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1.
Genes (Basel) ; 12(4)2021 03 29.
Article in English | MEDLINE | ID: mdl-33805549

ABSTRACT

While virtually all animals show certain abilities for regeneration after an injury, these abilities vary greatly among metazoans. Porifera (Sponges) is basal metazoans characterized by a wide variety of different regenerative processes, including whole-body regeneration (WBR). Considering phylogenetic position and unique body organization, sponges are highly promising models, as they can shed light on the origin and early evolution of regeneration in general and WBR in particular. The present review summarizes available data on the morphogenetic and cellular mechanisms accompanying different types of WBR in sponges. Sponges show a high diversity of WBR, which principally could be divided into (1) WBR from a body fragment and (2) WBR by aggregation of dissociated cells. Sponges belonging to different phylogenetic clades and even to different species and/or differing in the anatomical structure undergo different morphogeneses after similar operations. A common characteristic feature of WBR in sponges is the instability of the main body axis: a change of the organism polarity is described during all types of WBR. The cellular mechanisms of WBR are different across sponge classes, while cell dedifferentiations and transdifferentiations are involved in regeneration processes in all sponges. Data considering molecular regulation of WBR in sponges are extremely scarce. However, the possibility to achieve various types of WBR ensured by common morphogenetic and cellular basis in a single species makes sponges highly accessible for future comprehensive physiological, biochemical, and molecular studies of regeneration processes.


Subject(s)
Morphogenesis , Porifera/physiology , Regeneration , Animals , Porifera/growth & development , Signal Transduction
2.
Curr Biol ; 31(2): 433-437.e3, 2021 01 25.
Article in English | MEDLINE | ID: mdl-33220182

ABSTRACT

Larval settlement and metamorphosis are regulated by nitric oxide (NO) signaling in a wide diversity of marine invertebrates.1-10 It is thus surprising that, in most invertebrates, the substrate for NO synthesis-arginine-cannot be biosynthesized but instead must be exogenously sourced.11 In the sponge Amphimedon queenslandica, vertically inherited proteobacterial symbionts in the larva are able to biosynthesize arginine.12,13 Here, we test the hypothesis that symbionts provide arginine to the sponge host so that nitric oxide synthase expressed in the larva can produce NO, which regulates metamorphosis,8 and the byproduct citrulline (Figure 1). First, we find support for an arginine-citrulline biosynthetic loop in this sponge larval holobiont by using stable isotope tracing. In symbionts, incorporated 13C-citrulline decreases as 13C-arginine increases, consistent with the use of exogenous citrulline for arginine synthesis. In contrast, 13C-citrulline accumulates in larvae as 13C-arginine decreases, demonstrating the uptake of exogenous arginine and its conversion to NO and citrulline. Second, we show that, although Amphimedon larvae can derive arginine directly from seawater, normal settlement and metamorphosis can occur in artificial sea water lacking arginine. Together, these results support holobiont complementation of the arginine-citrulline loop and NO biosynthesis in Amphimedon larvae, suggesting a critical role for bacterial symbionts in the development of this marine sponge. Given that NO regulates settlement and metamorphosis in diverse animal phyla1-10 and arginine is procured externally in most animals,11 we propose that symbionts might play an equally critical regulatory role in this essential life cycle transition in other metazoans.


Subject(s)
Aquatic Organisms/growth & development , Bacteria/metabolism , Larva/growth & development , Porifera/growth & development , Symbiosis/physiology , Animals , Aquatic Organisms/metabolism , Aquatic Organisms/microbiology , Arginine/biosynthesis , Citrulline/metabolism , Larva/metabolism , Larva/microbiology , Metamorphosis, Biological , Nitric Oxide/biosynthesis , Porifera/metabolism , Porifera/microbiology , Seawater/chemistry
3.
Environ Microbiol Rep ; 12(6): 619-638, 2020 12.
Article in English | MEDLINE | ID: mdl-33048474

ABSTRACT

Sponges have co-evolved for millions of years alongside several types of microorganisms, which aside from participating in the animal's diet, are mostly symbionts. Since most of the genetic repertoire in the holobiont genome is provided by microbes, it is expected that the host-associated microbiome will be at least partially heritable. Sponges can therefore acquire their symbionts in different ways. Both vertical transmission (VT) and horizontal transmission (HT) have different advantages and disadvantages in the life cycle of these invertebrates. However, a third mode of transmission, called leaky vertical transmission or mixed mode of transmission (MMT), which incorporates both VT and HT modes, has gained relevance and seems to be the most robust model. In that regard, the aim of this review is to present the evolving knowledge on these main modes of transmission of the sponge microbiome. Our conclusions lead us to suggest that MMT may be more common for all sponges, with its frequency varying across the transmission spectrum between species and the environment. This hybrid model supports the stable and specific transmission of these microbial partners and reinforces their assistance in the resilience of sponges over the years.


