Gregarines

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Brian S Leander - One of the best experts on this subject based on the ideXlab platform.

  • molecular phylogenetic positions of two new marine Gregarines apicomplexa paralecudina anankea n sp and lecudina caspera n sp from the intestine of lumbrineris inflata polychaeta show patterns of co evolution
    Journal of Eukaryotic Microbiology, 2018
    Co-Authors: Davis Iritani, Kevin C Wakeman, Brian S Leander
    Abstract:

    Gregarine apicomplexans are unicellular parasites commonly found in the intestines and coeloms of invertebrate hosts. Traits associated with the conspicuous feeding stage of Gregarines, known as the trophozoite, have been used in combination with molecular phylogenetic data for species delimitation and the reconstruction of evolutionary history. Trophozoite morphology alone is often inadequate for inferring phylogenetic relationships and delimiting species due to frequent cases of high intraspecific variation combined with relatively low interspecific variation. The current study combined morphological data with small subunit (SSU) rDNA sequences to describe and establish two novel marine gregarine species isolated from the intestine of a polychaete host Lumbrineris inflata collected in British Columbia (Canada): Paralecudina anankea n. sp. and Lecudina caspera n. sp. The sister species to the host is Lumbrineris japonica, which can be found on the opposite side of the Pacific Ocean (Japan) and contains two different species of gregarine parasites: Paralecudina polymorpha and Lecudina longissima. Molecular phylogenetic analyses placed P. anankea n. sp. as the sister species to P. polymorpha and L. caspera n. sp. as the sister species to L. longissima. This phylogenetic pattern demonstrates a co-evolutionary history whereby speciation of the host (Lumbrineris) corresponds with simultaneous speciation of the two different lineages of intestinal Gregarines (Paralecudina and Lecudina). This article is protected by copyright. All rights reserved.

  • molecular phylogeny and ultrastructure of caliculium glossobalani n gen et sp apicomplexa from a pacific glossobalanus minutus hemichordata confounds the relationships between marine and terrestrial Gregarines
    Journal of Eukaryotic Microbiology, 2014
    Co-Authors: Kevin C Wakeman, James Davis Reimer, Holger Jenkekodama, Brian S Leander
    Abstract:

    Gregarines are a diverse group of apicomplexan parasites with a conspicuous extracellular feeding stage, called a “trophozoite”, that infects the intestines and other body cavities of invertebrate hosts. Although the morphology of trophozoites is very diverse in Gregarines as a whole, high degrees of intraspecific variation combined with relatively low degrees of interspecific variation make the delimitation of different species based on trophozoite morphology observed with light microscopy difficult. The coupling of molecular phylogenetic data with comparative morphology has shed considerable light onto the boundaries and interrelationships of different gregarine species. In this study, we isolated a novel marine gregarine from the hepatic region of a Pacific representative of the hemichordate Glossobalanus minutus, and report the first ultrastructural and molecular data from any gregarine infecting this distinctive group of hosts. Molecular phylogenetic analyses of an SSU rDNA sequence derived from two single-cell isolates of this marine gregarine demonstrated a strong and unexpected affiliation with a clade of terrestrial Gregarines (e.g. Gregarina). This molecular phylogenetic data combined with a comparison of the morphological features in previous reports of Gregarines collected from Atlantic representatives of G. minutus justified the establishment of a new binomial for the new isolate, namely Caliculium glossobalani n. gen. et sp. The molecular phylogenetic analyses demonstrated a clade of terrestrial Gregarines associated with a sequence acquired from a marine species, which suggest that different groups of terrestrial/freshwater Gregarines evolved independently from marine ancestors.

  • identification of a divergent environmental dna sequence clade using the phylogeny of gregarine parasites apicomplexa from crustacean hosts
    PLOS ONE, 2011
    Co-Authors: Timur G. Simdyanov, Sonja Rueckert, Vladimir V Aleoshin, Brian S Leander
    Abstract:

    Background Environmental SSU rDNA surveys have significantly improved our understanding of microeukaryotic diversity. Many of the sequences acquired using this approach are closely related to lineages previously characterized at both morphological and molecular levels, making interpretation of these data relatively straightforward. Some sequences, by contrast, appear to be phylogenetic orphans and are sometimes inferred to represent “novel lineages” of unknown cellular identity. Consequently, interpretation of environmental DNA surveys of cellular diversity rely on an adequately comprehensive database of DNA sequences derived from identified species. Several major taxa of microeukaryotes, however, are still very poorly represented in these databases, and this is especially true for diverse groups of single-celled parasites, such as gregarine apicomplexans. Methodology/Principal Findings This study attempts to address this paucity of DNA sequence data by characterizing four different gregarine species, isolated from the intestines of crustaceans, at both morphological and molecular levels: Thiriotia pugettiae sp. n. from the graceful kelp crab (Pugettia gracilis), Cephaloidophora cf. communis from two different species of barnacles (Balanus glandula and B. balanus), Heliospora cf. longissima from two different species of freshwater amphipods (Eulimnogammarus verrucosus and E. vittatus), and Heliospora caprellae comb. n. from a skeleton shrimp (Caprella alaskana). SSU rDNA sequences were acquired from isolates of these gregarine species and added to a global apicomplexan alignment containing all major groups of Gregarines characterized so far. Molecular phylogenetic analyses of these data demonstrated that all of the Gregarines collected from crustacean hosts formed a very strongly supported clade with 48 previously unidentified environmental DNA sequences. Conclusions/Significance This expanded molecular phylogenetic context enabled us to establish a major clade of intestinal gregarine parasites and infer the cellular identities of several previously unidentified environmental SSU rDNA sequences, including several sequences that have formerly been discussed broadly in the literature as a suspected “novel” lineage of eukaryotes

  • molecular systematics of marine Gregarines apicomplexa from north eastern pacific polychaetes and nemerteans with descriptions of three novel species lecudina phyllochaetopteri sp nov difficilina tubulani sp nov and difficilina paranemertis sp nov
    International Journal of Systematic and Evolutionary Microbiology, 2010
    Co-Authors: Sonja Rueckert, Chitchai Chantangsi, Brian S Leander
    Abstract:

    Most eugregarine apicomplexans infecting the intestines of marine invertebrates have been described within the family Lecudinidae and the type genus Lecudina. The diversity of these parasites is vast and poorly understood and only a tiny number of species has been characterized at the molecular phylogenetic level. DNA sequences coupled with high-resolution micrographs of trophozoites provide an efficient and precise approach for delimiting gregarine lineages from one another and also facilitate our overall understanding of gregarine biodiversity. In this study, phylogenetic analyses of small subunit (SSU) rDNA sequences from five (uncultivated) Gregarines isolated from polychaetes and nemerteans in the North-eastern Pacific Ocean are presented. Lecudina phyllochaetopteri sp. nov. was isolated from the intestines of the parchment tubeworm Phyllochaetopterus prolifica (Polychaeta). Lecudina longissima and Lecudina polymorpha were both isolated from the intestines of Lumbrineris japonica (Polychaeta). Difficilina tubulani sp. nov. was isolated from the nemertean Tubulanus polymorpha and Difficilina paranemertis sp. nov. was isolated from the nemertean Paranemertes peregrina. This is the first report of molecular sequence data from Gregarines that infect nemerteans. The two novel species of the genus Difficilina described in this study formed a strongly supported clade in the phylogenetic analyses. This Difficilina clade formed the sister group to a robust subclade of lecudinids consisting of Lecudina longissima, Lecudina phyllochaetopteri sp. nov. (which lacked epicytic folds), Lecudina tuzetae, species of the genus Lankesteria and several sequences derived from previous environmental DNA surveys of marine biodiversity.

  • morphology and phylogenetic position of two novel marine Gregarines apicomplexa eugregarinorida from the intestines of north eastern pacific ascidians
    Zoologica Scripta, 2008
    Co-Authors: Sonja Rueckert, Brian S Leander
    Abstract:

    Eugregarine apicomplexans parasitize marine, freshwater and terrestrial invertebrates, and have lifecycles involving trophozoites (feeding stages) with complex morphologies and behaviour. The genus Lankesteria refers to marine aseptate euGregarines that parasitize ascidians. We described the surface ultrastructure of two new gregarine species, L helyosomae sp. n. and L. cystodytae sp. n. that inhabit the intestines of Chelyosoma columbianum and Cystodytes lobatus , respectively, collected from the North-eastern Pacific Ocean. Apart from inhabiting different hosts and major differences in the cell size of L. chelyosomae sp. n. (mean length 182 μ m) and L. cystodytae sp. n. (mean length 70 μ m), the morphology of both gregarine species was quite similar. The trophozoites ranged from elliptoid to obdeltoid in shape and were brownish in colour. The nucleus was situated at the anterior end of the cell just behind a pointed mucron. A dense array of epicytic knobs was present over the entire surface of trophozoites in both species, and longitudinal epicytical folds were only weakly developed. We also sequenced the small subunit rDNA from the Gregarines collected from both hosts, which supported the establishment of two new Lankesteria species. Phylogenetic analyses of the new DNA sequences and those derived from other alveolates, demonstrated that both new species clustered in a strongly supported clade consisting of other Lankesteria species, Lecudina species, and some environmental sequences. These morphological and molecular phylogenetic data suggested that improved knowledge of gregarine diversity could lead to the recognition of more than one distinct clade (genus) of Gregarines within ascidian hosts.

Timur G. Simdyanov - One of the best experts on this subject based on the ideXlab platform.

  • A new view on the morphology and phylogeny of euGregarines suggested by the evidence from the gregarine Ancora sagittata (Leuckart, 1860) Labbé, 1899 (Apicomplexa: Eugregarinida)
    PeerJ, 2017
    Co-Authors: Timur G. Simdyanov, Andrei Diakin, Laure Guillou, Kirill V. Mikhailov, Joseph Schrével, Vladimir V Aleoshin
    Abstract:

    Background: Gregarines are a group of early branching Apicomplexa parasitizing invertebrate animals. Despite their wide distribution and relevance to the understanding the phylogenesis of apicomplexans, Gregarines remain understudied: light microscopy data are insufficient for classification, and electron microscopy and molecular data are fragmentary and overlap only partially. Methods Scanning and transmission electron microscopy, PCR, DNA cloning and sequencing (Sanger and NGS), molecular phylogenetic analyses using ribosomal RNA genes (18S (SSU), 5.8S, and 28S (LSU) ribosomal DNAs (rDNAs)). Results and Discussion: We present the results of an ultrastructural and molecular phylogenetic study on the marine gregarine Ancora sagittata from the polychaete Capitella capitata followed by evolutionary and taxonomic synthesis of the morphological and molecular phylogenetic evidence on euGregarines. The ultrastructure of Ancora sagittata generally corresponds to that of other euGregarines, but reveals some differences in epicytic folds (crests) and attachment apparatus to Gregarines in the family Lecudinidae, where Ancora sagittata has been classified. Molecular phylogenetic trees based on SSU (18S) rDNA reveal several robust clades (superfamilies) of euGregarines, including Ancoroidea superfam. nov., which comprises two families (Ancoridae fam. nov. and Polyplicariidae) and branches separately from the Lecudinidae; thus, all representatives of Ancoroidea are here officially removed from the Lecudinidae. Analysis of sequence data also points to possible cryptic species within Ancora sagittata and the inclusion of numerous environmental sequences from anoxic habitats within the Ancoroidea. LSU (28S) rDNA phylogenies, unlike the analysis of SSU rDNA alone, recover a well-supported monophyly of the Gregarines involved (euGregarines), although this conclusion is currently limited by sparse taxon sampling and the presence of fast-evolving sequences in some species. Comparative morphological analyses of gregarine teguments and attachment organelles lead us to revise their terminology. The terms “longitudinal folds” and “mucron” are restricted to archiGregarines, whereas the terms “epicystic crests” and “epimerite” are proposed to describe the candidate synapomorphies of euGregarines, which, consequently, are considered as a monophyletic group. Abolishing the suborders Aseptata and Septata, incorporating neoGregarines into the Eugregarinida, and treating the major molecular phylogenetic lineages of euGregarines as superfamilies appear as the best way of reconciling recent morphological and molecular evidence. Accordingly, the diagnosis of the order Eugregarinida Léger, 1900 is updated.

