scholarly journals Deep-sea sponge grounds as nutrient sinks: High denitrification rates in boreo-arctic sponges

2019 ◽  
Author(s):  
Christine Rooks ◽  
James Kar-Hei Fang ◽  
Pål Tore Mørkved ◽  
Rui Zhao ◽  
Hans Tore Rapp ◽  
...  
Keyword(s):  
Organic Matter ◽  
Deep Sea ◽  
Marine Ecosystem ◽  
Coastal Sediments ◽  
Sponge Species ◽  
Sponge Tissue ◽  
Ammonium Oxidation ◽  
Genes Encoding ◽  
Key Enzyme ◽  
Nutrient Sinks

Abstract. Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bio-available nutrients such as ammonium and nitrate. In this study we challenge this view. We show that nutrient removal through microbial denitrification is a common feature in six cold-water sponge species from boreal and Arctic sponge grounds. Denitrification rates were quantified by incubating sponge tissue sections with 15NO3- – amended oxygen saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. Rates of anaerobic ammonium oxidation (anammox) using incubations with 15NH4+ could not be detected. Denitrification rates of the different sponge species ranged from 0 to 114 nmol N cm-3 sponge day-1 under oxic conditions, and from 47 to 342 nmol N cm-3 sponge day-1 under anoxic conditions. An exponential relationship between the highest potential rates of denitrification (in the absence of oxygen) and the species-specific abundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for denitrification, suggests that the denitrifying community in these sponge species is both prepared and optimized for denitrification. The lack of a lag phase in the linear accumulation of the 15N labelled N2 gas in any of our tissue incubations is another indicator for an active community of denitrifiers in the investigated sponge species. High rates for coupled nitrification-denitrification (up to 89 % of nitrate reduction in the presence of oxygen) shows that under these conditions, the NO3- reduced in denitrification was primarily derived from nitrification within the sponge, directly coupling organic matter degradation and nitrification to denitrification in sponge tissues. Under anoxic condition when nitrification was not possible, nitrate to fuel the much higher denitrification rates had to be retrieved directly from the seawater. The lack of nifH genes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that the nitrogen cycle is not closed in the sponge grounds. The denitrified nitrogen, no matter of its origin, is then no longer available as a nutrient for the marine ecosystem. Considering average sponge biomasses on typical boreal and Arctic sponge grounds, our sponge denitrification rates reveal areal denitrification rates of 0.8 mmol N m-2 day-1 assuming non-pumping sponges and still 0.3 mmol N m-2 day-1 assuming pumping sponges. This is well within the range of denitrification rates of continental shelf sediments. For the most densely populated boreal sponge grounds we calculated denitrification rates of up to 2 mmol N m-2 day-1, which is comparable to rates in coastal sediments. Increased future impact of sponge grounds by anthropogenic stressors reducing sponge pumping activity and further stimulating sponge anaerobic processes may thus lead to that deep-sea sponge grounds change their role in the marine ecosystem from nutrient sources to nutrient sinks.

scholarly journals Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges

2020 ◽  
Vol 17 (5) ◽  
pp. 1231-1245 ◽  
Author(s):  
Christine Rooks ◽  
James Kar-Hei Fang ◽  
Pål Tore Mørkved ◽  
Rui Zhao ◽  
Hans Tore Rapp ◽  
...  
Keyword(s):  
Deep Sea ◽  
Cold Water ◽  
Marine Ecosystem ◽  
Sponge Species ◽  
Lag Phase ◽  
Sponge Tissue ◽  
Ammonium Oxidation ◽  
Genes Encoding ◽  
Key Enzyme ◽  
Nutrient Sinks

Abstract. Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bioavailable nutrients such as ammonium and nitrate. In this study we challenge this view. We show that nutrient removal through microbial denitrification is a common feature in six cold-water sponge species from boreal and Arctic sponge grounds. Denitrification rates were quantified by incubating sponge tissue sections with 15NO3--amended oxygen-saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. It was not possible to detect any rates of anaerobic ammonium oxidation (anammox) using incubations with 15NH4+. Denitrification rates of the different sponge species ranged from below detection to 97 nmol N cm−3 sponge d−1 under oxic conditions, and from 24 to 279 nmol N cm−3 sponge d−1 under anoxic conditions. A positive relationship between the highest potential rates of denitrification (in the absence of oxygen) and the species-specific abundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for denitrification, suggests that the denitrifying community in these sponge species is active and prepared for denitrification. The lack of a lag phase in the linear accumulation of the 15N-labelled N2 gas in any of our tissue incubations is another indicator for an active community of denitrifiers in the investigated sponge species. Low rates for coupled nitrification–denitrification indicate that also under oxic conditions, the nitrate used to fuel denitrification rates was derived rather from the ambient seawater than from sponge nitrification. The lack of nifH genes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that the nitrogen cycle is not closed in the sponge grounds. The denitrified nitrogen, no matter its origin, is then no longer available as a nutrient for the marine ecosystem. These results suggest a high potential denitrification capacity of deep-sea sponge grounds based on typical sponge biomass on boreal and Arctic sponge grounds, with areal denitrification rates of 0.6 mmol N m−2 d−1 assuming non-pumping sponges and still 0.3 mmol N m−2 d−1 assuming pumping sponges. This is well within the range of denitrification rates of continental shelf sediments. Anthropogenic impact and global change processes affecting the sponge redox state may thus lead to deep-sea sponge grounds changing their role in marine ecosystem from being mainly nutrient sources to becoming mainly nutrient sinks.