Subject(s)
Bacteria/isolation & purification , Bacterial Physiological Phenomena , Microbiota , Porifera/microbiology , Animals , Bacteria/classification , Bacteria/genetics , Models, Biological , Phylogeny , Porifera/growth & development , Porifera/physiology , Symbiosis
4.
Nat Commun ; 11(1): 3676, 2020 07 27.
Article in English | MEDLINE | ID: mdl-32719321

ABSTRACT

The genomes of non-bilaterian metazoans are key to understanding the molecular basis of early animal evolution. However, a full comprehension of how animal-specific traits, such as nervous systems, arose is hindered by the scarcity and fragmented nature of genomes from key taxa, such as Porifera. Ephydatia muelleri is a freshwater sponge found across the northern hemisphere. Here, we present its 326 Mb genome, assembled to high contiguity (N50: 9.88 Mb) with 23 chromosomes on 24 scaffolds. Our analyses reveal a metazoan-typical genome architecture, with highly shared synteny across Metazoa, and suggest that adaptation to the extreme temperatures and conditions found in freshwater often involves gene duplication. The pancontinental distribution and ready laboratory culture of E. muelleri make this a highly practical model system which, with RNAseq, DNA methylation and bacterial amplicon data spanning its development and range, allows exploration of genomic changes both within sponges and in early animal evolution.


Subject(s)
Chromosome Mapping , Chromosomes/genetics , Evolution, Molecular , Porifera/genetics , Adaptation, Physiological/genetics , Animals , Epigenesis, Genetic , Fresh Water , Gene Expression Regulation, Developmental , Molecular Sequence Annotation , Phylogeny , Porifera/growth & development , RNA-Seq , Sequence Analysis, DNA , Synteny
5.
Microbiol Res ; 240: 126553, 2020 Nov.
Article in English | MEDLINE | ID: mdl-32711340

ABSTRACT

The coral-killing invasive sponge, Terpios hoshinota, causes extensive mortality to live corals and is a potential threat to reefs at different geographical locations. However, to date, the invasive mechanism remains largely unknown. In this study, we aimed to understand the bacterial competition between sponge and coral hosted bacteria when sponge outcompetes corals. We analysed the bacterial community of Terpios-invaded coral tissue, and the adjacent healthy tissue of sponge-invaded Favites colonies from Palk bay reef (South East Asia) of the Indian Ocean by using next-generation sequencing. Comparative analysis revealed similar bacterial diversity in both healthy and sponge covered coral tissues. However, relative abundance found to be differed between the groups. Terpios covered coral tissue had higher bacterial abundance than the healthy coral tissue. Bacterial phyla such as Bacteroidetes, Proteobacteria, Firmicutes, Actinobacteria, and Verrucomicrobia live both in sponge covered and healthy coral tissue. Notably, many of the lower abundant bacteria in healthy coral tissue (abundance <1%) became the most abundant in sponge-invaded tissue. In particular, the genus Neisseria, Bacteroides, and members of Pseudoalteromonas predominant in sponge-invaded tissue. Similar bacterial diversity between normal and and sponge-invaded coral tissues suggest that bacteria follow an exploitative competition, which might favoured sponge growth over corals.


