A genomic view of the microbiome of coral reef demosponges

The ISME Journal, Journal Year: 2021, Volume and Issue: 15(6), P. 1641 - 1654

Published: Jan. 19, 2021

Abstract Sponges underpin the productivity of coral reefs, yet few their microbial symbionts have been functionally characterised. Here we present an analysis ~1200 metagenome-assembled genomes (MAGs) spanning seven sponge species and 25 phyla. Compared to MAGs derived from reef seawater, sponge-associated were enriched in glycosyl hydrolases targeting components tissue, mucus macroalgae, revealing a critical role for cycling organic matter. Further, visualisation distribution these genes amongst symbiont taxa uncovered functional guilds matter degradation. Genes utilisation sialic acids glycosaminoglycans tissue found specific lineages that also encoded attachment sponge-derived fibronectins cadherins, suggesting can utilise structural elements tissue. encoding CRISPR restriction-modification systems used defence against mobile genetic symbionts, along with eukaryote-like gene motifs thought be involved maintaining host association. Finally, provide evidence many sponge-enriched are laterally transferred between taxa, they confer selective advantage within niche therefore play ecology evolution.

Language: Английский

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A Deep-Sea Sponge Loop? Sponges Transfer Dissolved and Particulate Organic Carbon and Nitrogen to Associated Fauna

Frontiers in Marine Science, Journal Year: 2021, Volume and Issue: 8

Published: March 19, 2021

Cold-water coral reefs and sponge grounds are deep-sea biological hotspots, equivalent to shallow-water tropical reefs. In ecosystems, biodiversity productivity maintained through efficient recycling pathways, such as the loop. this pathway, encrusting sponges recycle dissolved organic matter (DOM) into particulate detritus. Subsequently, sponge-produced detritus serves a food source for other organisms on reef. Alternatively, DOM stored in massive was recently hypothesized be transferred higher trophic levels predation of these sponges, instead production. However, existence all prerequisite, consecutive steps loop have not yet been established. Here, we tested whether cold-water similar their counterparts, take up transfer assimilated associated fauna via either production or predation. We traced fate 13 carbon (C)- 15 nitrogen (N)-enriched (POM) time using pulse-chase approach. During 24-h pulse, uptake C/ N-enriched POM by two species, species Geodia barretti Hymedesmia sp., assessed. subsequent 9-day chase label-free seawater, investigated consumed brittle stars possible scenarios: (1) consumption detrital waste (2) direct feeding tissue. found that released both contained C from previously tracer POM, and, after exposure labeled detritus, enrichment N also detected tissue stars. These results therefore provide first evidence pathway sponges. cannot distinguish at present is acting predatory but conclude scenarios feasible. could play an important role many ecosystems where they abundant, although situ measurements needed confirm hypothesis.

Language: Английский

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Impact of Marine Chemical Ecology Research on the Discovery and Development of New Pharmaceuticals

Marine Drugs, Journal Year: 2023, Volume and Issue: 21(3), P. 174 - 174

Published: March 9, 2023

Diverse ecologically important metabolites, such as allelochemicals, infochemicals and volatile organic chemicals, are involved in marine organismal interactions. Chemically mediated interactions between intra- interspecific organisms can have a significant impact on community organization, population structure ecosystem functioning. Advances analytical techniques, microscopy genomics providing insights the chemistry functional roles of metabolites This review highlights targeted translational value several chemical ecology-driven research studies their sustainable discovery novel therapeutic agents. These ecology-based approaches include activated defense, allelochemicals arising from interactions, spatio-temporal variations phylogeny-based approaches. In addition, innovative techniques used mapping surface well metabolite translocation within holobionts summarized. Chemical information related to maintenance symbioses biosyntheses specialized compounds be harnessed for biomedical applications, particularly microbial fermentation compound production. Furthermore, climate change ecology organisms—especially production, functionality perception allelochemicals—and its implications drug efforts will presented.

