Size Is the Major Determinant of Pumping Rates in Marine Sponges

Morganti, Teresa Maria; Ribes, Marta; Yahel, Gitai; Coma, Rafael

doi:10.3389/fphys.2019.01474

Cited by 74 publications

(114 citation statements)

References 103 publications

(201 reference statements)

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“…5b, c). These and recent findings suggest relationships between DOM uptake and microbial abundance/ pumping rate are more complex [5,73] and are further influenced by factors such as sponge growth form [5] as well as DOM quantity and composition [22,37,74,75]. Microbes did appear to allow the HMA sponge to efficiently utilize a greater variety of dissolved compounds, which could contribute to trophic niche partitioning between HMA and LMA sponges [22,76,77].…”

Section: Dom Is Assimilated By Both Host and Symbiont Cellsmentioning

confidence: 77%

“…Samples were taken for dissolved organic carbon (DOC) and pico-and nanoplankton as the primary particulate organic carbon (POC) diet component (sampling details in Supplementary Methods). Sponge pumping rates were calculated using the dye front speed method as described by Morganti et al [7]. Uptake rates (C flux ) of DOC and POC were calculated as…”

Section: Scanning Electron Microscopy (Sem) and Nanosimsmentioning

confidence: 99%

“…A. aerophoba data n = 10. D. avara feeding data from [22] (n = 6) and pumping data from [7] (n = 10). DOC dissolved organic carbon, POC particulate organic carbon.…”

Section: Dom Is Assimilated By Both Host and Symbiont Cellsmentioning

confidence: 99%

“…HMA sponges have been considered better adapted for DOM uptake due to: (1) higher symbiont densities and (2) slower pumping rates which increase the residence time of water in the sponge aquiferous system and therefore the contact time for the cells to access DOM [6]. However, the relationship between HMA/LMA status and pumping rate has recently been questioned [7] and we found limited evidence that decreased pumping resulted in increased DOM uptake as we consistently found similar enrichments in host and symbiont cells of both species despite differences in pumping rate (Fig. 4).…”

Section: Dom Is Assimilated By Both Host and Symbiont Cellsmentioning

confidence: 99%

“…These sessile, filter-feeding invertebrates are ubiquitous from the tropics to the poles and from freshwater mountain lakes to the deep-sea floor thousands of meters deep [3]. In the many ecosystems where they are abundant (e.g., coral reefs and sponge grounds), sponges play a major role in nutrient cycles [4,5], due to both their unrivaled capacity to filter seawater [6,7] and their association with diverse and abundant microbial symbionts [7,8]. Sponges and their symbionts have evolved multiple nutritional strategies to cope with the vastly different environments they occupy, including photosynthesis on shallow, oligotrophic coral reefs [9], chemosynthesis at hydro-carbon seeps [10], and even carnivory in the food-limited deep-sea [11]; however, the majority of sponges are chiefly heterotrophic filter-feeders that capture food using specialized feeding cells (choanocytes).…”

Section: Introductionmentioning

confidence: 99%

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Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

et al. 2020

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Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean.

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Section: Dom Is Assimilated By Both Host and Symbiont Cellsmentioning

confidence: 77%

Section: Scanning Electron Microscopy (Sem) and Nanosimsmentioning

confidence: 99%

“…A. aerophoba data n = 10. D. avara feeding data from [22] (n = 6) and pumping data from [7] (n = 10). DOC dissolved organic carbon, POC particulate organic carbon.…”

Section: Dom Is Assimilated By Both Host and Symbiont Cellsmentioning

confidence: 99%

Section: Dom Is Assimilated By Both Host and Symbiont Cellsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

et al. 2020

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Deep‐sea sponge derived environmental DNA analysis reveals demersal fish biodiversity of a remote Arctic ecosystem

Brodnicke,

Meyer,

Busch

et al. 2023

Environmental DNA

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The deep‐sea is vast, remote, and largely underexplored. However, methodological advances in environmental DNA (eDNA) surveys could aid in the exploration efforts, such as using sponges as natural eDNA filters for studying fish biodiversity. In this study, we analyzed the eDNA from 116 sponge tissue samples and compared these to 18 water eDNA samples and visual surveys obtained on an Arctic seamount. Across survey methods, we revealed approximately 30% of the species presumed to inhabit this area and 11 fish species were detected via sponge derived eDNA alone. These included commercially important fish such as the Greenland halibut and Atlantic mackerel. Fish eDNA detection was highly variable across sponge samples. Highest detection rates were found in sponges with low microbial activity such as those from the class Hexactinellida. The different survey methods also detected alternate fish communities, highlighted by only one species overlap between the visual surveys and the sponge eDNA samples. Therefore, we conclude that sponge eDNA can be a useful tool for surveying deep‐sea demersal fish communities and it synergises with visual surveys improving overall biodiversity assessments. Datasets such as this can form comprehensive baselines on fish biodiversity across seamounts, which in turn can inform marine management and conservation practices in the regions where such surveys are undertaken.

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Dissolved organic carbon (DOC) is essential to balance the metabolic demands of four dominant North‐Atlantic deep‐sea sponges

Bart

Mueller

Rombouts

et al. 2020

Limnology & Oceanography

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Sponges are ubiquitous components of various deep-sea habitats, including cold water coral reefs, and form deep-sea sponge grounds. Although the deep sea is generally considered to be a food-limited environment, these ecosystems are known to be hotspots of biodiversity and carbon cycling. To assess the role of sponges in the carbon cycling of deep-sea ecosystems, we studied the carbon budgets of six dominant deep-sea sponges of different phylogenetic origin, with various growth forms and hosting distinct associated microbial communities, in an ex situ aquarium setup. Additionally, we determined biomass metrics-planar surface area, volume, wet weight, dry weight (DW), ash-free dry weight, and organic carbon (C) content-and conversion factors for all species. Oxygen (O 2) removal rates averaged 3.3 ± 2.8 μmol O 2 g DW sponge h −1 (mean ± SD), live particulate (bacterio-and phytoplankton) organic carbon removal rates averaged 0.30 ± 0.39 μmol C g DW sponge h −1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 μmol C g DW sponge h −1. Carbon mass balances were calculated for four species and revealed that the sponges acquired 1.3-6.6 times the amount of carbon needed to sustain their minimal respiratory demands. These results indicate that irrespective of taxonomic class, growth form, and abundance of microbial symbionts, DOC is responsible for over 90% of the total net organic carbon removal of deep-sea sponges and allows them to sustain themselves in otherwise food-limited environments on the ocean floor.

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Size Is the Major Determinant of Pumping Rates in Marine Sponges

Cited by 74 publications

References 103 publications

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

Deep‐sea sponge derived environmental DNA analysis reveals demersal fish biodiversity of a remote Arctic ecosystem

Dissolved organic carbon (DOC) is essential to balance the metabolic demands of four dominant North‐Atlantic deep‐sea sponges

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