Subject(s)
Anthozoa/growth & development , Anthozoa/microbiology , Bacteria/classification , Bacteria/genetics , Porifera/growth & development , Porifera/microbiology , Animals , Bacteria/isolation & purification , DNA, Bacterial/genetics , Indian Ocean , Metagenome , Metagenomics , Phylogeny , RNA, Ribosomal, 16S/genetics
6.
Sci Rep ; 10(1): 8176, 2020 05 18.
Article in English | MEDLINE | ID: mdl-32424237

ABSTRACT

The glass sponge Aphrocallistes vastus contributes to the formation of large reefs unique to the Northeast Pacific Ocean. These habitats have tremendous filtration capacity that facilitates flow of carbon between trophic levels. Their sensitivity and resilience to climate change, and thus persistence in the Anthropocene, is unknown. Here we show that ocean acidification and warming, alone and in combination have significant adverse effects on pumping capacity, contribute to irreversible tissue withdrawal, and weaken skeletal strength and stiffness of A. vastus. Within one month sponges exposed to warming (including combined treatment) ceased pumping (50-60%) and exhibited tissue withdrawal (10-25%). Thermal and acidification stress significantly reduced skeletal stiffness, and warming weakened it, potentially curtailing reef formation. Environmental data suggests conditions causing irreversible damage are possible in the field at +0.5 °C above current conditions, indicating that ongoing climate change is a serious and immediate threat to A. vastus, reef dependent communities, and potentially other glass sponges.


Subject(s)
Coral Reefs , Global Warming , Porifera/growth & development , Animals , Climate Change , Ecosystem , Hydrogen-Ion Concentration , Muscle Strength , Muscle, Skeletal/physiology , Pacific Ocean , Porifera/physiology , Seawater/chemistry
7.
Biotechnol Bioeng ; 117(6): 1789-1804, 2020 06.
Article in English | MEDLINE | ID: mdl-32068251

ABSTRACT

During evolution, sponges (Porifera) have honed the genetic toolbox and biosynthetic mechanisms for the fabrication of siliceous skeletal components (spicules). Spicules carry a protein scaffold embedded within biogenic silica (biosilica) and feature an amazing range of optical, structural, and mechanical properties. Thus, it is tempting to explore the low-energy synthetic pathways of spiculogenesis for the fabrication of innovative hybrid materials. In this synthetic biology approach, the uptake of multifunctional nonbiogenic nanoparticles (fluorescent, superparamagnetic) by spicule-forming cells of bioreactor-cultivated sponge primmorphs provides access to spiculogenesis. The ingested nanoparticles were detected within intracellular vesicles resembling silicasomes (silica-rich cellular compartments) and as cytosolic clusters where they lent primmorphs fluorescent/magnetic properties. During spiculogenesis, the nanoparticles initially formed an incomplete layer around juvenile, intracellular spicules. In the mature, extracellular spicules the nanoparticles were densely arranged as a surface layer that rendered the resulting composite fluorescent and magnetic. By branching off the conventional route of solid-state materials synthesis under harsh conditions, a new pathway has been opened to a versatile platform that allows adding functionalities to growing spicules as templates in living cells, using nonbiogenic nanoscale building blocks with multiple functionalities. The magnet-assisted alignment renders this composite with its fluorescent/magnetic properties potentially suitable for application in biooptoelectronics and microelectronics (e.g., microscale on-chip waveguides for applications of optical detection and sensing).


Subject(s)
Fluorescent Dyes/chemistry , Magnets/chemistry , Porifera/chemistry , Porifera/growth & development , Silicon Dioxide/chemistry , Animals , Bioreactors , Fluorescent Dyes/metabolism , Magnetic Iron Oxide Nanoparticles/chemistry , Porifera/metabolism , Silicon Dioxide/metabolism , Synthetic Biology/methods
8.
Sci Rep ; 10(1): 2340, 2020 02 11.
Article in English | MEDLINE | ID: mdl-32047192

ABSTRACT

Corals and sponges harbor diverse microbial communities that are integral to the functioning of the host. While the taxonomic diversity of their microbiomes has been well-established for corals and sponges, their functional roles are less well-understood. It is unclear if the similarities of symbiosis in an invertebrate host would result in functionally similar microbiomes, or if differences in host phylogeny and environmentally driven microhabitats within each host would shape functionally distinct communities. Here we addressed this question, using metatranscriptomic and 16S rRNA gene profiling techniques to compare the microbiomes of two host organisms from different phyla. Our results indicate functional similarity in carbon, nitrogen, and sulfur assimilation, and aerobic nitrogen cycling. Additionally, there were few statistical differences in pathway coverage or abundance between the two hosts. For example, we observed higher coverage of phosphonate and siderophore metabolic pathways in the star coral, Montastraea cavernosa, while there was higher coverage of chloroalkane metabolism in the giant barrel sponge, Xestospongia muta. Higher abundance of genes associated with carbon fixation pathways was also observed in M. cavernosa, while in X. muta there was higher abundance of fatty acid metabolic pathways. Metagenomic predictions based on 16S rRNA gene profiling analysis were similar, and there was high correlation between the metatranscriptome and metagenome predictions for both hosts. Our results highlight several metabolic pathways that exhibit functional similarity in these coral and sponge microbiomes despite the taxonomic differences between the two microbiomes, as well as potential specialization of some microbially based metabolism within each host.


