Dataset Information

Piercing Fishes: Porin Expansion and Adaptation to Hematophagy in the Vampire Snail Cumia reticulata.

ABSTRACT: Cytolytic pore-forming proteins are widespread in living organisms, being mostly involved in both sides of the host-pathogen interaction, either contributing to the innate defense or promoting infection. In venomous organisms, such as spiders, insects, scorpions, and sea anemones, pore-forming proteins are often secreted as key components of the venom. Coluporins are pore-forming proteins recently discovered in the Mediterranean hematophagous snail Cumia reticulata (Colubrariidae), highly expressed in the salivary glands that discharge their secretion at close contact with the host. To understand their putative functional role, we investigated coluporins' molecular diversity and evolutionary patterns. Coluporins is a well-diversified family including at least 30 proteins, with an overall low sequence similarity but sharing a remarkably conserved actinoporin-like predicted structure. Tracking the evolutionary history of the molluscan porin genes revealed a scattered distribution of this family, which is present in some other lineages of predatory gastropods, including venomous conoidean snails. Comparative transcriptomic analyses highlighted the expansion of porin genes as a lineage-specific feature of colubrariids. Coluporins seem to have evolved from a single ancestral porin gene present in the latest common ancestor of all Caenogastropoda, undergoing massive expansion and diversification in this colubrariid lineage through repeated gene duplication events paired with widespread episodic positive selection. As for other parasites, these findings are congruent with a "one-sided arms race," equipping the parasite with multiple variants in order to broaden its host spectrum. Overall, our results pinpoint a crucial adaptive role for coluporins in the evolution of the peculiar trophic ecology of vampire snails.

SUBMITTER: Gerdol M

PROVIDER: S-EPMC6231492 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Piercing Fishes: Porin Expansion and Adaptation to Hematophagy in the Vampire Snail Cumia reticulata.

Gerdol Marco M Cervelli Manuela M Oliverio Marco M Modica Maria Vittoria MV

Molecular biology and evolution 20181101 11

Cytolytic pore-forming proteins are widespread in living organisms, being mostly involved in both sides of the host-pathogen interaction, either contributing to the innate defense or promoting infection. In venomous organisms, such as spiders, insects, scorpions, and sea anemones, pore-forming proteins are often secreted as key components of the venom. Coluporins are pore-forming proteins recently discovered in the Mediterranean hematophagous snail Cumia reticulata (Colubrariidae), highly expres ...[more]

PMID: 30099551

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Project description:BackgroundHematophagy arose independently multiple times during metazoan evolution, with several lineages of vampire animals particularly diversified in invertebrates. However, the biochemistry of hematophagy has been studied in a few species of direct medical interest and is still underdeveloped in most invertebrates, as in general is the study of venom toxins. In cone snails, leeches, arthropods and snakes, the strong target specificity of venom toxins uniquely aligns them to industrial and academic pursuits (pharmacological applications, pest control etc.) and provides a biochemical tool for studying biological activities including cell signalling and immunological response. Neogastropod snails (cones, oyster drills etc.) are carnivorous and include active predators, scavengers, grazers on sessile invertebrates and hematophagous parasites; most of them use venoms to efficiently feed. It has been hypothesized that trophic innovations were the main drivers of rapid radiation of Neogastropoda in the late Cretaceous. We present here the first molecular characterization of the alimentary secretion of a non-conoidean neogastropod, Colubraria reticulata. Colubrariids successfully feed on the blood of fishes, throughout the secretion into the host of a complex mixture of anaesthetics and anticoagulants. We used a NGS RNA-Seq approach, integrated with differential expression analyses and custom searches for putative secreted feeding-related proteins, to describe in detail the salivary and mid-oesophageal transcriptomes of this Mediterranean vampire snail, with functional and evolutionary insights on major families of bioactive molecules.ResultsA remarkably low level of overlap was observed between the gene expression in the two target tissues, which also contained a high percentage of putatively secreted proteins when compared to the whole body. At least 12 families of feeding-related proteins were identified, including: 1) anaesthetics, such as ShK Toxin-containing proteins and turripeptides (ion-channel blockers), Cysteine-rich secretory proteins (CRISPs), Adenosine Deaminase (ADA); 2) inhibitors of primary haemostasis, such as novel vWFA domain-containing proteins, the Ectonucleotide pyrophosphatase/phosphodiesterase family member 5 (ENPP5) and the wasp Antigen-5; 3) anticoagulants, such as TFPI-like multiple Kunitz-type protease inhibitors, Peptidases S1 (PS1), CAP/ShKT domain-containing proteins, Astacin metalloproteases and Astacin/ShKT domain-containing proteins; 4) additional proteins, such the Angiotensin-Converting Enzyme (ACE: vasopressive) and the cytolytic Porins.ConclusionsColubraria feeding physiology seems to involve inhibitors of both primary and secondary haemostasis, anaesthetics, a vasoconstrictive enzyme to reduce feeding time and tissue-degrading proteins such as Porins and Astacins. The complexity of Colubraria venomous cocktail and the divergence from the arsenal of the few neogastropods studied to date (mostly conoideans) suggest that biochemical diversification of neogastropods might be largely underestimated and worth of extensive investigation.

