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Molecular phylogeny of the Cyathocotylidae (Digenea, Diplostomoidea) necessitates systematic changes and reveals a history of host and environment switches.

ABSTRACT: The Cyathocotylidae is a globally distributed family of digeneans parasitic as adults in fish, reptiles, birds, and mammals in both freshwater and marine environments. Molecular phylogenetic analysis of interrelationships among cyathocotylids is lacking with only a few species included in previous studies. We used sequences of the nuclear 28S rRNA gene to examine phylogenetic affinities of 11 newly sequenced taxa of cyathocotylids and the closely related family Brauninidae collected from fish, reptiles, birds, and dolphins from Australia, Southeast Asia, Europe, North America and South America. This is the first study to provide sequence data from adult cyathocotylids parasitic in fish and reptiles. Our analyses demonstrated that the members of the genus Braunina (family Brauninidae) belong to the Cyathocotylidae, placing the Brauninidae into synonymy with the Cyathocotylidae. In addition, our DNA sequences supported the presence of a second species in the currently monotypic Braunina. Our phylogeny revealed that Cyathocotyle spp. from crocodilians belong to a separate genus (Suchocyathocotyle, previously proposed as a subgenus) and subfamily (Suchocyathocotylinae subfam. n.). Morphological study of Gogatea serpentum indicum supported its elevation to species as Gogatea mehri. The phylogeny did not support Holostephanoides within the subfamily Cyathocotylinae; instead, Holostephanoides formed a strongly supported clade with members of the subfamily Szidatiinae (Gogatea and Neogogatea). Therefore, we transfer Holostephanoides into the Szidatiinae. DNA sequence data revealed the potential presence of cryptic species reported under the name Mesostephanus microbursa. Our phylogeny indicated at least two major host switching events in the evolutionary history of the subfamily Szidatiinae which likely resulted in the transition of these parasites from birds to fish and snakes. Likewise, the transition to dolphins by Braunina represents another major host switching event among the Cyathocotylidae. In addition, our phylogeny revealed more than a single transition between freshwater and marine environments demonstrated in our dataset by Braunina and some Mesostephanus.

SUBMITTER: Achatz TJ

PROVIDER: S-EPMC6959977 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The Proterodiplostomidae Dubois, 1936 is a relatively small family of diplostomoidean digeneans parasitising the intestines of reptilian hosts associated with freshwater environments in tropical and subtropical regions. The greatest diversity of proterodiplostomids is found in crocodilians, although some parasitise snakes and turtles. According to the most recent revision, the Proterodiplostomidae included 17 genera within 5 subfamilies. Despite the complex taxonomic structure of the family, availability of testable morphology-based phylogenetic hypotheses and ancient hosts, molecular phylogenetic analyses of the group were practically lacking. Herein, we use novel DNA sequence data of the nuclear lsrRNA gene and mitochondrial cox1 gene from a broad range of proterodiplostomid taxa obtained from crocodilian, fish, and snake hosts on four continents to test the monophyly of the family and evaluate the present morphology-based classification system of the Proterodiplostomidae in comparison with the molecular phylogeny. This first detailed phylogeny for the Proterodiplostomidae challenges the current systematic framework. Combination of molecular phylogenetic data with examination of freshly collected quality specimens and re-evaluation of morphological criteria resulted in a number of systematic and nomenclatural changes along with a new phylogeny-based classification of the Proterodiplostomidae. As the result of our molecular and morphological analyses: (i) the current subfamily structure of the Proterodiplostomidae is abolished; (ii) three new genera, Paraproterodiplostomum n. g., Neocrocodilicola n. g. and Proteroduboisia n. g., are described and Pseudoneodiplostomoides Yamaguti, 1954 is restored and elevated from subgenus to genus level; (iii) two new species, Paraproterodiplostomum currani n. g., n. sp. and Archaeodiplostomum overstreeti n. sp., are described from the American alligator in Mississippi, USA. Comparison of the structure of terminal ducts of the reproductive system in all proterodiplostomid genera did not support the use of these structures for differentiation among subfamilies (or major clades) within the family, although they proved to be useful for distinguishing among genera and species. Our study includes the first report of proterodiplostomids from Australia and the first evidence of a snake acting as a paratenic host for a proterodiplostomid. A key to proterodiplostomid genera is provided. Questions of proterodiplostomid-host associations parasitic in crocodilians are discussed in connection with their historical biogeography. Our molecular phylogeny of the Proterodiplostomidae closely matches the current molecular phylogeny of crocodilians. Directions for future studies of the Proterodiplostomidae are outlined.

Project description:The oomycete pathogen Phytophthora infestans causes potato and tomato late blight, a disease that is a serious threat to agriculture. P. infestans is a hemibiotrophic pathogen, and during infection, it scavenges nutrients from living host cells for its own proliferation. To date, the nutrient flux from host to pathogen during infection has hardly been studied, and the interlinked metabolisms of the pathogen and host remain poorly understood. Here, we reconstructed an integrated metabolic model of P. infestans and tomato (Solanum lycopersicum) by integrating two previously published models for both species. We used this integrated model to simulate metabolic fluxes from host to pathogen and explored the topology of the model to study the dependencies of the metabolism of P. infestans on that of tomato. This showed, for example, that P. infestans, a thiamine auxotroph, depends on certain metabolic reactions of the tomato thiamine biosynthesis. We also exploited dual-transcriptome data of a time course of a full late blight infection cycle on tomato leaves and integrated the expression of metabolic enzymes in the model. This revealed profound changes in pathogen-host metabolism during infection. As infection progresses, P. infestans performs less de novo synthesis of metabolites and scavenges more metabolites from tomato. This integrated metabolic model for the P. infestans-tomato interaction provides a framework to integrate data and generate hypotheses about in planta nutrition of P. infestans throughout its infection cycle.IMPORTANCE Late blight disease caused by the oomycete pathogen Phytophthora infestans leads to extensive yield losses in tomato and potato cultivation worldwide. To effectively control this pathogen, a thorough understanding of the mechanisms shaping the interaction with its hosts is paramount. While considerable work has focused on exploring host defense mechanisms and identifying P. infestans proteins contributing to virulence and pathogenicity, the nutritional strategies of the pathogen are mostly unresolved. Genome-scale metabolic models (GEMs) can be used to simulate metabolic fluxes and help in unravelling the complex nature of metabolism. We integrated a GEM of tomato with a GEM of P. infestans to simulate the metabolic fluxes that occur during infection. This yields insights into the nutrients that P. infestans obtains during different phases of the infection cycle and helps in generating hypotheses about nutrition in planta.

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Molecular phylogeny of the Cyathocotylidae (Digenea, Diplostomoidea) necessitates systematic changes and reveals a history of host and environment switches.

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