  • different motility modes in marine Gregarines representing the early emerging group of apicomplexa
    2016
    Co-Authors: Magdaléna Kováčiková, Andrei Diakin, Gita G. Paskerova, Timur G. Simdyanov, Andrea Bardůnek Valigurová
    Abstract:

    The motility of apicomplexan invasive stages (zoites), facilitated by a mechanism of substrate-dependent gliding, was investigated in important human pathogens as an essential mechanism for parasites’ migration and host cell invasion. Gregarines represent a diversified group of ancestral apicomplexans, with diverse host-parasite interactions and modes of locomotion, mechanism of which differs from apicomplexans zoites. In our research, the so called pendular or rolling movement in archigregarine Selenidium sp. was investigated after the application of drugs inducing assembly or disassembly of actin filaments (jasplakinolide, cytochalasin D) and depolymerisation of microtubules (oryzalin, colchicine). Our study confirms the influence of microtubules depolymerising drugs on Selenidium sp. motility. Despite the evidence that movement was blocked, experiments also revealed prolonged survival (90 min - 9 h) of Gregarines in extremely high doses (10 micro M - 100 mM) of these probes. In SEM observation no superficial changes of Selenidium sp. surface were observed, while the evident changes in distribution of cytoskeletal proteins after CLSM analysis were documented. Moreover, the influence of changed ions concentration in artificial sea water on archigregarine (Selenidium sp.) and eugregarine (Polyrhabdina sp.) motility was investigated. Further experiments were performed with changed concentration of ions: Na+, K+, Mg2+ and Ca2+. Motility index was calculated in set time intervals for both species. Although no significant changes in Gregarines’ survival and motility were observed under the light microscope, Gregarines were fixed for ultrastructural analysis (TEM). Furthermore, the gliding motility was studied in marine eugregarine Cephaloidophora cf. communis. The unusually active and variable modes of motility (e.g. jumping and rotational movements with rapid changes in the gliding direction and cell flexions) are facilitated by architecture of parasite epicytic folds.

  • morphology and molecular phylogeny of coelomic Gregarines apicomplexa with different types of motility urospora ovalis and u travisiae from the polychaete travisia forbesii
    Protist, 2016
    Co-Authors: Andrei Diakin, Gita G. Paskerova, Timur G. Simdyanov, Vladimir V Aleoshin, Andrea Bardůnek Valigurová
    Abstract:

    Urosporids (Apicomplexa: Urosporidae) are euGregarines that parasitise marine invertebrates, such as annelids, molluscs, nemerteans and echinoderms, inhabiting their coelom and intestine. Urosporids exhibit considerable morphological plasticity, which correlates with their different modes of motility and variations in structure of their cortical zone, according to the localisation within the host. The Gregarines Urospora ovalis and U. travisiae from the marine polychaete Travisia forbesii were investigated with an emphasis on their general morphology and phylogenetic position. Solitary ovoid trophozoites and syzygies of U. ovalis were located free in the host coelom and showed metabolic activity, a non-progressive movement with periodic changes of the cell shape. Solitary trophozoites of U. travisiae, attached to the host tissue or free floating in the coelom, were V-shaped. Detached trophozoites demonstrated gliding motility, a progressive movement without observable cell body changes. In both Gregarines, the cortex formed numerous epicytic folds, but superfolds appeared exclusively on the surface of U. ovalis during metabolic activity. SSU rDNA sequences obtained from U. ovalis and U. travisiae revealed that they belong to the Lecudinoidea clade; however, they are not affiliated with other coelomic urosporids (Pterospora spp. and Lithocystis spp.), but surprisingly with intestinal lecudinids (Difficilina spp.) parasitising nemerteans.

  • ultrastructure and 28s rdna phylogeny of two Gregarines cephaloidophora cf communis and heliospora cf longissima with remarks on gregarine morphology and phylogenetic analysis
    Acta Protozoologica, 2015
    Co-Authors: Timur G. Simdyanov, Andrei Diakin, Vladimir V Aleoshin
    Abstract:

    S rRNA gene sequences (SSU rDNA) in Gregarines are problematic for phylogenetic analysis, mainly due to artifacts related to long branch attraction (LBA). In this study, we sequenced 18S rRNA (SSU rRNA), 5.8S rRNA, and 28S rRNA (LSU rRNA) genes of two gregarine species from crustacean hosts (gregarine superfamily Cephaloidophoroidea): Cephaloidophora cf. communis from a marine cirripedian Balanus balanus (White Sea), and Heliospora cf. longissima from the freshwater amphipods, Eulimnogammarus verrucosus and E. vittatus (Lake Baikal). Phylogenetic analyses of SSU rDNA sequences failed to produce a robust tree topology, for a limited taxon sample (31 operational taxonomic units (OTU), based on 1,604 sites), while LSU (2,869 sites), and concatenated dataset based on SSU, 5.8S, and LSU (4,627 sites) produced more consistent tree topologies for the same taxon sample. Analyses testing for LBA-influence were negative, therefore we suggested that the main reason of the failed topologies in SSU rDNA analyses is insufficient data (insufficient taxon sampling and limited molecular data), rather than LBA. Possible advantages of Bayesian analyses, compared to Maximum Likelihood, and usage of LSU rDNA within the context of apicomplexan phylogenetics were discussed. One of the advantages of LSU is likely its lower rate of evolution in long-branching apicomplexans (e.g., Gregarines), relative to other (non-long-branching) apicomplexans, compared to SSU rDNA. Ultrastructure of the epicytic folds was studied. There are 3 to 5 apical arcs (also known as rippled dense structures) and 2 to 5 apical filaments in the tops of the folds. This small number of the apical structures fits into morphological diversity of the epicyte in other Cephaloidophoroidea, but this is not a synapomorphy of the group because this was also detected in several unrelated Gregarines. C. cf. communis was found to contain a septum between the epimerite and the protomerite, which has not been reported in other Gregarines. More exact terminology, which takes into account number of body sections and septa, is proposed for morphological descriptions of trophozoites and free mature gamonts of Gregarines. In accordance with this, C. cf. communis gamonts are tricystid and biseptate, whereas H. cf. longis­ sima gamonts are tricystid and uniseptate, similar to other euGregarines.

