| 1. |
- Cranston, Alex, et al.
(författare)
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A population specific mitochondrial intron from the sponge Phakellia robusta in the North-East Atlantic
- 2021
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Ingår i: Deep Sea Research Part I. - : Elsevier. - 0967-0637 .- 1879-0119. ; 172
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Tidskriftsartikel (refereegranskat)abstract
- Self-splicing mitochondrial introns are a rarely reported phenomenon in animals, with a sparse and uneven distribution confined to some species of sponges, corals, placozoans, and a single species of annelid. Here, we describe a mitochondrial intron present only in some populations of Phakellia robusta, a sponge distributed across the North-east Atlantic deep-sea. The mitochondrial intron of P. robusta was detected in the position 387 of the COI gene and classified as a Group I intron of class IB. Interestingly, this intron was only detected in the shallower populations of P. robusta from Ireland to Norway, spanning 1000 km and was absent in deeper samples of the species. Such deeper populations have recently been proposed to be the result of hybridization between P. robusta and its congeneric Phakellia hirondellei. We propose that this past hybridization might be behind the absence of the intron in the specimens of P. robusta occurring at deep waters. Our analyses indicate that the intron detected in P. robusta might have a double origin (most likely fungi and other organism), as it has previously suggested for the sponge Stupenda singularis. BLAST searches produced matches with the homing endonuclease gene (HEG) nested within the S. singularis intron and this HEG belongs to the family of LAGLIDADG homing endonucleases (LHEs). The evolutionary relevance of the presence/absence of this intron for this species needs to be determined and potential adaptive advantages should not be ruled out.
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| 2. |
- Koutsouveli, Vasiliki, et al.
(författare)
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Insights into the reproduction of some Antarctic dendroceratid, poecilosclerid, and haplosclerid demosponges
- 2018
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Ingår i: PLOS ONE. - : Public Library of Science (PLoS). - 1932-6203. ; 13:2
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Tidskriftsartikel (refereegranskat)abstract
- Sponges are a dominant element of the Antarctic benthic communities, posing both high species richness and large population densities. Despite their importance in Antarctic ecosystems, very little is known about their reproductive patterns and strategies. In our study, we surveyed the tissue of six different species for reproductive elements, namely, Dendrilla antarctica Topsent, 1905 (order Dendroceratida), Phorbas areolatus (Thiele, 1905), Kirkpatrickia variolosa (Kirkpatrick, 1907), and Isodictya kerguelenensis (Ridley & Dendy, 1886) (order Poecilosclerida), and Hemigellius pilosus (Kirkpatrick, 1907) and Haliclona penicillata (Topsent, 1908) (Haplosclerida). Samples of these six species containing various reproductive elements were collected in Deception Island and were processed for both light and transmission electron microscopy (TEM). Even though we were not able to monitor the entire reproductive cycle, due to time and meteorological conditions, we report important aspects of the reproduction of these species. This includes oocyte and embryo morphology and cell ultrastructure, follicular structures and nurse cell activity, as well as vitellogenesis. All species were brooding their embryos within their mesohyl. Both oocytes and embryos were registered in the majority of the studied species, and a single sperm cell being carried to an egg for fertilization was observed in H. penicillata. While the reproductive periods of all species coincided temporally, some of them seemed to rely on a single spawning event, this being suggested by the synchronic oogenesis and embryogenesis occurrence of D. antarctica, P. areolatus and I. kerguelenensis. In contrast, K. variolosa had an asynchronous embryo development, which suggests several larval release events. Our results suggest that differences in the reproductive strategies and morphological traits might succeed in the coexistence of these species at the same habitat avoiding the direct competition between them.
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| 3. |
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| 4. |
- Koutsouveli, Vasiliki, et al.