Subject(s)
Anthozoa/microbiology , Bacteria/classification , Metagenome , Microbiota , Porifera/microbiology , RNA, Ribosomal, 16S/analysis , Symbiosis , Animals , Anthozoa/genetics , Anthozoa/growth & development , Bacteria/genetics , Bacteria/isolation & purification , Biodiversity , Host-Pathogen Interactions , Metabolic Networks and Pathways , Phylogeny , Porifera/genetics , Porifera/growth & development
9.
Acta Biotheor ; 68(1): 61-71, 2020 Mar.
Article in English | MEDLINE | ID: mdl-31468242

ABSTRACT

Simulation of complex biological systems with agent-based models is becoming more relevant with the increase in Graphics Processing Unit (GPU) power. In those simulations, up to millions of virtual cells are individually computed, involving daunting processing times. An important part of computational models is the algorithm that manages how agents perceive their surroundings. This can be particularly problematic in three-dimensional environments where agents have deformable virtual membranes. This article presents a GPU algorithm that gives the possibility for agents to integrate the signals scattered on their virtual membrane. It is detailed to be coded in languages like OpenCL or Cuda. Its performances are tested to show its speed with current GPU devices. Finally, it was implemented inside an existing software to test and illustrate the possibilities it offers.


Subject(s)
Algorithms , Cell Membrane/physiology , Cell Physiological Phenomena , Computer Simulation , Porifera/growth & development , Software , Animals , Computer Graphics
10.
Sci Rep ; 9(1): 18398, 2019 12 05.
Article in English | MEDLINE | ID: mdl-31804527

ABSTRACT

The growth rates and ages of many benthic marine organisms are poorly understood, complicating our understanding of ecosystem change. This is particularly true for sponges, which are morphologically diverse and lack indicators of annual growth. In this study, we used emerging technologies to measure volume, surface area, and approximate age of 16 sponge species on the Tibbetts shipwreck off Cayman Brac, Caribbean Sea. Photogrammetry was used to determine the volume of individual sponges on the wreck surface, and a time series of YouTube videos was amassed in order to approximate the greatest possible age of the sponges as 8.74 y. Applying the volume measurements to an existing growth equation for the Caribbean sponge Aiolochroia crassa yielded age estimates of 5.2-10.4 y for the largest individuals of the 16 species. Specific growth rates were then calculated for 7 species from the Tibbetts and 8 species from a second shipwreck (Spiegel Grove, Key Largo, FL). Subsequent growth forecasts from these 15 species corroborate a resource trade-off between growth and the production of chemical defenses. Shipwrecks and other anthropogenic structures can be an important source of demographic information for benthic organisms, provided that certain assumptions about their provenance and history can be met.


Subject(s)
Aquatic Organisms/growth & development , Ecosystem , Porifera/growth & development , Animals , Caribbean Region , Coral Reefs , Cyclonic Storms/history , History, 21st Century , Humans , Imaging, Three-Dimensional , Oceans and Seas , Photogrammetry , Ships/history , Structure Collapse
11.
PLoS One ; 14(10): e0223949, 2019.
Article in English | MEDLINE | ID: mdl-31622402