  • protococcidian eleutheroschizon duboscqi an unusual apicomplexan interconnecting Gregarines and cryptosporidia
    PLOS ONE, 2015
    Co-Authors: Andrea Bardůnek Valigurová, Gita G. Paskerova, Andrei Diakin, Magdaléna Kováčiková, Timur G. Simdyanov
    Abstract:

    This study focused on the attachment strategy, cell structure and the host-parasite interactions of the protococcidian Eleutheroschizon duboscqi, parasitising the polychaete Scoloplos armiger. The attached trophozoites and gamonts of E. duboscqi were detected at different development stages. The parasite develops epicellularly, covered by a host cell-derived, two-membrane parasitophorous sac forming a caudal tipped appendage. Staining with Evans blue suggests that this tail is protein-rich, supported by the presence of a fibrous substance in this area. Despite the ultrastructural evidence for long filaments in the tail, it stained only weakly for F-actin, while spectrin seemed to accumulate in this area. The attachment apparatus consists of lobes arranged in one (trophozoites) or two (gamonts) circles, crowned by a ring of filamentous fascicles. During trophozoite maturation, the internal space between the parasitophorous sac and parasite turns translucent, the parasite trilaminar pellicle seems to reorganise and is covered by a dense fibrous glycocalyx. The parasite surface is organised in broad folds with grooves in between. Micropores are situated at the bottom of the grooves. A layer of filaments organised in bands, underlying the folds and ending above the attachment fascicles, was detected just beneath the pellicle. Confocal microscopy, along with the application of cytoskeletal drugs (jasplakinolide, cytochalasin D, oryzalin) confirmed the presence of actin and tubulin polymerised forms in both the parasitophorous sac and the parasite, while myosin labelling was restricted to the sac. Despite positive tubulin labelling, no microtubules were detected in mature stages. The attachment strategy of E. duboscqi shares features with that of cryptosporidia and Gregarines, i.e. the parasite itself conspicuously resembles an epicellularly located gregarine, while the parasitophorous sac develops in a similar manner to that in cryptosporidia. This study provides a re-evaluation of epicellular development in other apicomplexans and directly compares their niche with that of E. duboscqi.

Vladimir V Aleoshin - One of the best experts on this subject based on the ideXlab platform.

  • A new view on the morphology and phylogeny of euGregarines suggested by the evidence from the gregarine Ancora sagittata (Leuckart, 1860) Labbé, 1899 (Apicomplexa: Eugregarinida)
    PeerJ, 2017
    Co-Authors: Timur G. Simdyanov, Andrei Diakin, Laure Guillou, Kirill V. Mikhailov, Joseph Schrével, Vladimir V Aleoshin
    Abstract:

    Background: Gregarines are a group of early branching Apicomplexa parasitizing invertebrate animals. Despite their wide distribution and relevance to the understanding the phylogenesis of apicomplexans, Gregarines remain understudied: light microscopy data are insufficient for classification, and electron microscopy and molecular data are fragmentary and overlap only partially. Methods Scanning and transmission electron microscopy, PCR, DNA cloning and sequencing (Sanger and NGS), molecular phylogenetic analyses using ribosomal RNA genes (18S (SSU), 5.8S, and 28S (LSU) ribosomal DNAs (rDNAs)). Results and Discussion: We present the results of an ultrastructural and molecular phylogenetic study on the marine gregarine Ancora sagittata from the polychaete Capitella capitata followed by evolutionary and taxonomic synthesis of the morphological and molecular phylogenetic evidence on euGregarines. The ultrastructure of Ancora sagittata generally corresponds to that of other euGregarines, but reveals some differences in epicytic folds (crests) and attachment apparatus to Gregarines in the family Lecudinidae, where Ancora sagittata has been classified. Molecular phylogenetic trees based on SSU (18S) rDNA reveal several robust clades (superfamilies) of euGregarines, including Ancoroidea superfam. nov., which comprises two families (Ancoridae fam. nov. and Polyplicariidae) and branches separately from the Lecudinidae; thus, all representatives of Ancoroidea are here officially removed from the Lecudinidae. Analysis of sequence data also points to possible cryptic species within Ancora sagittata and the inclusion of numerous environmental sequences from anoxic habitats within the Ancoroidea. LSU (28S) rDNA phylogenies, unlike the analysis of SSU rDNA alone, recover a well-supported monophyly of the Gregarines involved (euGregarines), although this conclusion is currently limited by sparse taxon sampling and the presence of fast-evolving sequences in some species. Comparative morphological analyses of gregarine teguments and attachment organelles lead us to revise their terminology. The terms “longitudinal folds” and “mucron” are restricted to archiGregarines, whereas the terms “epicystic crests” and “epimerite” are proposed to describe the candidate synapomorphies of euGregarines, which, consequently, are considered as a monophyletic group. Abolishing the suborders Aseptata and Septata, incorporating neoGregarines into the Eugregarinida, and treating the major molecular phylogenetic lineages of euGregarines as superfamilies appear as the best way of reconciling recent morphological and molecular evidence. Accordingly, the diagnosis of the order Eugregarinida Léger, 1900 is updated.

  • morphology and molecular phylogeny of coelomic Gregarines apicomplexa with different types of motility urospora ovalis and u travisiae from the polychaete travisia forbesii
    Protist, 2016
    Co-Authors: Andrei Diakin, Gita G. Paskerova, Timur G. Simdyanov, Vladimir V Aleoshin, Andrea Bardůnek Valigurová
    Abstract:

    Urosporids (Apicomplexa: Urosporidae) are euGregarines that parasitise marine invertebrates, such as annelids, molluscs, nemerteans and echinoderms, inhabiting their coelom and intestine. Urosporids exhibit considerable morphological plasticity, which correlates with their different modes of motility and variations in structure of their cortical zone, according to the localisation within the host. The Gregarines Urospora ovalis and U. travisiae from the marine polychaete Travisia forbesii were investigated with an emphasis on their general morphology and phylogenetic position. Solitary ovoid trophozoites and syzygies of U. ovalis were located free in the host coelom and showed metabolic activity, a non-progressive movement with periodic changes of the cell shape. Solitary trophozoites of U. travisiae, attached to the host tissue or free floating in the coelom, were V-shaped. Detached trophozoites demonstrated gliding motility, a progressive movement without observable cell body changes. In both Gregarines, the cortex formed numerous epicytic folds, but superfolds appeared exclusively on the surface of U. ovalis during metabolic activity. SSU rDNA sequences obtained from U. ovalis and U. travisiae revealed that they belong to the Lecudinoidea clade; however, they are not affiliated with other coelomic urosporids (Pterospora spp. and Lithocystis spp.), but surprisingly with intestinal lecudinids (Difficilina spp.) parasitising nemerteans.