(författare)
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Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
- 2022
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Ingår i: Scientific reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 12:1, s. 6317-
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Tidskriftsartikel (refereegranskat)abstract
- Sponges contain an astounding diversity of lipids that serve in several biological functions, including yolk formation in their oocytes and embryos. The study of lipid metabolism during reproduction can provide information on food-web dynamics and energetic needs of the populations in their habitats, however, there are no studies focusing on the lipid metabolism of sponges during their seasonal reproduction. In this study, we used histology, lipidome profiling (UHPLC-MS), and transcriptomic analysis (RNA-seq) on the deep-sea sponge Phakellia ventilabrum (Demospongiae, Bubarida), a key species of North-Atlantic sponge grounds, with the goal to (i) assess the reproductive strategy and seasonality of this species, (ii) examine the relative changes in the lipidome signal and the gene expression patterns of the enzymes participating in lipid metabolism during oogenesis. Phakellia ventilabrum is an oviparous and most certainly gonochoristic species, reproducing in May and September in the different studied areas. Half of the specimens were reproducing, generating two to five oocytes per mm2. Oocytes accumulated lipid droplets and as oogenesis progressed, the signal of most of the unsaturated and monounsaturated triacylglycerides increased, as well as of a few other phospholipids. In parallel, we detected upregulation of genes in female tissues related to triacylglyceride biosynthesis and others related to fatty acid beta-oxidation. Triacylglycerides are likely the main type of lipid forming the yolk in P. ventilabrum since this lipid category has the most marked changes. In parallel, other lipid categories were engaged in fatty acid beta-oxidation to cover the energy requirements of female individuals during oogenesis. In this study, the reproductive activity of the sponge P. ventilabrum was studied for the first time uncovering their seasonality and revealing 759 lipids, including 155 triacylglycerides. Our study has ecological and evolutionary implications providing essential information for understanding the molecular basis of reproduction and the origins and formation of lipid yolk in early-branching metazoans.
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| 5. |
- Koutsouveli, Vasiliki, et al.
(författare)
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Reproductive Biology of Geodia Species (Porifera, Tetractinellida) From Boreo-Arctic North-Atlantic Deep-Sea Sponge Grounds
- 2020
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Ingår i: Frontiers in Marine Science. - : Frontiers Media SA. - 2296-7745. ; 7
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Tidskriftsartikel (refereegranskat)abstract
- Boreo-arctic sponge grounds are essential deep-sea structural habitats that provide important services for the ecosystem. These large sponge aggregations are dominated by demosponges of the genus Geodia (order Tetractinellida, family Geodiidae). However, little is known about the basic biological features of these species, such as their life cycle and dispersal capabilities. Here, we surveyed five deep-sea species of Geodia from the North-Atlantic Ocean and studied their reproductive cycle and strategy using light and electron microscopy. The five species were oviparous and gonochoristic. Synchronous development was observed at individual and population level in most of the species. Oocytes had diameters ranging from 8 μm in previtellogenic stage to 103 μm in vitellogenic stage. At vitellogenic stages, oocytes had high content of lipid yolk entirely acquired by autosynthesis, with no participation of nurse cells. Intense vertical transmission of bacterial symbionts to the oocytes by phagocytosis through pseudopodia was observed, especially in late stages of oogenesis. The density of oocytes within the sponge tissue was on average 10 oocytes/mm2 across all species, higher than that of most temperate and tropical oviparous species studied elsewhere. Spermatic cysts were widespread over the tissue during early stages, or fused in larger cysts, around the canals in later stages, and occupying between 1.5 and 12% of the tissue in males. The reproductive season spanned similar periods for all Geodia spp.: from late spring to early autumn. During the reproductive peak of each species, between 60 and 90% of the population was engaged in reproduction for most species. Given the present hazards that threaten the boreo-arctic tetractinellid sponge grounds, it becomes crucial to understand the processes behind the maintenance and regeneration of populations of keystone deep-sea species in order to predict the magnitude of human impacts and estimate their ability to recover. The information provided in this study will be useful for developing adequate conservation strategies for these vulnerable deep-sea habitats.