Project description:BackgroundGene and genome duplication play important roles in the evolution of gene function. Compared to individual duplicated genes, gene clusters attract particular attention considering their frequent associations with innovation and adaptation. Here, we report for the first time the expansion of the apolipoprotein D (ApoD) ligand-transporter genes in a cluster manner specific to teleost fishes.ResultsBased on comparative genomic and transcriptomic analyses, protein 3D structure comparison, positive selection detection and breakpoints detection, the single ApoD gene in the ancestor expanded into two clusters following a dynamic evolutionary pattern in teleost fishes. Orthologous genes show conserved expression patterns, whereas lineage-specific duplicated genes show tissue-specific expression patterns and even evolve new gene expression profiles. Positive selection occurred in branches before and after gene duplication, especially for lineage-specific duplicated genes. Cluster analyses based on protein 3D structure comparisons, especially comparisons of the four loops at the opening side, show gene duplication-segregating patterns. Duplicated ApoD genes are predicted to be associated with forkhead transcription factors and MAPK genes. ApoD clusters are located next to the breakpoints of genome rearrangements.ConclusionsHere, we report the expansion of ApoD genes specific to teleost fishes in a cluster manner for the first time. Neofunctionalization and subfunctionalization were observed at both the protein and expression levels after duplication. Evidence from different aspects-i.e., abnormal expression-induced disease in humans, fish-specific expansion, predicted associations with forkhead transcription factors and MAPK genes, specific expression patterns in tissues related to sexual selection and adaptation, duplicated genes under positive selection and their location next to the breakpoints of genome rearrangements-suggests the potentially advantageous roles of ApoD genes in teleost fishes. The cluster expansion of ApoD genes specific to teleost fishes provides thus an ideal evo-devo model for studying gene duplication, cluster maintenance and new gene function emergence.

Project description:How much does natural selection, as opposed to genetic drift, admixture, and gene flow, contribute to the evolution of invasive species following introduction to a new environment? Here we assess how evolution can shape biological invasions by examining population genomic variation in non-native guppies (Poecilia reticulata) introduced to the Hawaiian Islands approximately a century ago. By examining 18 invasive populations from four Hawaiian islands and four populations from the native range in northern South America, we reconstructed the history of introductions and evaluated population structure as well as the extent of ongoing gene flow across watersheds and among islands. Patterns of differentiation indicate that guppies have developed significant population structure, with little natural or human-mediated gene flow having occurred among populations following introduction. Demographic modeling and admixture graph analyses together suggest that guppies were initially introduced to O'ahu and Maui and then translocated to Hawai'i and Kaua'i. We detected evidence for only one introduction event from the native range, implying that any adaptive evolution in introduced populations likely utilized the genetic variation present in the founding population. Environmental association tests accounting for population structure identified loci exhibiting signatures of adaptive variation related to predators and landscape characteristics but not nutrient regimes. When paired with high estimates of effective population sizes and detectable population structure, the presence of environment-associated loci supports the role of natural selection in shaping contemporary evolution of Hawaiian guppy populations. Our findings indicate that local adaptation may engender invasion success, particularly in species with life histories that facilitate rapid evolution. Finally, evidence of low gene flow between populations suggests that removal could be an effective approach to control invasive guppies across the Hawaiian archipelago.

Project description:To address the impacts of past climate changes, particularly since the last glacial period, on the history of the distribution and demography of marine species, we investigated the evolutionary and demographic responses of the intertidal batillariid gastropod, Batillaria attramentaria, to these changes, using the snail as a model species in the northwest Pacific. We applied phylogeographic and divergence population genetic approaches to mitochondrial COI sequences from B. attramentaria. To cover much of its distributional range, 197 individuals collected throughout Korea and 507 publically available sequences (mostly from Japan) were used. Finally, a Bayesian skyline plot (BSP) method was applied to reconstruct the demographic history of this species. We found four differentiated geographic groups around Korea, confirming the presence of two distinct, geographically subdivided haplogroups on the Japanese coastlines along the bifurcated routes of the warm Tsushima and Kuroshio Currents. These two haplogroups were estimated to have begun to split approximately 400,000 years ago. Population divergence analysis supported the hypothesis that the Yellow Sea was populated by a northward range expansion of a small fraction of founders that split from a southern ancestral population since the last glacial maximum (LGM: 26,000-19,000 years ago), when the southern area became re-submerged. BSP analyses on six geographically and genetically defined groups in Korea and Japan consistently demonstrated that each group has exponentially increased approximately since the LGM. This study resolved the phylogeography of B. attramentaria as a series of events connected over space and time; while paleoceanographic conditions determining the connectivity of neighboring seas in East Asia are responsible for the vicariance of this species, the postglacial sea-level rise and warming temperatures have played a crucial role in rapid range shifts and broad demographic expansions of its populations.

Dataset Information

Piercing Fishes: Porin Expansion and Adaptation to Hematophagy in the Vampire Snail Cumia reticulata.

Publications

Piercing Fishes: Porin Expansion and Adaptation to Hematophagy in the Vampire Snail Cumia reticulata.

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