  • ultrastructure and 28s rdna phylogeny of two Gregarines cephaloidophora cf communis and heliospora cf longissima with remarks on gregarine morphology and phylogenetic analysis
    Acta Protozoologica, 2015
    Co-Authors: Timur G. Simdyanov, Andrei Diakin, Vladimir V Aleoshin
    Abstract:

    S rRNA gene sequences (SSU rDNA) in Gregarines are problematic for phylogenetic analysis, mainly due to artifacts related to long branch attraction (LBA). In this study, we sequenced 18S rRNA (SSU rRNA), 5.8S rRNA, and 28S rRNA (LSU rRNA) genes of two gregarine species from crustacean hosts (gregarine superfamily Cephaloidophoroidea): Cephaloidophora cf. communis from a marine cirripedian Balanus balanus (White Sea), and Heliospora cf. longissima from the freshwater amphipods, Eulimnogammarus verrucosus and E. vittatus (Lake Baikal). Phylogenetic analyses of SSU rDNA sequences failed to produce a robust tree topology, for a limited taxon sample (31 operational taxonomic units (OTU), based on 1,604 sites), while LSU (2,869 sites), and concatenated dataset based on SSU, 5.8S, and LSU (4,627 sites) produced more consistent tree topologies for the same taxon sample. Analyses testing for LBA-influence were negative, therefore we suggested that the main reason of the failed topologies in SSU rDNA analyses is insufficient data (insufficient taxon sampling and limited molecular data), rather than LBA. Possible advantages of Bayesian analyses, compared to Maximum Likelihood, and usage of LSU rDNA within the context of apicomplexan phylogenetics were discussed. One of the advantages of LSU is likely its lower rate of evolution in long-branching apicomplexans (e.g., Gregarines), relative to other (non-long-branching) apicomplexans, compared to SSU rDNA. Ultrastructure of the epicytic folds was studied. There are 3 to 5 apical arcs (also known as rippled dense structures) and 2 to 5 apical filaments in the tops of the folds. This small number of the apical structures fits into morphological diversity of the epicyte in other Cephaloidophoroidea, but this is not a synapomorphy of the group because this was also detected in several unrelated Gregarines. C. cf. communis was found to contain a septum between the epimerite and the protomerite, which has not been reported in other Gregarines. More exact terminology, which takes into account number of body sections and septa, is proposed for morphological descriptions of trophozoites and free mature gamonts of Gregarines. In accordance with this, C. cf. communis gamonts are tricystid and biseptate, whereas H. cf. longis­ sima gamonts are tricystid and uniseptate, similar to other euGregarines.

  • identification of a divergent environmental dna sequence clade using the phylogeny of gregarine parasites apicomplexa from crustacean hosts
    PLOS ONE, 2011
    Co-Authors: Timur G. Simdyanov, Sonja Rueckert, Vladimir V Aleoshin, Brian S Leander
    Abstract:

    Background Environmental SSU rDNA surveys have significantly improved our understanding of microeukaryotic diversity. Many of the sequences acquired using this approach are closely related to lineages previously characterized at both morphological and molecular levels, making interpretation of these data relatively straightforward. Some sequences, by contrast, appear to be phylogenetic orphans and are sometimes inferred to represent “novel lineages” of unknown cellular identity. Consequently, interpretation of environmental DNA surveys of cellular diversity rely on an adequately comprehensive database of DNA sequences derived from identified species. Several major taxa of microeukaryotes, however, are still very poorly represented in these databases, and this is especially true for diverse groups of single-celled parasites, such as gregarine apicomplexans. Methodology/Principal Findings This study attempts to address this paucity of DNA sequence data by characterizing four different gregarine species, isolated from the intestines of crustaceans, at both morphological and molecular levels: Thiriotia pugettiae sp. n. from the graceful kelp crab (Pugettia gracilis), Cephaloidophora cf. communis from two different species of barnacles (Balanus glandula and B. balanus), Heliospora cf. longissima from two different species of freshwater amphipods (Eulimnogammarus verrucosus and E. vittatus), and Heliospora caprellae comb. n. from a skeleton shrimp (Caprella alaskana). SSU rDNA sequences were acquired from isolates of these gregarine species and added to a global apicomplexan alignment containing all major groups of Gregarines characterized so far. Molecular phylogenetic analyses of these data demonstrated that all of the Gregarines collected from crustacean hosts formed a very strongly supported clade with 48 previously unidentified environmental DNA sequences. Conclusions/Significance This expanded molecular phylogenetic context enabled us to establish a major clade of intestinal gregarine parasites and infer the cellular identities of several previously unidentified environmental SSU rDNA sequences, including several sequences that have formerly been discussed broadly in the literature as a suspected “novel” lineage of eukaryotes

Sonja Rueckert - One of the best experts on this subject based on the ideXlab platform.

  • the symbiotic spectrum where do the Gregarines fit
    Trends in Parasitology, 2019
    Co-Authors: Sonja Rueckert, Emma L Betts, Anastasios D Tsaousis
    Abstract:

    Gregarine apicomplexans are closely related to parasites such as Plasmodium, Toxoplasma, and Cryptosporidium, which are causing severe health and economic burdens. Colonizing only invertebrates and having no obvious medical relevance, they are mostly ignored in ‘omics’ studies, although Gregarines are the most basal apicomplexans and therefore key players in the understanding of the evolution of parasitism in the Apicomplexa from free-living ancestors. They belong to the largest exclusively parasitic phylum, but is this perception actually true? The effects of Gregarines on their hosts seem to cover the whole spectrum of symbiosis from mutualistic to parasitic. We suggest future research directions to understand the evolutionary role of Gregarines, by elucidating their biology and interaction with their hosts and the hosts’ microbiota.

