ALBERT

Description: 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.

Description: Background Lithistid demosponges, also known as rock sponges, are a polyphyletic group of sponges which are widely distributed. In the Northeast Atlantic (NEA), 17 species are known and the current knowledge on their distribution is mainly restricted to the Macaronesian islands. In the Mediterranean Sea, 14 species are recorded and generally found in marine caves. Methods Lithistids were sampled in nine NEA seamounts during the scientific expeditions Seamount 1 (1987) and Seamount 2 (1993) organized by the MNHN of Paris. Collected specimens were identified through the analyses of external and internal morphological characters using light and scanning electron microscopy, and compared with material from various museum collections as well as literature records. Results A total of 68 specimens were analysed and attributed to 17 species across two orders, seven families, and seven genera, representing new records of distribution. Ten of these species are new to science, viz. Neoschrammeniella inaequalis sp. nov., N. piserai sp. nov., N. pomponiae sp. nov., Discodermia arbor sp. nov., D. kellyae sp. nov., Macandrewia schusterae sp. nov., M. minima sp. nov., Exsuperantia levii sp. nov., Leiodermatium tuba sp. nov. and Siphonidium elongatus sp. nov., and are here described and illustrated. New bathymetric records were also found for D. ramifera, D. verrucosa and M. robusta. The Meteor seamount group has a higher species richness (15 species) compared to the Lusitanian seamount group (six species). The majority of the species had their distribution restricted to one seamount, and ten are only known from a single locality, but this can be a result of sample bias. Discussion The number of species shared between the seamounts and the Macaronesian islands is very reduced. The same pattern repeats between the NEA and Mediterranean Sea. This study demonstrates that NEA seamounts are ecosystems with a higher diversity of lithistids than previously thought, increasing the number of lithistids known to occur in the NEA and Mediterranean Sea from 26 to 36 species.

Description: 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.

Description: Siliceous spicules in demosponges exist in a variety of shapes, some of which look like minute spheres of glass. They are called “sterrasters” when they belong to the Geodiidae family (Tetractinellida order) and “selenasters” when they belong to the Placospongiidae family (Clionaida order). Today, the Geodiidae represent a highly diverse sponge family with more than 340 species, occurring in shallow to deep waters worldwide, except for the Antarctic. The molecular phylogeny of Geodiidae is currently difficult to interpret because we are lacking morphological characters to support most of its clades. To fill this knowledge gap, the surface microornamentations of sterrasters were compared in different genera. Observations with scanning electron microscopy revealed four types of surfaces, which remarkably matched some of the Geodiidae genera: type I characteristic of Geodia, type II characteristic of Pachymatisma, Caminus, and some Erylus; type III characteristic of other Erylus; type IV characteristic of Caminella. Two subtypes were identified in Geodia species: warty vs. smooth rosettes. These different microornamentations were mapped on new Geodiidae COI (Folmer fragment) and 28S (C1–D2) phylogenetic trees. The monophyly of the Geodiidae was once again challenged, thereby suggesting that sterrasters have evolved independently at least three times: in the Geodiinae, in the Erylinae and in Caminella. Surface microornamentations were used to review the fossil record of sterrasters and selenasters through the paleontology literature and examination of fossils. It was concluded that “rhaxes” in the literature may represent mixes of sterrasters and selenasters: while Rhaxella spicules may belong to the Placospongiidae, Rhaxelloides spicules belong to the Geodiidae. The putative Geodiidae fossil genera, Geoditesia, and Geodiopsis, are reallocated to Tetractinellida incertae sedis. Isolated Miocene-Pliocene fossil sterrasters Hataina (Huang, 1967), Silicosphaera (Hughes, 1985) and Conciliaspongia (Robinson and Haslett, 1995) become junior synonyms of Geodia (Lamarck, 1815). Overall, the fossil record suggested that Geodiidae was present at least since the Middle Jurassic (163–166 Mya), while Geodia sterrasters were present since the Santonian/Campanian boundary, Late Cretaceous (83.6 Mya).ZooBank Article Registrationurn:lsid:zoobank.org:pub:91B1B3AC-8862-4751-B272-8A3BDF4DEE77.

Description: Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever.

Description: Background Among all present demosponges, lithistids represent a polyphyletic group with exceptionally well-preserved fossils dating back to the Cambrian. Knowledge of their recent diversity, particularly in the Tropical Western Atlantic Ocean (TWA) where they are common in deep waters, is scarce making any comparison between present and past major ‘lithistid’ faunas difficult. In addition, the lack of sufficient molecular and morphological data hamper any predictions on phylogenetic relationships or phylodiversity from this region. The Harbor Branch Oceanographic Institute (HBOI, Fort Pierce, Florida) holds the largest collection of TWA lithistid sponges worldwide, however, the majority remain to be taxonomically identified and revised. Principal Findings In this study we provide sequences of 249 lithistid demosponges using two independent molecular markers (28S rDNA (C1-D2) and cox1 mtDNA). In addition, a morphological documentation of 70 lithistid specimens is provided in the database of the Sponge Barcoding Project (SBP). This integrated dataset represents the largest and most comprehensive of the TWA lithistids to date. The phylogenetic diversity of ‘lithistid’ demosponges in the Bahamas and Jamaica are high in comparison to other TWA regions; Theonellidae and Corallistidae dominate the fauna, while Neopeltidae and Macandrewiidae are rare. A proposed tetractinellid suborder, one undescribed genus and several undescribed species are recognized and the Pacific ‘lithistid’ genera, Herengeria and Awhiowhio, are reported from the TWA for the first time. The higher-taxa relationships of desma-bearing tetractinellids are discussed and topics for revision suggested. Conclusion This first integrative approach of TWA ‘lithistid’ demosponges contributes to a better understanding of their phylogenetic affinities, diversity and bathymetric distribution patterns within the TWA. As in the Pacific, the TWA ‘lithistid’ demosponges dominate deep-water habitats. Deeper taxonomic investigations will undoubtedly contribute to a better comparison between present major ‘lithistid’ faunas and their fossil record in the Mesozoic.

Description: Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever.