scholarly journals The myxozoan minicollagen gene repertoire was not simplified by the parasitic lifestyle: computational identification of a novel myxozoan minicollagen gene

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Jiří Kyslík ◽  
Anush Kosakyan ◽  
Serafim Nenarokov ◽  
Astrid S. Holzer ◽  
Ivan Fiala

Abstract Background Lineage-specific gene expansions represent one of the driving forces in the evolutionary dynamics of unique phylum traits. Myxozoa, a cnidarian subphylum of obligate parasites, are evolutionarily altered and highly reduced organisms with a simple body plan including cnidarian-specific organelles and polar capsules (a type of nematocyst). Minicollagens, a group of structural proteins, are prominent constituents of nematocysts linking Myxozoa and Cnidaria. Despite recent advances in the identification of minicollagens in Myxozoa, the evolutionary history and diversity of minicollagens in Myxozoa and Cnidaria remain elusive. Results We generated new transcriptomes of two myxozoan species using a novel pipeline for filtering of closely related contaminant species in RNA-seq data. Mining of our transcriptomes and published omics data confirmed the existence of myxozoan Ncol-4, reported only once previously, and revealed a novel noncanonical minicollagen, Ncol-5, which is exclusive to Myxozoa. Phylogenetic analyses support a close relationship between myxozoan Ncol-1–3 with minicollagens of Polypodium hydriforme, but suggest independent evolution in the case of the myxozoan minicollagens Ncol-4 and Ncol-5. Additional genome- and transcriptome-wide searches of cnidarian minicollagens expanded the dataset to better clarify the evolutionary trajectories of minicollagen. Conclusions The development of a new approach for the handling of next-generation data contaminated by closely related species represents a useful tool for future applications beyond the field of myxozoan research. This data processing pipeline allowed us to expand the dataset and study the evolution and diversity of minicollagen genes in Myxozoa and Cnidaria. We identified a novel type of minicollagen in Myxozoa (Ncol-5). We suggest that the large number of minicollagen paralogs in some cnidarians is a result of several recent large gene multiplication events. We revealed close juxtaposition of minicollagens Ncol-1 and Ncol-4 in myxozoan genomes, suggesting their common evolutionary history. The unique gene structure of myxozoan Ncol-5 suggests a specific function in the myxozoan polar capsule or tubule. Despite the fact that myxozoans possess only one type of nematocyst, their gene repertoire is similar to those of other cnidarians.

2020 ◽  
Author(s):  
Jiří Kyslík ◽  
Anush Kosakyan ◽  
Serafim Nenarokov ◽  
Astrid S. Holzer ◽  
Ivan Fiala

Abstract BackgroundLineage-specific gene expansions represent one of the driving forces in the evolutionary dynamics of unique phylum traits. The obligate parasitic group of Cnidaria, Myxozoa, are evolutionarily altered and highly reduced organisms with a simple body plan including cnidarian-specific organelles, polar capsules (a type of nematocyst). A prominent constituent of nematocysts, linking Myxozoa and Cnidaria, represents a group of structural proteins, minicollagens. Despite recent advances in the identification of minicollagens in Myxozoa, the evolutionary history and diversity of minicollagens in Myxozoa and Cnidaria remain elusive. ResultsWe present newly generated transcriptomes of two myxozoan species with a novel pipeline for filtering of closely related contaminant species in RNA-seq data. Mining of the set of our transcriptomes and published -omics data confirmed the existence of myxozoan Ncol-4, once only reported, and we discovered a novel non-canonical type of minicollagen, Ncol-5, which is exclusive to Myxozoa. Phylogenetic analyses support a close relationship of myxozoan Ncol-1,2,3 with minicollagens of Polypodium hydriforme, however, suggest rather independent evolution in the case of two myxozoan minicollagens Ncol-4 and Ncol-5. Additional genome- and transcriptome-wide searches of cnidarian minicollagens expand the dataset to clarify better minicollagen evolutionary trajectories. ConclusionsThe development of a new approach for the handling of contaminated next-generation data by closely related species represents a useful tool for future applications not only in the field of myxozoan research. This pipeline of data processing allowed us to expand the dataset and study the evolution and diversity of minicollagen gene family in Myxozoa and Cnidaria. We identified a novel type of minicollagen in Myxozoa (Ncol-5). We suggest that a high number of minicollagen paralogs in some cnidarians is a result of several recent large gene multiplication events. We revealed a close localization of minicollagens Ncol-1 and Ncol-4 in myxozoan genomes suggesting their common evolutionary history. The unique gene structure of myxozoan Ncol-5 may indicate a putative specific function in the myxozoan polar capsule or tubule. The range of myxozoan minicollagens proves that the myxozoan minicollagen gene repertoire is similar to other cnidarians and is not simplified by the parasitic lifestyle.