  • morphology and molecular systematic of marine Gregarines apicomplexa from southwestern atlantic spionid polychaetes
    Journal of Invertebrate Pathology, 2018
    Co-Authors: Sonja Rueckert, Natusha Irina Glasinovich, Maria Emilia Diez, Florencia Cremonte, Nuria Natalia Vazquez
    Abstract:

    Abstract Gregarines are a common group of parasites that infect the intestines of marine invertebrates, and particularly polychaetes. Here, we describe for the first time four gregarine species that inhabit the intestines of three spionid species: Dipolydora cf. flava, Spio quadrisetosa and Boccardia proboscidea from the Patagonian coast, Argentina, using light and scanning electron microscopy and molecular phylogenetic analyses of small subunit (SSU) rDNA sequences. Even though the spionid species thrive in the same environments, our results showed a high host specificity of the gregarine species. Selenidium cf. axiferens and Polyrhabdina aff. polydorae were both identified from the intestine of D. cf. flava. The new species, Polyrhabdina madrynense sp. n. and Selenidium patagonica sp. n., were described from the intestines of S. quadrisetosa and the invasive species B. proboscidea, respectively. All specimens of D. cf. flava and S. quadrisetosa were infected by Gregarines (P = 100%), recording the highest mean intensity values of infection (MI = 80; 60 respectively), in contrast to B. proboscidea (P = 60%; MI = 38). We associated this finding with the recent invasion of this host. It is expected that in the future, an increase of its population density might favour a rising intensity of this gregarine infection.

  • Gregarines apicomplexa gregarinasina in psocids insecta psocoptera including a new species description and their potential use as pest control agents
    European Journal of Protistology, 2017
    Co-Authors: Sonja Rueckert, Dusan Devetak
    Abstract:

    Gregarine apicomplexans are unicellular organisms that infect invertebrate hosts in marine, freshwater and terrestrial habitats. The largest group of invertebrates infested on land is the insects. The insect order Psocoptera (booklice) has recently gained wider interest due to specimens occurring in stored food products and therefore being considered pest organisms. Biological control agents are often used to eliminate pest organisms. In this study we examined the psocid Dorypteryx domestica, an invasive psocid species that is spreading all over the world. We were able to isolate and describe a new gregarine species (Enterocystis dorypterygis sp. n.) infecting D. domestica. The trophozoites are panduri- or pyriform and their association/syzygy is caudo-frontal. The surface is inscribed by longitudinal epicytic folds covering the complete cell. Phylogenetic analyses of the SSU rDNA gene revealed an only weakly supported relationship with two Gregarina species G. ormieri and G. basiconstrictonea, both from tenebrionid beetles. Gregarines have been proposed to have some potential as biological control agents for several insects. Identifying the gregarine species infecting pest organisms like psocids is a first step and prerequisite for the probable utilization of these parasites as biological control agents in the future.

  • identification of a divergent environmental dna sequence clade using the phylogeny of gregarine parasites apicomplexa from crustacean hosts
    PLOS ONE, 2011
    Co-Authors: Timur G. Simdyanov, Sonja Rueckert, Vladimir V Aleoshin, Brian S Leander
    Abstract:

    Background Environmental SSU rDNA surveys have significantly improved our understanding of microeukaryotic diversity. Many of the sequences acquired using this approach are closely related to lineages previously characterized at both morphological and molecular levels, making interpretation of these data relatively straightforward. Some sequences, by contrast, appear to be phylogenetic orphans and are sometimes inferred to represent “novel lineages” of unknown cellular identity. Consequently, interpretation of environmental DNA surveys of cellular diversity rely on an adequately comprehensive database of DNA sequences derived from identified species. Several major taxa of microeukaryotes, however, are still very poorly represented in these databases, and this is especially true for diverse groups of single-celled parasites, such as gregarine apicomplexans. Methodology/Principal Findings This study attempts to address this paucity of DNA sequence data by characterizing four different gregarine species, isolated from the intestines of crustaceans, at both morphological and molecular levels: Thiriotia pugettiae sp. n. from the graceful kelp crab (Pugettia gracilis), Cephaloidophora cf. communis from two different species of barnacles (Balanus glandula and B. balanus), Heliospora cf. longissima from two different species of freshwater amphipods (Eulimnogammarus verrucosus and E. vittatus), and Heliospora caprellae comb. n. from a skeleton shrimp (Caprella alaskana). SSU rDNA sequences were acquired from isolates of these gregarine species and added to a global apicomplexan alignment containing all major groups of Gregarines characterized so far. Molecular phylogenetic analyses of these data demonstrated that all of the Gregarines collected from crustacean hosts formed a very strongly supported clade with 48 previously unidentified environmental DNA sequences. Conclusions/Significance This expanded molecular phylogenetic context enabled us to establish a major clade of intestinal gregarine parasites and infer the cellular identities of several previously unidentified environmental SSU rDNA sequences, including several sequences that have formerly been discussed broadly in the literature as a suspected “novel” lineage of eukaryotes

  • molecular systematics of marine Gregarines apicomplexa from north eastern pacific polychaetes and nemerteans with descriptions of three novel species lecudina phyllochaetopteri sp nov difficilina tubulani sp nov and difficilina paranemertis sp nov
    International Journal of Systematic and Evolutionary Microbiology, 2010
    Co-Authors: Sonja Rueckert, Chitchai Chantangsi, Brian S Leander
    Abstract:

    Most eugregarine apicomplexans infecting the intestines of marine invertebrates have been described within the family Lecudinidae and the type genus Lecudina. The diversity of these parasites is vast and poorly understood and only a tiny number of species has been characterized at the molecular phylogenetic level. DNA sequences coupled with high-resolution micrographs of trophozoites provide an efficient and precise approach for delimiting gregarine lineages from one another and also facilitate our overall understanding of gregarine biodiversity. In this study, phylogenetic analyses of small subunit (SSU) rDNA sequences from five (uncultivated) Gregarines isolated from polychaetes and nemerteans in the North-eastern Pacific Ocean are presented. Lecudina phyllochaetopteri sp. nov. was isolated from the intestines of the parchment tubeworm Phyllochaetopterus prolifica (Polychaeta). Lecudina longissima and Lecudina polymorpha were both isolated from the intestines of Lumbrineris japonica (Polychaeta). Difficilina tubulani sp. nov. was isolated from the nemertean Tubulanus polymorpha and Difficilina paranemertis sp. nov. was isolated from the nemertean Paranemertes peregrina. This is the first report of molecular sequence data from Gregarines that infect nemerteans. The two novel species of the genus Difficilina described in this study formed a strongly supported clade in the phylogenetic analyses. This Difficilina clade formed the sister group to a robust subclade of lecudinids consisting of Lecudina longissima, Lecudina phyllochaetopteri sp. nov. (which lacked epicytic folds), Lecudina tuzetae, species of the genus Lankesteria and several sequences derived from previous environmental DNA surveys of marine biodiversity.

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  • A new view on the morphology and phylogeny of euGregarines suggested by the evidence from the gregarine Ancora sagittata (Leuckart, 1860) Labbé, 1899 (Apicomplexa: Eugregarinida)
    PeerJ, 2017
    Co-Authors: Timur G. Simdyanov, Andrei Diakin, Laure Guillou, Kirill V. Mikhailov, Joseph Schrével, Vladimir V Aleoshin
    Abstract:

    Background: Gregarines are a group of early branching Apicomplexa parasitizing invertebrate animals. Despite their wide distribution and relevance to the understanding the phylogenesis of apicomplexans, Gregarines remain understudied: light microscopy data are insufficient for classification, and electron microscopy and molecular data are fragmentary and overlap only partially. Methods Scanning and transmission electron microscopy, PCR, DNA cloning and sequencing (Sanger and NGS), molecular phylogenetic analyses using ribosomal RNA genes (18S (SSU), 5.8S, and 28S (LSU) ribosomal DNAs (rDNAs)). Results and Discussion: We present the results of an ultrastructural and molecular phylogenetic study on the marine gregarine Ancora sagittata from the polychaete Capitella capitata followed by evolutionary and taxonomic synthesis of the morphological and molecular phylogenetic evidence on euGregarines. The ultrastructure of Ancora sagittata generally corresponds to that of other euGregarines, but reveals some differences in epicytic folds (crests) and attachment apparatus to Gregarines in the family Lecudinidae, where Ancora sagittata has been classified. Molecular phylogenetic trees based on SSU (18S) rDNA reveal several robust clades (superfamilies) of euGregarines, including Ancoroidea superfam. nov., which comprises two families (Ancoridae fam. nov. and Polyplicariidae) and branches separately from the Lecudinidae; thus, all representatives of Ancoroidea are here officially removed from the Lecudinidae. Analysis of sequence data also points to possible cryptic species within Ancora sagittata and the inclusion of numerous environmental sequences from anoxic habitats within the Ancoroidea. LSU (28S) rDNA phylogenies, unlike the analysis of SSU rDNA alone, recover a well-supported monophyly of the Gregarines involved (euGregarines), although this conclusion is currently limited by sparse taxon sampling and the presence of fast-evolving sequences in some species. Comparative morphological analyses of gregarine teguments and attachment organelles lead us to revise their terminology. The terms “longitudinal folds” and “mucron” are restricted to archiGregarines, whereas the terms “epicystic crests” and “epimerite” are proposed to describe the candidate synapomorphies of euGregarines, which, consequently, are considered as a monophyletic group. Abolishing the suborders Aseptata and Septata, incorporating neoGregarines into the Eugregarinida, and treating the major molecular phylogenetic lineages of euGregarines as superfamilies appear as the best way of reconciling recent morphological and molecular evidence. Accordingly, the diagnosis of the order Eugregarinida Léger, 1900 is updated.

  • different motility modes in marine Gregarines representing the early emerging group of apicomplexa
    2016
    Co-Authors: Magdaléna Kováčiková, Andrei Diakin, Gita G. Paskerova, Timur G. Simdyanov, Andrea Bardůnek Valigurová
    Abstract:

    The motility of apicomplexan invasive stages (zoites), facilitated by a mechanism of substrate-dependent gliding, was investigated in important human pathogens as an essential mechanism for parasites’ migration and host cell invasion. Gregarines represent a diversified group of ancestral apicomplexans, with diverse host-parasite interactions and modes of locomotion, mechanism of which differs from apicomplexans zoites. In our research, the so called pendular or rolling movement in archigregarine Selenidium sp. was investigated after the application of drugs inducing assembly or disassembly of actin filaments (jasplakinolide, cytochalasin D) and depolymerisation of microtubules (oryzalin, colchicine). Our study confirms the influence of microtubules depolymerising drugs on Selenidium sp. motility. Despite the evidence that movement was blocked, experiments also revealed prolonged survival (90 min - 9 h) of Gregarines in extremely high doses (10 micro M - 100 mM) of these probes. In SEM observation no superficial changes of Selenidium sp. surface were observed, while the evident changes in distribution of cytoskeletal proteins after CLSM analysis were documented. Moreover, the influence of changed ions concentration in artificial sea water on archigregarine (Selenidium sp.) and eugregarine (Polyrhabdina sp.) motility was investigated. Further experiments were performed with changed concentration of ions: Na+, K+, Mg2+ and Ca2+. Motility index was calculated in set time intervals for both species. Although no significant changes in Gregarines’ survival and motility were observed under the light microscope, Gregarines were fixed for ultrastructural analysis (TEM). Furthermore, the gliding motility was studied in marine eugregarine Cephaloidophora cf. communis. The unusually active and variable modes of motility (e.g. jumping and rotational movements with rapid changes in the gliding direction and cell flexions) are facilitated by architecture of parasite epicytic folds.