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

2021 ◽  
Vol 8 ◽  
Author(s):  
Martijn C. Bart ◽  
Meggie Hudspith ◽  
Hans Tore Rapp ◽  
Piet F. M. Verdonschot ◽  
Jasper M. de Goeij
Keyword(s):  
Organic Matter ◽  
Coral Reefs ◽  
Shallow Water ◽  
Deep Sea ◽  
Cold Water ◽  
Trophic Levels ◽  
Sponge Species ◽  
Sponge Tissue ◽  
Associated Fauna ◽  
Brittle Stars

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

scholarly journals Linking extracellular enzymes to phylogeny indicates a predominantly particle-associated lifestyle of deep-sea prokaryotes

2020 ◽  
Vol 6 (16) ◽  
pp. eaaz4354 ◽  
Author(s):  
Zihao Zhao ◽  
Federico Baltar ◽  
Gerhard J. Herndl
Keyword(s):  
Organic Matter ◽  
Deep Sea ◽  
Organic Molecules ◽  
Extracellular Enzymes ◽  
Surrounding Medium ◽  
Hydrolytic Enzymes ◽  
Diffusion Limited ◽  
Genes Encoding ◽  
Key Enzyme ◽  
Heterotrophic Prokaryotes

Heterotrophic prokaryotes express extracellular hydrolytic enzymes to cleave large organic molecules before taking up the hydrolyzed products. According to foraging theory, extracellular enzymes should be cell associated in dilute systems such as deep sea habitats, but secreted into the surrounding medium in diffusion-limited systems. However, extracellular enzymes in the deep sea are found mainly dissolved in ambient water rather than cell associated. In order to resolve this paradox, we conducted a global survey of peptidases and carbohydrate-active enzymes (CAZymes), two key enzyme groups initiating organic matter assimilation, in an integrated metagenomics, metatranscriptomics, and metaproteomics approach. The abundance, percentage, and diversity of genes encoding secretory processes, i.e., dissolved enzymes, consistently increased from epipelagic to bathypelagic waters, indicating that organic matter cleavage, and hence prokaryotic metabolism, is mediated mainly by particle-associated prokaryotes releasing their extracellular enzymes into diffusion-limited particles in the bathypelagic realm.

scholarly journals A genomic view of the microbiome of coral reef demosponges

2021 ◽  
Author(s):  
S. J. Robbins ◽  
W. Song ◽  
J. P. Engelberts ◽  
B. Glasl ◽  
B. M. Slaby ◽  
...  
Keyword(s):  
Organic Matter ◽  
Critical Role ◽  
Selective Advantage ◽  
Sponge Tissue ◽  
Glycosyl Hydrolases ◽  
Coral Mucus ◽  
Genes Encoding ◽  
Host Ecology ◽  
Microbial Symbionts ◽  
Sponge Symbionts

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

scholarly journals Highly diverse Asgard archaea participate in organic matter degradation in coastal sediments

2019 ◽  
Author(s):  
Mingwei Cai ◽  
Yang Liu ◽  
Xiuran Yin ◽  
Zhichao Zhou ◽  
Michael W. Friedrich ◽  
...  
Keyword(s):  
Organic Matter ◽  
Inorganic Carbon ◽  
Coastal Sediments ◽  
Ecological Niches ◽  
Organic Matter Degradation ◽  
Genomic Analyses ◽  
Organic And Inorganic Carbon ◽  
Ecological Roles ◽  
Genes Encoding ◽  
Origin Of Eukaryotes