ABSTRACT

The Ligurian Sea is one of the most studied Mediterranean basins. Since the beginning of the last century, many research expeditions have characterized its benthic and pelagic fauna through scuba diving and trawl surveys. However, a large knowledge gap exists about the composition of benthic communities extending into the so-called mesophotic or twilight depth range, currently under intense pressure from commercial and recreational fishing. A series of visual surveys, carried out by means of remotely operated vehicles between 2012 and 2018, were conducted along the Ligurian deep continental shelf and shelf break, between 30 and 210 m depth, in order to characterize the main benthic biocoenoses dwelling at this depth range and to determine the most relevant environmental factors that explain their spatial distribution. Deep circalittoral communities of the Ligurian Sea were represented by a mixture of species belonging to the deepest extension of shallow-water habitats and deep circalittoral ones. Twelve major biocoenoses were identified, each one characterized by specific preferences in depth range, substrate type and seabed slope. Those biocoenoses included gorgonian and hydrozoan forests, dense keratose sponge grounds, Dendrophyllia cornigera gardens, bryozoan beds and soft-bottom meadows of sabellid polychaetes and soft-corals. Other less common aggregations included six forests of black corals and two populations of Paramuricea macrospina. A georeferenced database has been created in order to provide information to managers and stakeholders about the location of the identified communities and high-diversity areas, aiming to facilitate sustainable long-term conservation of the Ligurian benthic ecosystem.


Subject(s)
Aquatic Organisms/growth & development , Remote Sensing Technology/instrumentation , Animals , Anthozoa/classification , Anthozoa/growth & development , Aquatic Organisms/classification , Biodiversity , Bryozoa/classification , Bryozoa/growth & development , Diving , Magnoliopsida/classification , Magnoliopsida/growth & development , Mediterranean Sea , Porifera/classification , Porifera/growth & development , Species Specificity
12.
Curr Opin Genet Dev ; 57: 91-97, 2019 08.
Article in English | MEDLINE | ID: mdl-31546193

ABSTRACT

Animal morphogenesis can be summarized as a reconfiguration of a mass of cells. Although extracellular matrices that include rigid skeletal elements, such as cartilage/bones and exoskeletons, have important roles in morphogenesis, they are also secreted in situ by accumulated cells or epithelial cells. In contrast, recent studies of the skeleton construction of sponges (Porifera) illuminate a conceptually different mechanism of morphogenesis in which cells manipulate rather fine rigid materials (spicules) to form larger structures. Here, two different types of sponge skeleton formation using calcareous spicules or siliceous spicules are compared with regard to the concept of the production of rigid materials and their use in skeletons. The comparison highlights the advantages of their different strategies of forming sponge skeletons.


Subject(s)
Extracellular Matrix/genetics , Morphogenesis/genetics , Porifera/growth & development , Skeleton/growth & development , Animal Shells/growth & development , Animals , Cartilage/growth & development , Epithelial Cells/metabolism , Porifera/genetics
13.
Adv Protein Chem Struct Biol ; 116: 421-449, 2019.
Article in English | MEDLINE | ID: mdl-31036299

ABSTRACT

Cell-to-cell signaling is responsible for regulation of many developmental processes such as proliferation, cell migration, survival, cell fate specification and axis patterning. In this article we discussed the role of signaling in the metamorphosis of sponges with a focus on epithelial-mesenchymal transition (EMT) accompanying this event. Sponges (Porifera) are an ancient lineage of morphologically simple animals occupying a basal position on the tree of life. The study of these animals is necessary for understanding the origin of multicellularity and the evolution of developmental processes. Development of sponges is quite diverse. It finishes with the metamorphosis of a free-swimming larva into a young settled sponge. The outer surface of sponge larvae consists of a ciliated epithelial sheath, which ensures locomotion, while their internal structure varies from genus to genus. The fate of larval ciliated cells is the most intriguing aspect of metamorphosis. In this review we discuss the fate of larval ciliated cells, the processes going on in cells during metamorphosis at the molecular level and the regulation of this process. The review is based on information about several sponge species with a focus on Halisarca dujardini, Sycon ciliatum and Amphimedon queenslandica. In our model sponge, H. dujardini, ciliated cells leave the larval epithelium during metamorphosis and migrate to the internal cell mass as amoeboid cells to be differentiated into choanocytes of the juvenile sponge. Ciliated cells undergo EMT and internalize within minutes. As EMT involves the disappearance of adherens junctions and as cadherin, the main adherens junction protein, was identified in the transcriptome of several sponges, we suppose that EMT is regulated through cadherin-containing adherens junctions between ciliated cells. We failed to identify the master genes of EMT in the H. dujardini transcriptome, possibly because transcription was absent in the sequenced stages. They may be revealed by a search in the genome. The master genes themselves are controlled by various signaling pathways. Sponges have all the six signaling pathways conserved in Metazoa: Wnt, TGF-beta, Hedgehog, Notch, FGF and NO-dependent pathways. Summarizing the new data about intercellular communication in sponges, we can put forward two main questions regarding metamorphosis: (1) Which of the signaling pathways and in what hierarchical order are involved in metamorphosis? (2) How is the organization of a young sponge related to that of the larva or, in other words, is there a heredity of axes between the larva and the adult sponge?