  • morphology and molecular phylogeny of coelomic Gregarines apicomplexa with different types of motility urospora ovalis and u travisiae from the polychaete travisia forbesii
    Protist, 2016
    Co-Authors: Andrei Diakin, Gita G. Paskerova, Timur G. Simdyanov, Vladimir V Aleoshin, Andrea Bardůnek Valigurová
    Abstract:

    Urosporids (Apicomplexa: Urosporidae) are euGregarines that parasitise marine invertebrates, such as annelids, molluscs, nemerteans and echinoderms, inhabiting their coelom and intestine. Urosporids exhibit considerable morphological plasticity, which correlates with their different modes of motility and variations in structure of their cortical zone, according to the localisation within the host. The Gregarines Urospora ovalis and U. travisiae from the marine polychaete Travisia forbesii were investigated with an emphasis on their general morphology and phylogenetic position. Solitary ovoid trophozoites and syzygies of U. ovalis were located free in the host coelom and showed metabolic activity, a non-progressive movement with periodic changes of the cell shape. Solitary trophozoites of U. travisiae, attached to the host tissue or free floating in the coelom, were V-shaped. Detached trophozoites demonstrated gliding motility, a progressive movement without observable cell body changes. In both Gregarines, the cortex formed numerous epicytic folds, but superfolds appeared exclusively on the surface of U. ovalis during metabolic activity. SSU rDNA sequences obtained from U. ovalis and U. travisiae revealed that they belong to the Lecudinoidea clade; however, they are not affiliated with other coelomic urosporids (Pterospora spp. and Lithocystis spp.), but surprisingly with intestinal lecudinids (Difficilina spp.) parasitising nemerteans.

  • ultrastructure and 28s rdna phylogeny of two Gregarines cephaloidophora cf communis and heliospora cf longissima with remarks on gregarine morphology and phylogenetic analysis
    Acta Protozoologica, 2015
    Co-Authors: Timur G. Simdyanov, Andrei Diakin, Vladimir V Aleoshin
    Abstract:

    S rRNA gene sequences (SSU rDNA) in Gregarines are problematic for phylogenetic analysis, mainly due to artifacts related to long branch attraction (LBA). In this study, we sequenced 18S rRNA (SSU rRNA), 5.8S rRNA, and 28S rRNA (LSU rRNA) genes of two gregarine species from crustacean hosts (gregarine superfamily Cephaloidophoroidea): Cephaloidophora cf. communis from a marine cirripedian Balanus balanus (White Sea), and Heliospora cf. longissima from the freshwater amphipods, Eulimnogammarus verrucosus and E. vittatus (Lake Baikal). Phylogenetic analyses of SSU rDNA sequences failed to produce a robust tree topology, for a limited taxon sample (31 operational taxonomic units (OTU), based on 1,604 sites), while LSU (2,869 sites), and concatenated dataset based on SSU, 5.8S, and LSU (4,627 sites) produced more consistent tree topologies for the same taxon sample. Analyses testing for LBA-influence were negative, therefore we suggested that the main reason of the failed topologies in SSU rDNA analyses is insufficient data (insufficient taxon sampling and limited molecular data), rather than LBA. Possible advantages of Bayesian analyses, compared to Maximum Likelihood, and usage of LSU rDNA within the context of apicomplexan phylogenetics were discussed. One of the advantages of LSU is likely its lower rate of evolution in long-branching apicomplexans (e.g., Gregarines), relative to other (non-long-branching) apicomplexans, compared to SSU rDNA. Ultrastructure of the epicytic folds was studied. There are 3 to 5 apical arcs (also known as rippled dense structures) and 2 to 5 apical filaments in the tops of the folds. This small number of the apical structures fits into morphological diversity of the epicyte in other Cephaloidophoroidea, but this is not a synapomorphy of the group because this was also detected in several unrelated Gregarines. C. cf. communis was found to contain a septum between the epimerite and the protomerite, which has not been reported in other Gregarines. More exact terminology, which takes into account number of body sections and septa, is proposed for morphological descriptions of trophozoites and free mature gamonts of Gregarines. In accordance with this, C. cf. communis gamonts are tricystid and biseptate, whereas H. cf. longis­ sima gamonts are tricystid and uniseptate, similar to other euGregarines.

  • protococcidian eleutheroschizon duboscqi an unusual apicomplexan interconnecting Gregarines and cryptosporidia
    PLOS ONE, 2015
    Co-Authors: Andrea Bardůnek Valigurová, Gita G. Paskerova, Andrei Diakin, Magdaléna Kováčiková, Timur G. Simdyanov
    Abstract:

    This study focused on the attachment strategy, cell structure and the host-parasite interactions of the protococcidian Eleutheroschizon duboscqi, parasitising the polychaete Scoloplos armiger. The attached trophozoites and gamonts of E. duboscqi were detected at different development stages. The parasite develops epicellularly, covered by a host cell-derived, two-membrane parasitophorous sac forming a caudal tipped appendage. Staining with Evans blue suggests that this tail is protein-rich, supported by the presence of a fibrous substance in this area. Despite the ultrastructural evidence for long filaments in the tail, it stained only weakly for F-actin, while spectrin seemed to accumulate in this area. The attachment apparatus consists of lobes arranged in one (trophozoites) or two (gamonts) circles, crowned by a ring of filamentous fascicles. During trophozoite maturation, the internal space between the parasitophorous sac and parasite turns translucent, the parasite trilaminar pellicle seems to reorganise and is covered by a dense fibrous glycocalyx. The parasite surface is organised in broad folds with grooves in between. Micropores are situated at the bottom of the grooves. A layer of filaments organised in bands, underlying the folds and ending above the attachment fascicles, was detected just beneath the pellicle. Confocal microscopy, along with the application of cytoskeletal drugs (jasplakinolide, cytochalasin D, oryzalin) confirmed the presence of actin and tubulin polymerised forms in both the parasitophorous sac and the parasite, while myosin labelling was restricted to the sac. Despite positive tubulin labelling, no microtubules were detected in mature stages. The attachment strategy of E. duboscqi shares features with that of cryptosporidia and Gregarines, i.e. the parasite itself conspicuously resembles an epicellularly located gregarine, while the parasitophorous sac develops in a similar manner to that in cryptosporidia. This study provides a re-evaluation of epicellular development in other apicomplexans and directly compares their niche with that of E. duboscqi.

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