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| 6. |
- Koutsouveli, Vasiliki
(författare)
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Sex, Molecules, and Gene control : Ecophysiological and evolutionary aspects of key sponge species from Antarctic shallow waters and the deep sea
- 2020
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Doktorsavhandling (övrigt vetenskapligt/konstnärligt)abstract
- Very little is known about the ecophysiological aspects of Porifera (sponges) from Antarctica and North Atlantic, even though they are keystone components of these habitats. Being the earliest diverging metazoan lineage, sponges also play a fundamental role in our understanding of animal evolution. The main focus of this thesis was to study several aspects of the reproduction of sponges from the Antarctic shallow waters and the North Atlantic deep-sea sponge grounds and to describe the molecular toolkit that regulates their gametogenesis from an evolutionary perspective.In paper I, the reproductive strategy of six demosponge species commonly found in the shallow waters of Antarctica was examined with histological analyses. All species were brooders and although they reproduced during similar periods of the year, differences in their reproductive strategies might have allowed their coexistence in a habitat with annual food limitation events and low temperature.In paper II, the reproductive strategy of five species of the genus Geodia, a keystone genus of boreo-arctic sponge grounds, was assessed with histological analyses. All species were gonochoristic and oviparous, reproducing during similar periods (1-2 cycles annually) and with a high reproductive effort. The abundant lipid yolk and bacterial symbionts in their oocytes might enhance embryonic survival in the water column. Slight differences in reproductive strategies among species indicate specific adaptations for their successful colonization. This is the most detailed description of the reproductive biology of deep-sea Geodia sponges, providing essential information for the design of adequate conservation strategies in these vulnerable areas.In paper III, the genes and proteins regulating the oogenesis and spermatogenesis of the same five Geodia spp. were identified with RNA-seq and proteomic analyses and it was concluded that the molecular toolkit behind the main stages of gametogenesis is conserved across Metazoa. This is the most comprehensive molecular study on the gametogenesis of sponges and has profound implications for understanding the evolution of sexual reproduction in animals.In Manuscript IV, the reproductive features, the lipid signals and the accompanying gene expression patterns during oogenesis of the keystone deep-sea sponge Phakellia ventilabrum were assessed with histological, lipidomic and RNA-seq analyses. In this oviparous species, most of the triacylglycerides showed a tendency for signal increase during oogenesis, correlated with significant overexpression of genes related to their biosynthesis. This might suggest that triacylglyceride-rich yolk is the main lipid storage for the future embryo. This study unveils lipid metabolism patterns associated with female reproduction in sponges for the first time, setting the basis for a better understanding of the chemical ecology of this species and for future comparative analyses across species.
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| 7. |
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| 8. |
- Koutsouveli, Vasiliki, et al.
(författare)
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The Molecular Machinery of Gametogenesis in Geodia Demosponges (Porifera) : Evolutionary Origins of a Conserved Toolkit across Animals
- 2020
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Ingår i: Molecular biology and evolution. - OXFORD ENGLAND : Oxford University Press (OUP). - 0737-4038 .- 1537-1719. ; 37:12, s. 3485-3506
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Tidskriftsartikel (refereegranskat)abstract
- All animals are capable of undergoing gametogenesis. The ability of forming haploid cells from diploid cells through meiosis and recombination appeared early in eukaryotes, whereas further gamete differentiation is mostly a metazoan signature. Morphologically, the gametogenic process presents many similarities across animal taxa, but little is known about its conservation at the molecular level. Porifera are the earliest divergent animals and therefore are an ideal phylum to understand evolution of the gametogenic toolkits. Although sponge gametogenesis is well known at the histological level, the molecular toolkits for gamete production are largely unknown. Our goal was to identify the genes and their expression levels which regulate oogenesis and spermatogenesis in five gonochoristic and oviparous species of the genus Geodia, using both RNAseq and proteomic analyses. In the early stages of both female and male gametogenesis, genes involved in germ cell fate and cell-renewal were upregulated. Then, molecular signals involved in retinoic acid pathway could trigger the meiotic processes. During later stages of oogenesis, female sponges expressed genes involved in cell growth, vitellogenesis, and extracellular matrix reassembly, which are conserved elements of oocyte maturation in Metazoa. Likewise, in spermatogenesis, genes regulating the whole meiotic cycle, chromatin compaction, and flagellum axoneme formation, that are common across Metazoa were overexpressed in the sponges. Finally, molecular signals possibly related to sperm capacitation were identified during late stages of spermatogenesis for the first time in Porifera. In conclusion, the activated molecular toolkit during gametogenesis in sponges was remarkably similar to that deployed during gametogenesis in vertebrates.