2021 ◽  
Vol 4 (1) ◽  
Author(s):  
E. Hekkala ◽  
J. Gatesy ◽  
A. Narechania ◽  
R. Meredith ◽  
M. Russello ◽  
...  

AbstractAncient DNA is transforming our ability to reconstruct historical patterns and mechanisms shaping modern diversity and distributions. In particular, molecular data from extinct Holocene island faunas have revealed surprising biogeographic scenarios. Here, we recovered partial mitochondrial (mt) genomes for 1300–1400 year old specimens (n = 2) of the extinct “horned” crocodile, Voay robustus, collected from Holocene deposits in southwestern Madagascar. Phylogenetic analyses of partial mt genomes and tip-dated timetrees based on molecular, fossil, and stratigraphic data favor a sister group relationship between Voay and Crocodylus (true crocodiles). These well supported trees conflict with recent morphological systematic work that has consistently placed Voay within Osteolaeminae (dwarf crocodiles and kin) and provide evidence for likely homoplasy in crocodylian cranial anatomy and snout shape. The close relationship between Voay and Crocodylus lends additional context for understanding the biogeographic origins of these genera and refines competing hypotheses for the recent extinction of Voay from Madagascar.


PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e11208
Author(s):  
Ashlie Hartigan ◽  
Adrian Jaimes-Becerra ◽  
Beth Okamura ◽  
Liam B. Doonan ◽  
Malcolm Ward ◽  
...  

Cnidarians are the oldest lineage of venomous animals and use nematocysts to discharge toxins. Whether venom toxins have been recruited to support parasitic lifestyles in the Endocnidozoa (Myxozoa + Polypodium) is, however, unknown. To examine this issue we variously employed transcriptomic, proteomic, associated molecular phylogenies, and localisation studies on representative primitive and derived myxozoans (Malacosporea and Myxosporea, respectively), Polypodium hydriforme, and the free-living staurozoan Calvadosia cruxmelitensis. Our transcriptomics and proteomics analyses provide evidence for expression and translation of venom toxin homologs in myxozoans. Phylogenetic placement of Kunitz type serine protease inhibitors and phospholipase A2 enzymes reveals modification of toxins inherited from ancestral free-living cnidarian toxins, and that venom diversity is reduced in myxozoans concordant with their reduced genome sizes. Various phylogenetic analyses of the Kunitz-type toxin family in Endocnidozoa suggested lineage-specific gene duplications, which offers a possible mechanism for enhancing toxin diversification. Toxin localisation in the malacosporean Buddenbrockia plumatellae substantiates toxin translation and thus illustrates a repurposing of toxin function for endoparasite development and interactions with hosts, rather than for prey capture or defence. Whether myxozoan venom candidates are expressed in transmission stages (e.g. in nematocysts or secretory vesicles) requires further investigation.


2020 ◽  
Vol 12 (3) ◽  
pp. 66-76 ◽  
Author(s):  
Wencheng Zong ◽  
Bo Gao ◽  
Mohamed Diaby ◽  
Dan Shen ◽  
Saisai Wang ◽  
...  