Subject(s)
Porifera/cytology , Porifera/growth & development , Signal Transduction , Animals , Epithelial-Mesenchymal Transition , Larva/cytology , Larva/growth & development , Metamorphosis, Biological , Porifera/embryology
14.
PLoS One ; 14(2): e0212005, 2019.
Article in English | MEDLINE | ID: mdl-30794564

ABSTRACT

Canonical and non-canonical Wnt signaling, as well as the Pax/Six gene network, are involved in patterning the freshwater sponge aquiferous system. Using computational approaches to identify transcription factor binding motifs in a freshwater sponge genome, we located putative PaxB binding sites near a Secreted Frizzled Related Protein (SFRP) gene in Ephydatia muelleri. EmSFRP is expressed throughout development, but with highest levels in juvenile sponges. In situ hybridization and antibody staining show EmSFRP expression throughout the pinacoderm and choanoderm in a subpopulation of amoeboid cells that may be differentiating archeocytes. Knockdown of EmSFRP leads to ectopic oscula formation during development, suggesting that EmSFRP acts as an antagonist of Wnt signaling in E. muelleri. Our findings support a hypothesis that regulation of the Wnt pathway by the Pax/Six network as well as the role of Wnt signaling in body plan morphogenesis was established before sponges diverged from the rest of the metazoans.


Subject(s)
Intracellular Signaling Peptides and Proteins/metabolism , Otx Transcription Factors/metabolism , Porifera/growth & development , Animals , Binding Sites , Body Patterning , Computational Biology , Fresh Water , Gene Expression Regulation, Developmental , Gene Knockdown Techniques , Intracellular Signaling Peptides and Proteins/chemistry , Intracellular Signaling Peptides and Proteins/genetics , Porifera/genetics , Porifera/metabolism , Wnt Signaling Pathway
15.
Proc Biol Sci ; 285(1881)2018 06 27.
Article in English | MEDLINE | ID: mdl-29925613

ABSTRACT

Chancelloriids are an extinct group of spiny Cambrian animals of uncertain phylogenetic position. Despite their sponge-like body plan, their spines are unlike modern sponge spicules, but share several features with the sclerites of certain Cambrian bilaterians, notably halkieriids. However, a proposed homology of these 'coelosclerites' implies complex transitions in body plan evolution. A new species of chancelloriid, Allonnia nuda, from the lower Cambrian (Stage 3) Chengjiang Lagerstätte is distinguished by its large size and sparse spination, with modified apical sclerites surrounding an opening into the body cavity. The sclerite arrangement in A. nuda and certain other chancelloriids indicates that growth involved sclerite addition in a subapical region, thus maintaining distinct zones of body sclerites and apical sclerites. This pattern is not seen in halkieriids, but occurs in some modern calcarean sponges. With scleritome assembly consistent with a sponge affinity, and in the absence of cnidarian- or bilaterian-grade features, it is possible to interpret chancelloriids as sponges with an unusually robust outer epithelium, strict developmental control of body axis formation, distinctive spicule-like structures and, by implication, minute ostia too small to be resolved in fossils. In this light, chancelloriids may contribute to the emerging picture of high disparity among early sponges.