Language: Английский

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Heterotrophy in marine animal forests in an era of climate change

Biological reviews/Biological reviews of the Cambridge Philosophical Society, Journal Year: 2024, Volume and Issue: 99(3), P. 965 - 978

Published: Jan. 29, 2024

Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three-dimensional structures formed suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in world's oceans. However, MAFs decline due to global local stressors that threaten survival growth of their foundational species associated biodiversity. Innovative scalable interventions needed address degradation increase resilience under change. Surprisingly, few studies have considered trophic interactions heterotrophic feeding MAF an integral component conservation. Yet, important for nutrient cycling, energy flow within food web, biodiversity, carbon sequestration, stability. This comprehensive review describes at all levels ecological organisation tropical, temperate, cold-water MAFs. It examines strengths weaknesses available tools estimating capacities then discusses threats climate change poses processes. Finally, it presents strategies improving heterotrophy, which can help maintain health

Language: Английский

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Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

Microbiome, Journal Year: 2021, Volume and Issue: 9(1)

Published: Feb. 14, 2021

Abstract Background Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM POM) the exceptional metabolic repertoire of diverse abundant microbial communities. Functional studies determining host microbiome uptake exchange, however, limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) visualise translocation 13 C- 15 N-labelled food at subcellular level high abundance sponge Plakortis angulospiculatus low Halisarca caerulea. Results The two species showed significant enrichment DOM- POM-derived C N into tissue over time. Microbial symbionts were actively involved assimilation DOM, but filtering cells (choanocytes) appeared be primary site DOM POM overall, via pinocytosis phagocytosis, respectively. Translocation carbon nitrogen from choanocytes occurred time, irrespective abundance, reflecting recycling waste products by microbiome. Conclusions Here, provide empirical evidence indicating that prokaryotic communities a obtain nutritional benefits host-associated lifestyle. interaction between highly efficient filter-feeding its likely provides competitive advantage holobiont oligotrophic environments which they thrive, retaining limiting nutrients. present unique model link symbiotic interactions function, and, cascading effects, functioning, one earliest metazoan–microbe symbioses.

Language: Английский

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Symbiont transmission in marine sponges: reproduction, development, and metamorphosis

BMC Biology, Journal Year: 2022, Volume and Issue: 20(1)

Published: May 6, 2022

Abstract Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here, we integrate embryology and microbiology to review how symbiotic microorganisms are in this early-diverging lineage. We describe vertical transmission is widespread but not universal, microbes vertically during a select window, properties of the microbiome depends on whether species high or low abundance sponge. Reproduction, development, symbiosis thus deeply rooted, why these partnerships remains central elusive tenet symbioses.

Language: Английский

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Giant sponge grounds of Central Arctic seamounts are associated with extinct seep life

Nature Communications, Journal Year: 2022, Volume and Issue: 13(1)

Published: Feb. 8, 2022

Abstract The Central Arctic Ocean is one of the most oligotrophic oceans on Earth because its sea-ice cover and short productive season. Nonetheless, across peaks extinct volcanic seamounts Langseth Ridge (87°N, 61°E), we observe a surprisingly dense benthic biomass. Bacteriosponges are abundant fauna within this community, with mass 460 g C m −2 an estimated carbon demand around 110 yr −1 , despite export fluxes from regional primary productivity only sufficient to provide <1% required carbon. Observed sponge distribution, bulk compound-specific isotope data fatty acids suggest that microbiome taps into refractory dissolved particulate organic matter, including remnants seep community. metabolic profile bacteriosponge expressed genes indicate autotrophic symbionts contribute significantly assimilation. We hotspot ecosystem unique associated biota, once fueled by degassing mounts.