ABSTRACTAsgard is an archaeal superphylum that might hold the key to understand the origin of eukaryotes, but its diversity and ecological roles remain poorly understood. Here, we reconstructed 15 metagenomic-assembled genomes (MAGs) from coastal sediments covering most known Asgard archaea and a novel group, which is proposed as a new Asgard phylum named as the “Gerdarchaeota”. Genomic analyses predict that Gerdarchaeota are facultative anaerobes in utilizing both organic and inorganic carbon. Unlike their closest relatives Heimdallarchaeota, Gerdarchaeota have genes encoding for cellulase and enzymes involving in the tetrahydromethanopterin-based Wood–Ljungdahl pathway. Transcriptomic evidence showed that all known Asgard archaea are capable of degrading organic matter, including peptides, amino acids and fatty acids, in different ecological niches in sediments. Overall, this study broadens the diversity of the mysterious Asgard archaea and provides evidence for their ecological roles in coastal sediments.

scholarly journals Isolating an active and inactive CACTA transposon from lettuce color mutants and characterizing their family

2021 ◽  
Author(s):  
Csanad Gurdon ◽  
Alexander Kozik ◽  
Rong Tao ◽  
Alexander Poulev ◽  
Isabel Armas ◽  
...  
Keyword(s):  
Anthocyanin Biosynthesis ◽  
Mobile Element ◽  
Bioinformatic Analysis ◽  
Relative Expression Level ◽  
Gene Coding ◽  
Genes Encoding ◽  
Key Enzyme ◽  
Natural Derivative ◽  
Dark Green ◽  
Transposon Insertions

Abstract Dietary flavonoids play an important role in human nutrition and health. Flavonoid biosynthesis genes have recently been identified in lettuce (Lactuca sativa); however, few mutants have been characterized. We now report the causative mutations in Green Super Lettuce (GSL), a natural light green mutant derived from red cultivar NAR; and GSL-Dark Green (GSL-DG), an olive-green natural derivative of GSL. GSL harbors CACTA 1 (LsC1), a 3.9-kb active nonautonomous CACTA superfamily transposon inserted in the 5′ untranslated region of anthocyanidin synthase (ANS), a gene coding for a key enzyme in anthocyanin biosynthesis. Both terminal inverted repeats (TIRs) of this transposon were intact, enabling somatic excision of the mobile element, which led to the restoration of ANS expression and the accumulation of red anthocyanins in sectors on otherwise green leaves. GSL-DG harbors CACTA 2 (LsC2), a 1.1-kb truncated copy of LsC1 that lacks one of the TIRs, rendering the transposon inactive. RNA-sequencing and reverse transcription quantitative PCR of NAR, GSL, and GSL-DG indicated the relative expression level of ANS was strongly influenced by the transposon insertions. Analysis of flavonoid content indicated leaf cyanidin levels correlated positively with ANS expression. Bioinformatic analysis of the cv Salinas lettuce reference genome led to the discovery and characterization of an LsC1 transposon family with a putative transposon copy number greater than 1,700. Homologs of tnpA and tnpD, the genes encoding two proteins necessary for activation of transposition of CACTA elements, were also identified in the lettuce genome.

scholarly journals Phylogenomic Insights into Distribution and Adaptation of Bdellovibrionota in Marine Waters

2021 ◽  
Vol 9 (4) ◽  
pp. 757
Author(s):  
Qing-Mei Li ◽  
Ying-Li Zhou ◽  
Zhan-Fei Wei ◽  
Yong Wang
Keyword(s):  
Comparative Genomics ◽  
Deep Sea ◽  
Binding Protein ◽  
Glycerol Metabolism ◽  
Metabolic Reconstruction ◽  
Type Ii Secretion ◽  
Phylogenetic Groups ◽  
Genes Encoding ◽  
Epipelagic Zone ◽  
Chitin Binding Protein

Bdellovibrionota is composed of obligate predators that can consume some Gram-negative bacteria inhabiting various environments. However, whether genomic traits influence their distribution and marine adaptation remains to be answered. In this study, we performed phylogenomics and comparative genomics studies using 132 Bdellovibrionota genomes along with five metagenome-assembled genomes (MAGs) from deep sea zones. Four phylogenetic groups, Oligoflexia, Bdello-group1, Bdello-group2 and Bacteriovoracia, were revealed by constructing a phylogenetic tree, of which 53.84% of Bdello-group2 and 48.94% of Bacteriovoracia were derived from the ocean. Bacteriovoracia was more prevalent in deep sea zones, whereas Bdello-group2 was largely distributed in the epipelagic zone. Metabolic reconstruction indicated that genes involved in chemotaxis, flagellar (mobility), type II secretion system, ATP-binding cassette (ABC) transporters and penicillin-binding protein were necessary for the predatory lifestyle of Bdellovibrionota. Genes involved in glycerol metabolism, hydrogen peroxide (H2O2) degradation, cell wall recycling and peptide utilization were ubiquitously present in Bdellovibrionota genomes. Comparative genomics between marine and non-marine Bdellovibrionota demonstrated that betaine as an osmoprotectant is probably widely used by marine Bdellovibrionota, and all the marine genomes have a number of genes for adaptation to marine environments. The genes encoding chitinase and chitin-binding protein were identified for the first time in Oligoflexia, which implied that Oligoflexia may prey on a wider spectrum of microbes. This study expands our knowledge on adaption strategies of Bdellovibrionota inhabiting deep seas and the potential usage of Oligoflexia for biological control.