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| 9. |
- Plese, Bruna, et al.
(författare)
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Mitochondrial evolution in the Demospongiae (Porifera) : Phylogeny, divergence time, and genome biology
- 2021
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Ingår i: Molecular Phylogenetics and Evolution. - : Elsevier. - 1055-7903 .- 1095-9513. ; 155
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Tidskriftsartikel (refereegranskat)abstract
- The sponge class Demospongiae is the most speciose and morphologically diverse in the phylum Porifera, and the species within it are vital components of a range of ecosystems worldwide. Despite their ubiquity, a number of recalcitrant problems still remain to be solved regarding their phylogenetic inter-relationships, the timing of their appearance, and their mitochondrial biology, the latter of which is only beginning to be investigated. Here we generated 14 new demosponge mitochondrial genomes which, alongside previously published mitochondrial resources, were used to address these issues. In addition to phylogenomic analysis, we have used syntenic data and analysis of coding regions to forge a framework for understanding the inter-relationships between Demospongiae sub-classes and orders. We have also leveraged our new resources to study the mitochondrial biology of these clades in terms of codon usage, optimisation and gene expression, to understand how these vital cellular components may have contributed to the success of the Porifera. Our results strongly support a sister relationship between Keratosa and (Verongimorpha + Heteroscleromorpha), contradicting previous studies using nuclear markers. Our study includes one species of Clionaida, and show for the first time support for a grouping of Suberitida+(Clionaida+(Tethyida + Poecilosclerida). The findings of our phylogenetic analyses are supported by in-depth examination of structural and coding-level evidence from our mitochondrial data. A time-calibrated phylogeny estimated the origin of Demospongiae in the Cambrian (similar to 529 Mya), and suggests that most demosponge order crown-groups emerged in the Mesozoic. This work therefore provides a robust basis for considering demosponge phylogenetic relationships, as well as essential mitochondrial data for understanding the biological basis for their success and diversity.
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| 10. |
- Taboada, Sergi, et al.
(författare)
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Genetic diversity, gene flow and hybridization in fan-shaped sponges (Phakellia spp.) in the North-East Atlantic deep sea
- 2022
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Ingår i: Deep Sea Research Part I. - : Elsevier. - 0967-0637 .- 1879-0119. ; 181
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Tidskriftsartikel (refereegranskat)abstract
- Deep-sea North Atlantic sponge grounds are crucial components of the marine fauna providing a key role in ecosystem functioning. To properly develop effective conservation and management plans, it is crucial to understand the genetic diversity, molecular connectivity patterns and turnover at the population level of the species involved. Here we present the study of two congeneric sponges, Phakellia robusta and Phakellia hirondellei, using multiple sources of evidence. Our phylogenetic study using a fragment of COI placed these two species as sister. Haplotype network analysis using COI revealed no genetic structure for P. hirondellei in samples from the Cantabrian Sea (<100 km). Contrastingly, P. robusta showed a clear genetic structure separating deep-water samples from the Cantabrian Sea and the Hatton-Rockall Basin, from samples from shallower waters from Kerry Head Reefs, NW of Orkney, and Norway. ddRADseq-derived SNPs for P. robusta also segregated samples by bathymetry rather than by geographical distances, and detected a predominant northwards migration for shallow-water specimens connecting sites separated ca. 2,000 km, probably thanks to prevalent oceanographic currents. Importantly, our analysis using SNPs combining the datasets of the two species revealed the presence of potential hybrids, which was corroborated by morphological (spicule) and microbial (16S amplicon sequencing) analyses. Our data suggest that hybridization between these two species occurred at least two times in the past. We discuss the importance of using next-generation techniques to unveil hybridization and the implications of our results for conservation.