Language: Английский

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On the paradox of thriving cold‐water coral reefs in the food‐limited deep sea

Biological reviews/Biological reviews of the Cambridge Philosophical Society, Journal Year: 2023, Volume and Issue: 98(5), P. 1768 - 1795

Published: May 26, 2023

ABSTRACT The deep sea is amongst the most food‐limited habitats on Earth, as only a small fraction (<4%) of surface primary production exported below 200 m water depth. Here, cold‐water coral (CWC) reefs form oases life: their biodiversity compares with tropical reefs, biomass and metabolic activity exceed other deep‐sea ecosystems by far. We critically assess paradox thriving CWC in sea, reviewing literature open‐access data habitats. This review shows firstly that CWCs typically occur areas where food supply not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost export organic matter to seabed, creating ‘feast’ conditions, interspersed ‘famine’ periods during non‐productive season. Secondly, CWCs, particularly common reef‐builder Desmophyllum pertusum (formerly known Lophelia pertusa ), are well adapted these fluctuations availability. Laboratory situ measurements revealed dietary flexibility, tissue reserves, variation growth energy allocation. Thirdly, high structural functional diversity increases resource retention: acting giant filters sustaining complex webs diverse recycling pathways, optimise gains over losses. Anthropogenic pressures, including climate change ocean acidification, threaten this fragile equilibrium through decreased supply, increased costs, dissolution calcium‐carbonate reef framework. Based review, we suggest additional criteria judge health chance persist future.

Language: Английский

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DNA ‐stable isotope probing (DNA‐SIP) identifies marine sponge‐associated bacteria actively utilizing dissolved organic matter (DOM)

Environmental Microbiology, Journal Year: 2021, Volume and Issue: 23(8), P. 4489 - 4504

Published: June 22, 2021

Sponges possess exceptionally diverse associated microbial communities and play a major role in (re)cycling of dissolved organic matter (DOM) marine ecosystems. Linking sponge-associated community structure with DOM utilization is essential to understand host-microbe interactions the uptake, processing, exchange resources. We coupled, for first time, DNA-stable isotope probing (DNA-SIP) 16S rRNA amplicon sequencing sponge holobiont identify which symbiotic bacterial taxa are metabolically active uptake. Parallel incubation experiments Plakortis angulospiculatus were amended equimolar quantities unlabelled (12 C) labelled (13 DOM. Seven sequence variants (ASVs), belonging phyla PAUC34f, Proteobacteria, Poribacteria, Nitrospirae, Chloroflexi, identified as consumers Our results support predictions that Chloroflexi capable degradation through heterotrophic carbon metabolism, while Nitrospirae may have potential mixotrophic metabolism. present new analytical application DNA-SIP detect substrate incorporation into complex provide experimental evidence links identity bacteria consumption

Language: Английский

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Reef communities associated with ‘dead’ cold-water coral framework drive resource retention and recycling in the deep sea

Deep Sea Research Part I Oceanographic Research Papers, Journal Year: 2021, Volume and Issue: 175, P. 103574 - 103574

Published: June 9, 2021

Cold-water coral (CWC) reefs create hotspots of metabolic activity in the deep sea, spite limited supply fresh organic matter from ocean surface (i.e. phytodetritus). We propose that 'dead' framework, which harbours diverse faunal and microbial communities, boosts reefs, through enhanced resource retention recycling. Analysis a video transect across 700-540 m-deep CWC mound (Rockall Bank, North-East Atlantic) revealed high benthic cover dead framework (64%). Box-cored fragments were incubated on-board showed oxygen consumption rates 0.078–0.182 μmol O2 (mmol carbon, i.e. OC)−1 h−1, indicating substantial contribution to total reef. During incubations, it was shown degradation stage influences nitrogen (re)cycling, corresponding differences community composition. New (less-degraded) released ammonium (0.005 ± 0.001 NH4+ h−1), probably due ammonotelic macrofauna. In contrast, old (more-degraded) nitrate (0.015 0.008 NO3− nitrifying microorganisms recycled fauna-excreted nitrate. Furthermore, removed natural dissolved (DOM) incubation water (0.005–0.122 C h−1). Additional feeding experiments all functional groups macrofauna taxa incorporated 13C-enriched ('labelled') DOM, widespread DOM uptake Finally, effectively retained phytodetritus, (a) by physical on biofilm-covered (b) biological filtration suspension-feeding fauna. therefore suggest acts as 'filtration-recycling factory' enhances reefs. The exposed however, is particularly vulnerable acidification, jeopardizing this important aspect reef functioning.

Language: Английский

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