Gametogenesis and the reproductive cycle in the deep-sea anemone Paracalliactis stephensoni (Cnidaria: Actiniaria)

1990 ◽  
Vol 70 (1) ◽  
pp. 163-172 ◽  
Author(s):  
Michel Praet-Van
Keyword(s):  
Organic Matter ◽  
Shallow Water ◽  
Deep Sea ◽  
Phytoplankton Bloom ◽  
Sea Anemone ◽  
Bay Of Biscay ◽  
Sea Anemones ◽  
Spring Phytoplankton Bloom ◽  
Sea Floor ◽  
Ultrastructural Investigation

This ultrastructural investigation of gametogenesis in a deep-sea anemone of the Bay of Biscay trawled around 2000 m depth, contributes to the knowledge of biology and strategy of reproduction of deep-sea benthos.This sea anemone is dioecious. The sperm appears very similar to those of shallow water sea anemones of the genus, Calliactis. The ultrastructural investigation of oogenesis allows the characteristics of the stages of previtellogenesis and vitellogenesis to be defined. The latter begins with a period of lipogenesis correlated with the formation of a trophonema. Mature oocytes measure up to 180 (im in diameter. Study of spermatogenesis and oogenesis reveals that spawning occurs in April/May. In males, the main area of testicular cysts, full of sperm, reaches maximal development from March to May and, in females, the percentage of mature oocytes decreases from 33% in April to 1% in May.Spawning may be induced by the advent in the deep-sea of the products of the spring phytoplankton bloom. This period of spawning, during the increased deposition of organic matter to the deep-sea floor, may be an advantageous strategy for early development of Paracalliactis.

scholarly journals Biogeochemical Regimes in Shallow Aquifers Reflect the Metabolic Coupling of the Elements Nitrogen, Sulfur, and Carbon

2018 ◽  
Vol 85 (5) ◽  
Author(s):  
Carl-Eric Wegner ◽  
Michael Gaspar ◽  
Patricia Geesink ◽  
Martina Herrmann ◽  
Manja Marz ◽  
...  
Keyword(s):  
Land Use ◽  
Organic Matter ◽  
Groundwater Flow ◽  
Inorganic Nitrogen ◽  
Sulfur Metabolism ◽  
Ammonium Oxidation ◽  
Metabolic Potential ◽  
Differentiation Potential ◽  
Near Surface ◽  
Monitoring Wells

ABSTRACTNear-surface groundwaters are prone to receive (in)organic matter input from their recharge areas and are known to harbor autotrophic microbial communities linked to nitrogen and sulfur metabolism. Here, we use multi-omic profiling to gain holistic insights into the turnover of inorganic nitrogen compounds, carbon fixation processes, and organic matter processing in groundwater. We sampled microbial biomass from two superimposed aquifers via monitoring wells that follow groundwater flow from its recharge area through differences in hydrogeochemical settings and land use. Functional profiling revealed that groundwater microbiomes are mainly driven by nitrogen (nitrification, denitrification, and ammonium oxidation [anammox]) and to a lesser extent sulfur cycling (sulfur oxidation and sulfate reduction), depending on local hydrochemical differences. Surprisingly, the differentiation potential of the groundwater microbiome surpasses that of hydrochemistry for individual monitoring wells. Being dominated by a few phyla (Bacteroidetes,Proteobacteria,Planctomycetes, andThaumarchaeota), the taxonomic profiling of groundwater metagenomes and metatranscriptomes revealed pronounced differences between merely present microbiome members and those actively participating in community gene expression and biogeochemical cycling. Unexpectedly, we observed a constitutive expression of carbohydrate-active enzymes encoded by different microbiome members, along with the groundwater flow path. The turnover of organic carbon apparently complements for lithoautotrophic carbon assimilation pathways mainly used by the groundwater microbiome depending on the availability of oxygen and inorganic electron donors, like ammonium.IMPORTANCEGroundwater is a key resource for drinking water production and irrigation. The interplay between geological setting, hydrochemistry, carbon storage, and groundwater microbiome ecosystem functioning is crucial for our understanding of these important ecosystem services. We targeted the encoded and expressed metabolic potential of groundwater microbiomes along an aquifer transect that diversifies in terms of hydrochemistry and land use. Our results showed that the groundwater microbiome has a higher spatial differentiation potential than does hydrochemistry.

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