Abstract The discovery of new members of the Tc1/mariner superfamily of transposons is expected based on the increasing availability of genome sequencing data. Here, we identified a new DD35E family termed Traveler (TR). Phylogenetic analyses of its DDE domain and full-length transposase showed that, although TR formed a monophyletic clade, it exhibited the highest sequence identity and closest phylogenetic relationship with DD34E/Tc1. This family displayed a very restricted taxonomic distribution in the animal kingdom and was only detected in ray-finned fish, anura, and squamata, including 91 vertebrate species. The structural organization of TRs was highly conserved across different classes of animals. Most intact TR transposons had a length of ∼1.5 kb (range 1,072–2,191 bp) and harbored a single open reading frame encoding a transposase of ∼340 aa (range 304–350 aa) flanked by two short-terminal inverted repeats (13–68 bp). Several conserved motifs, including two helix-turn-helix motifs, a GRPR motif, a nuclear localization sequence, and a DDE domain, were also identified in TR transposases. This study also demonstrated the presence of horizontal transfer events of TRs in vertebrates, whereas the average sequence identities and the evolutionary dynamics of TR elements across species and clusters strongly indicated that the TR family invaded the vertebrate lineage very recently and that some of these elements may be currently active, combining the intact TR copies in multiple lineages of vertebrates. These data will contribute to the understanding of the evolutionary history of Tc1/mariner transposons and that of their hosts.


2007 ◽  
Vol 20 (9) ◽  
pp. 1138-1148 ◽  
Author(s):  
Benoit Alunni ◽  
Zoltan Kevei ◽  
Miguel Redondo-Nieto ◽  
Adam Kondorosi ◽  
Peter Mergaert ◽  
...  

Deciphering the mechanisms leading to symbiotic nitrogen-fixing root nodule organogenesis in legumes resulted in the identification of numerous nodule-specific genes and gene families. Among them, NCR and GRP genes encode short secreted peptides with potential antimicrobial activity. These genes appear to form large multigenic families in Medicago truncatula and other closely related legume species, whereas no similar genes were found in databases of Lotus japonicus and Glycine max. We analyzed the genomic organization of these genes as well as their evolutionary dynamics in the M. truncatula genome. A total of 108 NCR and 23 GRP genes have been mapped that were often clustered in the genome. These included 29 new NCR and 17 new GRP genes. Reverse transcription-polymerase chain reaction analyses of the novel genes confirmed their exclusive nodule-specific expression similar to the previously identified members. Protein alignments and phylogenetic analyses revealed traces of several duplication events in the history of GRP and NCR genes. Moreover, microsyntenic evidences between M. truncatula and L. japonicus validated the hypothesis that these genes are specific for the inverted repeat–lacking clade of hologalegoid legumes, which allowed dating the appearance of these two gene families during the evolution of legume plants.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Javier Fernández-López ◽  
M. Teresa Telleria ◽  
Margarita Dueñas ◽  
Mara Laguna-Castro ◽  
Klaus Schliep ◽  
...  

AbstractThe use of different sources of evidence has been recommended in order to conduct species delimitation analyses to solve taxonomic issues. In this study, we use a maximum likelihood framework to combine morphological and molecular traits to study the case of Xylodon australis (Hymenochaetales, Basidiomycota) using the locate.yeti function from the phytools R package. Xylodon australis has been considered a single species distributed across Australia, New Zealand and Patagonia. Multi-locus phylogenetic analyses were conducted to unmask the actual diversity under X. australis as well as the kinship relations respect their relatives. To assess the taxonomic position of each clade, locate.yeti function was used to locate in a molecular phylogeny the X. australis type material for which no molecular data was available using morphological continuous traits. Two different species were distinguished under the X. australis name, one from Australia–New Zealand and other from Patagonia. In addition, a close relationship with Xylodon lenis, a species from the South East of Asia, was confirmed for the Patagonian clade. We discuss the implications of our results for the biogeographical history of this genus and we evaluate the potential of this method to be used with historical collections for which molecular data is not available.


Author(s):  
Sergio A Muñoz-Gómez ◽  
Keira Durnin ◽  
Laura Eme ◽  
Christopher Paight ◽  
Christopher E Lane ◽  
...  