Subject(s)
Biological Evolution , Fossils , Porifera/growth & development , Animals , China , Fossils/anatomy & histology , Porifera/anatomy & histology
16.
FEMS Microbiol Ecol ; 94(5)2018 05 01.
Article in English | MEDLINE | ID: mdl-29617990

ABSTRACT

Tedania sp. is a dominant sponge that is ubiquitous along the southeast coast of China. High-throughput sequencing and transmission electron microscopy were used to describe a detailed profile of sponge-associated microbiomes at seven life stages: adult, embryo-containing spawning adult, embryo, pre-competent larva at 2 h and 4 h, competent larva at 8 h and post-larva within 1-2h after settlement, as well as the surrounding seawater. Among a total of 15098 operational taxonomic units (OTUs), 13 were present exclusively in all stages of the sponge life cycle and could thus be identified as sponge-specific bacteria. Many OTUs were shared between the sponge and seawater, though abundance differed. The relative abundance of ß-Proteobacteria associated with sponges was much higher than found in seawater. The microbiomes from each life stage also exhibited a characteristic distribution. Synechococcales dominated in adults, and Enterobacteriaceae was prominent in larvae. The competent larva was notable, with sharp increases in the total OTUs, diversity indices, richness estimates and unique OTUs. Some bacterial groups that were rare in other sponge stages and seawater, such as Clostridia (5.6%), were markedly more abundant in competent larvae. In conclusion, this work greatly advances our understanding of the dynamics and persistence of the sponge-microbe association.


Subject(s)
Bacteria/isolation & purification , Life Cycle Stages , Microbiota , Porifera/microbiology , Animals , Bacteria/classification , Bacteria/genetics , Biodiversity , China , DNA, Bacterial/genetics , High-Throughput Nucleotide Sequencing , Phylogeny , Porifera/growth & development , RNA, Ribosomal, 16S/genetics , Seawater/microbiology , Sequence Analysis, DNA
17.
PLoS One ; 13(3): e0194659, 2018.
Article in English | MEDLINE | ID: mdl-29579118

ABSTRACT

The cold-water coral Lophelia pertusa is an ecosystem engineer that builds reef structures on the seafloor. The interaction of the reef topography with hydrodynamics is known to enhance the supply of suspended food sources to the reef communities. However, the reef framework is also a substrate for other organisms that may compete for the very same suspended food sources. Here, we used the passive suspension feeder Lophelia pertusa and the active suspension feeding sponge Hymedesmia coriacea as model organisms to study niche overlap using isotopically-enriched algae and bacteria as suspended food sources. The coral and the sponge were fed with a combination of 13C-enriched bacteria/15N-enriched algae or 15N-enriched bacteria/13C-enriched algae, which was subsequently traced into bulk tissue, coral skeleton and dissolved inorganic carbon (i.e. respiration). Both the coral and the sponge assimilated and respired the suspended bacteria and algae, indicating niche overlap between these species. The assimilation rates of C and N into bulk tissue of specimens incubated separately were not significantly different from assimilation rates during incubations with co-occurring corals and sponges. Hence, no evidence for exploitative resource competition was found, but this is likely due to the saturating experimental food concentration that was used. We do not rule out that exploitative competition occurs in nature during periods of low food concentrations. Food assimilation and respiration rates of the sponge were almost an order of magnitude higher than those of the cold-water coral. We hypothesize that the active suspension feeding mode of the sponge explains the observed differences in resource uptake as opposed to the passive suspension feeding mode of the cold-water coral. These feeding mode differences may set constraints on suitable habitats for cold-water corals and sponges in their natural habitats.


Subject(s)
Anthozoa/metabolism , Porifera/metabolism , Animal Feed , Animals , Anthozoa/chemistry , Anthozoa/growth & development , Bacteria/chemistry , Bacteria/metabolism , Carbon Isotopes/chemistry , Chlorophyta/chemistry , Chlorophyta/metabolism , Coral Reefs , Ecosystem , Isotope Labeling , Nitrogen Isotopes/chemistry , Porifera/chemistry , Porifera/growth & development
18.
Mol Ecol ; 27(8): 2124-2137, 2018 04.
Article in English | MEDLINE | ID: mdl-29473977

