), and is central for testing superordinate phylogenetic hypotheses (Platyzoa, Gnathifera) in the metazoan tree of life. Recent analyses of syndermatan phylogeny suggested paraphyly of Eurotatoria (free-living bdelloids and monogononts) with respect to endoparasitic Acanthocephalans. Data of epizoic seisonids, however, were absent, which may have affected the branching order within the syndermatan clade. Moreover, the position of Seisonidea within Syndermata should help in understanding the evolution of Acanthocephalan endoparasitism. Here, we report the first phylogenomic analysis that includes all four higher-ranked groups of Syndermata. The analyzed data sets comprise new transcriptome data for Seison spec. (Seisonidea), Brachionus manjavacas (Monogononta), Adineta vaga (Bdelloidea), and Paratenuisentis ambiguus (Acanthocephala). Maximum likelihood and Bayesian trees for a total of 19 metazoan species were reconstructed from up to 410 functionally diverse proteins. The results unanimously place Monogononta basally within Syndermata, and Bdelloidea appear as the sister group to a clade comprising epizoic Seisonidea and endoparasitic Acanthocephala. Our results support monophyly of Syndermata, Hemirotifera (Bdelloidea + Seisonidea + Acanthocephala), and Pararotatoria (Seisonidea + Acanthocephala), rejecting monophyly of traditional Rotifera and Eurotatoria. This serves as an indication that early Acanthocephalans lived epizoically or as ectoparasites on arthropods, before their complex lifecycle with arthropod intermediate and vertebrate definite hosts evolved.
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Phylogenetic analyses of endoparasitic Acanthocephala based on mitochondrial genomes suggest secondary loss of sensory organs
Molecular Phylogenetics and Evolution, 2013Co-Authors: Mathias Weber, Alexander Witek, Holger Herlyn, Alexandra R. Wey-fabrizius, Lars Podsiadlowski, Ralph O. Schill, László Sugár, Thomas HankelnAbstract:The metazoan taxon Syndermata (Monogononta, Bdelloidea, Seisonidea, Acanthocephala) comprises species with vastly different lifestyles. The focus of this study is on the phylogeny within the syndermatan subtaxon Acanthocephala (thorny-headed worms, obligate endoparasites). In order to investigate the controversially discussed phylogenetic relationships of Acanthocephalan subtaxa we have sequenced the mitochondrial (mt) genomes of Echinorhynchus truttae (PalaeAcanthocephala), Paratenuisentis ambiguus (EoAcanthocephala), Macracanthorhynchus hirudinaceus (ArchiAcanthocephala), and Philodina citrina (Bdelloidea). In doing so, we present the largest molecular phylogenetic dataset so far for this question comprising all major subgroups of Acanthocephala. Alongside with publicly available mt genome data of four additional syndermatans as well as 18 other lophotrochozoan (spiralian) taxa and one outgroup representative, the derived protein-coding sequences were used for Maximum Likelihood as well as Bayesian phylogenetic analyses. We achieved entirely congruent results, whereupon monophyletic ArchiAcanthocephala represent the sister taxon of a clade comprising EoAcanthocephala and monophyletic PalaeAcanthocephala (Echinorhynchida). This topology suggests the secondary loss of lateral sensory organs (sensory pores) within PalaeAcanthocephala and is further in line with the emergence of apical sensory organs in the stem lineage of ArchiAcanthocephala.
Thomas Hankeln - One of the best experts on this subject based on the ideXlab platform.
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The genome, transcriptome, and proteome of the fish parasite Pomphorhynchus laevis (Acanthocephala).
PLOS ONE, 2020Co-Authors: Katharina Mauer, Hans Zischler, Thomas Hankeln, Sören Lukas Hellmann, Marco Groth, Andreas C. Fröbius, Holger HerlynAbstract: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.
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Phylogeny of Syndermata (syn. Rotifera): Mitochondrial gene order verifies epizoic Seisonidea as sister to endoparasitic Acanthocephala within monophyletic Hemirotifera.
Molecular Phylogenetics and Evolution, 2016Co-Authors: Malte Sielaff, David B. Mark Welch, Thomas Hankeln, David Rosenkranz, Hanno Schmidt, Torsten H. Struck, Holger HerlynAbstract:A monophyletic origin of endoparasitic thorny-headed worms (Acanthocephala) and wheel-animals (Rotifera) is widely accepted. However, the phylogeny inside the clade, be it called Syndermata or Rotifera, has lacked validation by mitochondrial (mt) data. Herein, we present the first mt genome of the key taxon Seison and report conflicting results of phylogenetic analyses: while mt sequence-based topologies showed monophyletic Lemniscea (Bdelloidea+Acanthocephala), gene order analyses supported monophyly of Pararotatoria (Seisonidea+Acanthocephala) and Hemirotifera (Bdelloidea+Pararotatoria). Sequence-based analyses obviously suffered from substitution saturation, compositional bias, and branch length heterogeneity; however, we observed no compromising effects in gene order analyses. Moreover, gene order-based topologies were robust to changes in coding (genes vs. gene pairs, two-state vs. multistate, aligned vs. non-aligned), tree reconstruction methods, and the treatment of the two monogonont mt genomes. Thus, mt gene order verifies seisonids as sister to Acanthocephalans within monophyletic Hemirotifera, while deviating results of sequence-based analyses reflect artificial signal. This conclusion implies that the complex life cycle of extant Acanthocephalans evolved from a free-living state, as retained by most monogononts and bdelloids, via an epizoic state with a simple life cycle, as shown by seisonids. Hence, Acanthocephala represent a rare example where ancestral transitional stages have counterparts amongst the closest relatives.
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Transcriptome Data Reveal Syndermatan Relationships and Suggest the Evolution of Endoparasitism in Acanthocephala via an Epizoic Stage
PLoS ONE, 2014Co-Authors: Alexandra R. Wey-fabrizius, Alexander Witek, Holger Herlyn, David B. Mark Welch, Ingo Ebersberger, Benjamin Rieger, David Rosenkranz, Thomas HankelnAbstract:The taxon Syndermata comprises the biologically interesting wheel animals (“Rotifera”: Bdelloidea + Monogononta + Seisonidea) and thorny-headed worms (Acanthocephala), and is central for testing superordinate phylogenetic hypotheses (Platyzoa, Gnathifera) in the metazoan tree of life. Recent analyses of syndermatan phylogeny suggested paraphyly of Eurotatoria (free-living bdelloids and monogononts) with respect to endoparasitic Acanthocephalans. Data of epizoic seisonids, however, were absent, which may have affected the branching order within the syndermatan clade. Moreover, the position of Seisonidea within Syndermata should help in understanding the evolution of Acanthocephalan endoparasitism. Here, we report the first phylogenomic analysis that includes all four higher-ranked groups of Syndermata. The analyzed data sets comprise new transcriptome data for Seison spec. (Seisonidea), Brachionus manjavacas (Monogononta), Adineta vaga (Bdelloidea), and Paratenuisentis ambiguus (Acanthocephala). Maximum likelihood and Bayesian trees for a total of 19 metazoan species were reconstructed from up to 410 functionally diverse proteins. The results unanimously place Monogononta basally within Syndermata, and Bdelloidea appear as the sister group to a clade comprising epizoic Seisonidea and endoparasitic Acanthocephala. Our results support monophyly of Syndermata, Hemirotifera (Bdelloidea + Seisonidea + Acanthocephala), and Pararotatoria (Seisonidea + Acanthocephala), rejecting monophyly of traditional Rotifera and Eurotatoria. This serves as an indication that early Acanthocephalans lived epizoically or as ectoparasites on arthropods, before their complex lifecycle with arthropod intermediate and vertebrate definite hosts evolved.
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Phylogenetic analyses of endoparasitic Acanthocephala based on mitochondrial genomes suggest secondary loss of sensory organs
Molecular Phylogenetics and Evolution, 2013Co-Authors: Mathias Weber, Alexander Witek, Holger Herlyn, Alexandra R. Wey-fabrizius, Lars Podsiadlowski, Ralph O. Schill, László Sugár, Thomas HankelnAbstract:The metazoan taxon Syndermata (Monogononta, Bdelloidea, Seisonidea, Acanthocephala) comprises species with vastly different lifestyles. The focus of this study is on the phylogeny within the syndermatan subtaxon Acanthocephala (thorny-headed worms, obligate endoparasites). In order to investigate the controversially discussed phylogenetic relationships of Acanthocephalan subtaxa we have sequenced the mitochondrial (mt) genomes of Echinorhynchus truttae (PalaeAcanthocephala), Paratenuisentis ambiguus (EoAcanthocephala), Macracanthorhynchus hirudinaceus (ArchiAcanthocephala), and Philodina citrina (Bdelloidea). In doing so, we present the largest molecular phylogenetic dataset so far for this question comprising all major subgroups of Acanthocephala. Alongside with publicly available mt genome data of four additional syndermatans as well as 18 other lophotrochozoan (spiralian) taxa and one outgroup representative, the derived protein-coding sequences were used for Maximum Likelihood as well as Bayesian phylogenetic analyses. We achieved entirely congruent results, whereupon monophyletic ArchiAcanthocephala represent the sister taxon of a clade comprising EoAcanthocephala and monophyletic PalaeAcanthocephala (Echinorhynchida). This topology suggests the secondary loss of lateral sensory organs (sensory pores) within PalaeAcanthocephala and is further in line with the emergence of apical sensory organs in the stem lineage of ArchiAcanthocephala.
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Support for the monophyletic origin of Gnathifera from phylogenomics
Molecular Phylogenetics and Evolution, 2009Co-Authors: Alexander Witek, Holger Herlyn, David B. Mark Welch, Ingo Ebersberger, Thomas HankelnAbstract:The monophyletic origin of Spiralia within the metazoan tree of life is supported by many large-scale phylogenomic data. While there is now substantial molecular evidence for Lophotrochozoa being a monophyletic taxon within Spiralia, the phylogenetic affiliations of many other spiralian phyla remain unclear. Here we focus on the question of a monophyletic taxon Gnathifera, which was originally characterized by jaw morphology as comprising the taxa Rotifera, Acanthocephala and Gnathostomulida. Based on a large-scale molecular sequence dataset of 11,146 amino acid residues, we reconstructed phylogenetic trees of spiralian phyla using maximum-likelihood and Bayesian approaches. We obtain the first phylogenomic evidence for the clade Gnathifera, linking Syndermata (Rotifera + Acanthocephala) with Gnathostomulida. Furthermore, our data support recent findings concerning the paraphyly of Eurotatoria.