Abstract A most interesting exception within the parasitic Apicomplexa is Nephromyces, an extracellular, probably mutualistic, endosymbiont found living inside molgulid ascidian tunicates (i.e., sea squirts). Even though Nephromyces is now known to be an apicomplexan, many other questions about its nature remain unanswered. To gain further insights into the biology and evolutionary history of this unusual apicomplexan, we aimed to (1) find the precise phylogenetic position of Nephromyces within the Apicomplexa, (2) search for the apicoplast genome of Nephromyces, and (3) infer the major metabolic pathways in the apicoplast of Nephromyces. To do this, we sequenced a metagenome and a metatranscriptome from the molgulid renal sac, the specialized habitat where Nephromyces thrives. Our phylogenetic analyses of conserved nucleus-encoded genes robustly suggest that Nephromyces is a novel lineage sister to the Hematozoa, which comprises both the Haemosporidia (e.g., Plasmodium) and the Piroplasmida (e.g., Babesia and Theileria). Furthermore, a survey of the renal sac metagenome revealed 13 small contigs that closely resemble the genomes of the non-photosynthetic reduced plastids, or apicoplasts, of other apicomplexans. We show that these apicoplast genomes correspond to a diverse set of most closely related but genetically divergent Nephromyces lineages that co-inhabit a single tunicate host. In addition, the apicoplast of Nephromyces appears to have retained all biosynthetic pathways inferred to have been ancestral to parasitic apicomplexans. Our results shed light on the evolutionary history of the only probably mutualistic apicomplexan known, Nephromyces, and provide context for a better understanding of its life style and intricate symbiosis.


Biology ◽  
2021 ◽  
Vol 10 (2) ◽  
pp. 110
Author(s):  
Pavla Bartošová-Sojková ◽  
Jiří Kyslík ◽  
Gema Alama-Bermejo ◽  
Ashlie Hartigan ◽  
Stephen D. Atkinson ◽  
...  

The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.


2009 ◽  
Vol 90 (12) ◽  
pp. 2877-2883 ◽  
Author(s):  
Giovanna Carpi ◽  
Luigi Bertolotti ◽  
Sergio Rosati ◽  
Annapaola Rizzoli

Tick-borne encephalitis (TBE) is a severe disease that has been endemic in north-east Italy since 1992. Over the past two decades, there has been an increase in the number of human cases reported in many European countries, including Italy. To assess the current TBE infection risk, questing ticks were collected from known TBE foci, as well as from a site in northern Italy where no human infections have been reported previously. A total of 1739 Ixodes ricinus (1485 nymphs and 254 adults) was collected and analysed for TBEV prevalence by a real-time RT-PCR targeting the 3′ untranslated region. Phylogenetic analyses of the partial envelope gene were conducted on two newly sequenced TBE virus (TBEV) strains and 28 previously published sequences to investigate the genealogical relationships of the circulating TBEV strains. These phylogenetic analyses confirmed a previous report that the European TBEV subtype is the only subtype circulating within the TBE foci in north-east Italy. Interestingly, nucleotide sequence analysis revealed a high degree of divergence (mean 2.54 %) between the TBEV strains recovered in the Italian province of Trento, despite the circulation of a single TBEV subtype. This elevated genetic variability within a single TBE focus may reflect local differences in the long-standing evolutionary dynamics of TBEV at this site relative to previously characterized sites, or more recent and continuous reintroduction of various TBEV strains.


2007 ◽  
Vol 55 (2) ◽  
pp. 73 ◽  
Author(s):  
Amy Driskell ◽  
Les Christidis ◽  
B. J. Gill ◽  
Walter E. Boles ◽  
F. Keith Barker ◽  
...  

The results of phylogenetic analysis of two molecular datasets sampling all three endemic New Zealand ‘honeyeaters’ (Prosthemadera novaeseelandiae, Anthornis melanura and Notiomystis cincta) are reported. The undisputed relatedness of the first two species to other honeyeaters (Meliphagidae), and a close relationship between them, are demonstrated. However, our results confirm that Notiomystis is not a honeyeater, but is instead most closely related to the Callaeidae (New Zealand wattlebirds) represented by Philesturnus carunculatus in our study. An estimated divergence time for Notiomystis and Philesturnus of 33.8 mya (Oligocene) suggests a very long evolutionary history of this clade in New Zealand. As a taxonomic interpretation of these data we place Notiomystis in a new family of its own which takes the name Notiomystidae. We expect this new phylogenetic and taxonomic information to assist policy decisions for the conservation of this rare bird.


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