Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges

Este artículo contiene 14 páginas, 6 figuras.The biological utilization of dissolved silicon (DSi) influences ocean ecology and biogeochemistry. In the deep sea, hexactinellid sponges are major DSi consumers that remain poorly understood. Their DSi consumption departs from the Michaelis-Menten kinetics of shallow-water demosponges and appears particularly maladapted to incorporating DSi from the modest concentrations typical of the modern ocean. Why did sponges not adapt to the shrinking DSi availability that followed diatom expansion some 100 to 65 million years ago? We propose that sponges incorporate DSi combining passive (aquaglyceroporins) and active (ArsB) transporters, while only active transporters (SITs) operate in diatoms and choanoflagellates. Evolution of greater silicon transport efficiency appears constrained by the additional role of aquaglyceroporins in transporting essential metalloids other than silicon. We discuss the possibility that lower energy costs may have driven replacement of ancestral SITs by less efficient aquaglyceroporins, and discuss the functional implications of conservation of aquaglyceroporin-mediated DSi utilization in vertebrates.This research was completed mostly by funds from the SponGES H2020 grant (BG-01-2015.2, agreement number 679849-2) to M.M. and A.R. and from Fisheries and Oceans Canada Strategic Program for Ecosystem-Based Research and Advice (SPERA) and International Governance Strategy (IGS) projects awarded to L.B. and E.K. This study also benefitted from funding by a PBS grant (MINECO CTM2015-67221-R) to M.M. This study is in memory of Hans Tore Rapp, who passed away on 7 March 2020, and who was the main coordinator of the H2020 SponGES project that has made this research possible.Peer reviewe

First insights into the Aurelia aurita transcriptome response upon manipulation of its microbiome

IntroductionThe associated diverse microbiome contributes to the overall fitness of Aurelia aurita, particularly to asexual reproduction. However, how A. aurita maintains this specific microbiome or reacts to manipulations is unknown.MethodsIn this report, the response of A. aurita to manipulations of its native microbiome was studied by a transcriptomics approach. Microbiome-manipulated polyps were generated by antibiotic treatment and challenging polyps with a non-native, native, and potentially pathogenic bacterium. Total RNA extraction followed by RNAseq resulted in over 155 million reads used for a de novo assembly.ResultsThe transcriptome analysis showed that the antibiotic-induced change and resulting reduction of the microbiome significantly affected the host transcriptome, e.g., genes involved in processes related to immune response and defense mechanisms were highly upregulated. Similarly, manipulating the microbiome by challenging the polyp with a high load of bacteria (2 × 107 cells/polyp) resulted in induced transcription of apoptosis-, defense-, and immune response genes. A second focus was on host-derived quorum sensing interference as a potential defense strategy. Quorum Quenching (QQ) activities and the respective encoding QQ-ORFs of A. aurita were identified by functional screening a cDNA-based expression library generated in Escherichia coli. Corresponding sequences were identified in the transcriptome assembly. Moreover, gene expression analysis revealed differential expression of QQ genes depending on the treatment, strongly suggesting QQ as an additional defense strategy.DiscussionOverall, this study allows first insights into A. aurita’s response to manipulating its microbiome, thus paving the way for an in-depth analysis of the basal immune system and additional fundamental defense strategies

Insights into the reproduction of some Antarctic dendroceratid, poecilosclerid, and haplosclerid demosponges

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

Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)

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 mm(2). 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

Implications of population connectivity studies for the design of marine protected areas in the deep sea: An example of a demosponge from the Clarion-Clipperton Zone

The abyssal demosponge Plenaster craigi inhabits the Clarion‐Clipperton Zone (CCZ) in the northeast Pacific, a region with abundant seafloor polymetallic nodules with potential mining interest. Since P. craigi is a very abundant encrusting sponge on nodules, understanding its genetic diversity and connectivity could provide important insights into extinction risks and design of marine protected areas. Our main aim was to assess the effectiveness of the Area of Particular Environmental Interest 6 (APEI‐6) as a potential genetic reservoir for three adjacent mining exploration contract areas (UK‐1A, UK‐1B and OMS‐1A). As in many other sponges, COI showed extremely low variability even for samples ~900 km apart. Conversely, the 168 individuals of P. craigi, genotyped for 11 microsatellite markers, provided strong genetic structure at large geographical scales not explained by isolation by distance (IBD). Interestingly, we detected molecular affinities between samples from APEI‐6 and UK‐1A, despite being separated ~800 km. Although our migration analysis inferred very little progeny dispersal of individuals between areas, the major differentiation of OMS‐1A from the other areas might be explained by the occurrence of predominantly northeasterly transport predicted by the HYCOM hydrodynamic model. Our study suggests that although APEI‐6 does serve a conservation role, with species connectivity to the exploration areas, it is on its own inadequate as a propagule source for P. craigi for the entire eastern portion of the CCZ. Our new data suggest that an APEI located to the east and/or the south of the UK‐1, OMS‐1, BGR, TOML and NORI areas would be highly valuable

Tectono-sedimentary evolution of the Plio-Pleistocene Corinth rift, Greece

The onshore central Corinth rift contains a syn-rift succession >3 km thick deposited in 5–15 km-wide tilt blocks, all now inactive, uplifted and deeply incised. This part of the rift records upward deepening from fluviatile to lake-margin conditions and finally to sub-lacustrine turbidite channel and lobe complexes, and deep-water lacustrine conditions (Lake Corinth) were established over most of the rift by 3.6 Ma. This succession represents the first of two phases of rift development – Rift 1 from 5.0–3.6 to 2.2–1.8 Ma and Rift 2 from 2.2–1.8 Ma to present. Rift 1 developed as a 30 km-wide zone of distributed normal faulting. The lake was fed by four major N- to NE-flowing antecedent drainages along the southern rift flank. These sourced an axial fluvial system, Gilbert fan deltas and deep lacustrine turbidite channel and lobe complexes. The onset of Rift 2 and abandonment of Rift 1 involved a 30 km northward shift in the locus of rifting. In the west, giant Gilbert deltas built into a deepening lake depocentre in the hanging wall of the newly developing southern border fault system. Footwall and regional uplift progressively destroyed Lake Corinth in the central and eastern parts of the rift, producing a staircase of deltaic and, following drainage reversal, shallow marine terraces descending from >1000 m to present-day sea level. The growth, linkage and death of normal faults during the two phases of rifting is interpreted to reflect self-organisation and strain localisation along co-linear border faults. In the west, interaction with the Patras rift occurred along the major Patras dextral strike-slip fault. This led to enhanced migration of fault activity, uplift and incision of some early Rift 2 fan deltas, and opening of the Rion Straits at c. 400–600 ka. The landscape and stratigraphic evolution of the rift was strongly influenced by regional palaeotopographic variations and local antecedent drainage, both inherited from the Hellenide fold and thrust belt

Sex, Molecules, and Gene control : Ecophysiological and evolutionary aspects of key sponge species from Antarctic shallow waters and the deep sea

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.Zoom-link to the public defence: https://uu-se.zoom.us/j/67427889269</p