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| 11. |
- Taboada, Sergi, et al.
(författare)
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Insights into the symbiotic relationship between scale worms and carnivorous sponges (Cladorhizidae, Chondrocladia)
- 2020
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Ingår i: Deep Sea Research Part I. - : PERGAMON-ELSEVIER SCIENCE LTD. - 0967-0637 .- 1879-0119. ; 156
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Tidskriftsartikel (refereegranskat)abstract
- Symbiotic associations between polynoid scale worms and other marine invertebrates are common, but sometimes poorly understood. Compounding this problem is the fact that polynoid systematics is largely unresolved. Here, we transfer the species originally described as Nemidia antillicola chondrocladiae Fauvel (1943), and currently synonymized with Neopolynoe acanellae (Verrill, 1881), to the species Neopolynoe chondrocladiae n. comb. This species is characterized by living in association with the carnivorous sponges Chondrocladia robertballnrdi Cristobo, Rios, Pomponi & Xavier, 2015 and Chondrocladia virgata Thompson, 1873. The existence of specialized chaetae in N. chondrocladiae n. comb. and the occurrence of open galleries in the sponge, derived from a gradual overgrowth of the sponge to accommodate the worm, suggest an obligate symbiotic relationship between worm and sponge. The presence of a gravid female with relatively small oocytes (maximum diameter 56.94 +/- 14.89 mu m) suggests that N. chondrocladiae n. comb. is a gonochoristic broadcaster with a planktotrophic larva, a means of reproduction that would maximize the chances of this species finding new suitable hosts to colonize. We also provide a phylogenetic placement, using four genetic markers (18S, 28S, 16S and COI), for N. chondrocladiae n. comb. and N. acanellae, which confirms they are two different species. In addition, we also report here the occurrence of another deep-water polynoid species in association with the carnivorous sponge Chondrocladia vertical= Topsent, 1920, from the Gulf of Mexico, and place it in a phylogeny.
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| 12. |
- Taboada, Sergi, et al.
(författare)
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Long distance dispersal and oceanographic fronts shape the connectivity of the keystone sponge Phakellia ventilabrum in the deep northeast Atlantic
- 2023
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Ingår i: Frontiers in Marine Science. - : Frontiers Media S.A.. - 2296-7745. ; 10
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Tidskriftsartikel (refereegranskat)abstract
- Little is known about dispersal in deep-sea ecosystems, especially for sponges, which are abundant ecosystem engineers. Understanding patterns of gene flow in deep-sea sponges is essential, especially in areas where rising pressure from anthropogenic activities makes difficult to combine management and conservation. Here, we combined population genomics and oceanographic modelling to understand how Northeast Atlantic populations (Cantabrian Sea to Norway) of the deep-sea sponge Phakellia ventilabrum are connected. The analysis comprised ddRADseq derived SNP datasets of 166 individuals collected from 57 sampling stations from 17 different areas, including two Marine Protected Areas, one Special Area of Conservation and other areas with different levels of protection. The 4,017 neutral SNPs used indicated high connectivity and panmixis amongst the majority of areas (Ireland to Norway), spanning ca. 2,500-km at depths of 99-900 m. This was likely due to the presence of strong ocean currents allowing long-distance larval transport, as supported by our migration analysis and by 3D particle tracking modelling. On the contrary, the Cantabrian Sea and Roscoff (France) samples, the southernmost areas in our study, appeared disconnected from the remaining areas, probably due to prevailing current circulation patterns and topographic features, which might be acting as barriers for gene flow. Despite this major genetic break, our results suggest that all protected areas studied are well-connected with each other. Interestingly, analysis of SNPs under selection replicated results obtained for neutral SNPs. The relatively low genetic diversity observed along the study area, though, highlights the potential fragility of this species to changing climates, which might compromise resilience to future threats.
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