ABSTRACT

Bioeroding sponges break down calcium carbonate substratum, including coral skeleton, and their capacity for reef erosion is expected to increase in warmer and more acidic oceans. However, elevated temperature can disrupt the functionally important microbial symbionts of some sponge species, often with adverse consequences for host health. Here, we provide the first detailed description of the microbial community of the bioeroding sponge Cliona orientalis and assess how the community responds to seawater temperatures incrementally increasing from 23°C to 32°C. The microbiome, identified using 16S rRNA gene sequencing, was dominated by Alphaproteobacteria, including a single operational taxonomic unit (OTU; Rhodothalassium sp.) that represented 21% of all sequences. The "core" microbial community (taxa present in >80% of samples) included putative nitrogen fixers and ammonia oxidizers, suggesting that symbiotic nitrogen metabolism may be a key function of the C. orientalis holobiont. The C. orientalis microbiome was generally stable at temperatures up to 27°C; however, a community shift occurred at 29°C, including changes in the relative abundance and turnover of microbial OTUs. Notably, this microbial shift occurred at a lower temperature than the 32°C threshold that induced sponge bleaching, indicating that changes in the microbiome may play a role in the destabilization of the C. orientalis holobiont. C. orientalis failed to regain Symbiodinium or restore its baseline microbial community following bleaching, suggesting that the sponge has limited ability to recover from extreme thermal exposure, at least under aquarium conditions.


Subject(s)
Ecology , Microbiota/genetics , Porifera/microbiology , Animals , Microbiota/physiology , Porifera/genetics , Porifera/growth & development , Seawater/microbiology , Temperature
19.
Proc Biol Sci ; 285(1870)2018 01 10.
Article in English | MEDLINE | ID: mdl-29321296

ABSTRACT

The ability to encrust in order to secure and maintain growth on a substrate is a key competitive innovation in benthic metazoans. Here we describe the substrate growth dynamics, mode of biomineralization and possible affinity of Namapoikia rietoogensis, a large (up to 1 m), robustly skeletal, and modular Ediacaran metazoan which encrusted the walls of synsedimentary fissures within microbial-metazoan reefs. Namapoikia formed laminar or domal morphologies with an internal structure of open tubules and transverse elements, and had a very plastic, non-deterministic growth form which could encrust both fully lithified surfaces as well as living microbial substrates, the latter via modified skeletal holdfasts. Namapoikia shows complex growth interactions and substrate competition with contemporary living microbialites and thrombolites, including the production of plate-like dissepiments in response to microbial overgrowth which served to elevate soft tissue above the microbial surface. Namapoikia could also recover from partial mortality due to microbial fouling. We infer initial skeletal growth to have propagated via the rapid formation of an organic scaffold via a basal pinacoderm prior to calcification. This is likely an ancient mode of biomineralization with similarities to the living calcified demosponge Vaceletia. Namapoikia also shows inferred skeletal growth banding which, combined with its large size, implies notable individual longevity. In sum, Namapoikia was a large, relatively long-lived Ediacaran clonal skeletal metazoan that propagated via an organic scaffold prior to calcification, enabling rapid, effective and dynamic substrate occupation and competition in cryptic reef settings. The open tubular internal structure, highly flexible, non-deterministic skeletal organization, and inferred style of biomineralization of Namapoikia places probable affinity within total-group poriferans.


Subject(s)
Biomineralization , Fossils , Porifera/growth & development , Animals , Coral Reefs , Fossils/microbiology , Fossils/ultrastructure , Geologic Sediments , Porifera/microbiology , Porifera/ultrastructure
20.
PLoS One ; 12(8): e0182365, 2017.
Article in English | MEDLINE | ID: mdl-28787024

ABSTRACT

The coral-killing sponge, Terpios hoshinota is a global invasive species that has conquered coral patches within a short span of time, which has led to a significant decline in living coral cover at various geographical locations. In this study, we surveyed the linear progression and impact of the Terpios invasion on live coral patches along Palk Bay, Indian Ocean, from August 2013 to August 2015. The field inventory revealed an extensive fatality rate of 76% as a result of Terpios outbreak. Experimental findings showed that symbiotic cyanobacteria act as a nutritional factory for the aggressive growth of Terpios. Shading hypothetically impairs the nutritional symbiont of the invasive species: the effect of sunlight on cyanobacterial biomass and its influence on Terpios progression over live coral patches was tested through in situ shading experiments. This study showed that artificial shading with cotton fabric could effectively mitigate sponge growth on live coral without affecting coral homeostasis.


Subject(s)
Anthozoa , Porifera/physiology , Porifera/radiation effects , Sunlight , Animals , Anthozoa/growth & development , Biomass , Cyanobacteria/physiology , Introduced Species/statistics & numerical data , Linear Models , Porifera/growth & development , Porifera/microbiology , Symbiosis , Time Factors
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