Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915)

Georgios Kazanidis; Dick van Oevelen; Bart Veuger; Ursula F. M. Witte

doi:10.1016/j.dsr.2018.07.009

Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915)

Georgios Kazanidis^* (Corresponding Author), Dick van Oevelen, Bart Veuger, Ursula F. M. Witte

^*Corresponding author for this work

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Abstract

Sponges are often major players in the functioning of shallow-water ecosystems through their high biomass and high capacity in filter feeding. In comparison, little is known about the feeding and metabolic strategies of deep-sea sponges, although they can also form dense aggregations with high biomass. This situation hinders our understanding about how some sponge species thrive under the often food-limited conditions of the deep sea. In the present study we examined the feeding and metabolic strategies of 1) the massive demosponge Spongosorites coralliophaga, which was recently described as an important ecosystem engineer in cold-water coral reefs (CWCRs) and 2) the anthozoan Parazoanthus anguicomus and the ophiuroid Ophiura ophiura, i.e. two dominant epibionts on S. coralliophaga. All three benthic species have high density at CWCRs of the North-East Atlantic and knowing their feeding strategies facilitates future studies on carbon (C) and nitrogen (N) cycling at CWCRs. The on-board feeding experiments examined the processing of four isotopically-labelled food sources, namely ¹⁵N-ammonium chloride, ¹³C-glucose, ¹³C/¹⁵N-labelled microalgae, ¹³C/¹⁵N-labelled bacteria by S. coralliophaga and its symbiotic bacteria and the epibionts P. anguicomus and O. ophiura from the Mingulay reef complex and the Logachev mound (North-East Atlantic). There were no significant differences among the three species in terms of biomass-specific C and N assimilation rates; however, there were differences among S. coralliophaga, P. anguicomus and O. ophiura in how they processed the food sources and this is may be linked to interspecific variability in metabolic needs. S. coralliophaga preferentially assimilated particulate organic N (PON) over particulate organic C (POC) while this was not the case for P. anguicomus and O. ophiura. We did not detect the ¹⁵N tracer in the bacterial biomarker D-Alanine suggesting that the preferential assimilation of N over C in S. coralliophaga was mediated by sponge cells instead of the bacterial symbionts. S. coralliophaga assimilated C and N from all four food sources and this versatile feeding strategy was accompanied by an ability for de novo synthesis of essential and non-essential hydrolysable amino acids (HAAs). We suggest that the recorded feeding and metabolic flexibility of S. coralliophaga plays an important role in the survival of this massive sponge under food-limited conditions in the deep sea.

Original language	English
Pages (from-to)	71-82
Number of pages	11
Journal	Deep Sea Research Part I: Oceanographic Research Papers
Volume	141
Early online date	18 Jul 2018
DOIs	https://doi.org/10.1016/j.dsr.2018.07.009
Publication status	Published - Nov 2018

Bibliographical note

Thanks to Bill Richardson (Master) and the crew of the Royal Research Ship “James Cook” during the JC073 “Changing Oceans” expedition, Will Handley and the Holland-I ROV team. Also thanks to Dr Christina Mueller and Dr Evina Gontikaki for their guidance on experimental set-up and sample preparation for stable isotope analysis. Funding for the JC073 cruise was provided by the Natural Environment Research Council (NERC) UK Ocean Acidification (UKOA) research programme’s Benthic Consortium project (NE/H017305/1 to J Murray Roberts). Funding for the field work and analytical costs was provided by the Marine Alliance for Science and Technology for Scotland (MASTS) (Biodiversity Grant to UW, 140 SF10003-10, Deep-Sea Forum Small Grant DSSG4 awarded to GK) and by the Netherlands Organisation for Scientific Research (awarded to DvO). GK was funded by a MASTS PhD scholarship. The ATLAS project has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No 678760 (ATLAS). This output reflects only the author’s views, and the European Union cannot be held responsible for any use that may be made of the information contained therein. The funding sources had no involvement in study design, the collection, analysis and interpretation of data, in the writing of the report, and in the decision to submit the article for publication. The authors would like to thank the two reviewers of the manuscript for their constructive comments.

Keywords

cold-water reefs (CWCRs)
sponges
epibionts
essential amino acids
bentho-pelagic coupling
marine food webs

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Ursula Witte
Person: Academic

Cite this

Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915). / Kazanidis, Georgios (Corresponding Author); van Oevelen, Dick; Veuger, Bart et al.
In: Deep Sea Research Part I: Oceanographic Research Papers, Vol. 141, 11.2018, p. 71-82.

Research output: Contribution to journal › Article › peer-review

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title = "Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915)",

abstract = "Sponges are often major players in the functioning of shallow-water ecosystems through their high biomass and high capacity in filter feeding. In comparison, little is known about the feeding and metabolic strategies of deep-sea sponges, although they can also form dense aggregations with high biomass. This situation hinders our understanding about how some sponge species thrive under the often food-limited conditions of the deep sea. In the present study we examined the feeding and metabolic strategies of 1) the massive demosponge Spongosorites coralliophaga, which was recently described as an important ecosystem engineer in cold-water coral reefs (CWCRs) and 2) the anthozoan Parazoanthus anguicomus and the ophiuroid Ophiura ophiura, i.e. two dominant epibionts on S. coralliophaga. All three benthic species have high density at CWCRs of the North-East Atlantic and knowing their feeding strategies facilitates future studies on carbon (C) and nitrogen (N) cycling at CWCRs. The on-board feeding experiments examined the processing of four isotopically-labelled food sources, namely 15N-ammonium chloride, 13C-glucose, 13C/15N-labelled microalgae, 13C/15N-labelled bacteria by S. coralliophaga and its symbiotic bacteria and the epibionts P. anguicomus and O. ophiura from the Mingulay reef complex and the Logachev mound (North-East Atlantic). There were no significant differences among the three species in terms of biomass-specific C and N assimilation rates; however, there were differences among S. coralliophaga, P. anguicomus and O. ophiura in how they processed the food sources and this is may be linked to interspecific variability in metabolic needs. S. coralliophaga preferentially assimilated particulate organic N (PON) over particulate organic C (POC) while this was not the case for P. anguicomus and O. ophiura. We did not detect the 15N tracer in the bacterial biomarker D-Alanine suggesting that the preferential assimilation of N over C in S. coralliophaga was mediated by sponge cells instead of the bacterial symbionts. S. coralliophaga assimilated C and N from all four food sources and this versatile feeding strategy was accompanied by an ability for de novo synthesis of essential and non-essential hydrolysable amino acids (HAAs). We suggest that the recorded feeding and metabolic flexibility of S. coralliophaga plays an important role in the survival of this massive sponge under food-limited conditions in the deep sea.",

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note = "Thanks to Bill Richardson (Master) and the crew of the Royal Research Ship “James Cook” during the JC073 “Changing Oceans” expedition, Will Handley and the Holland-I ROV team. Also thanks to Dr Christina Mueller and Dr Evina Gontikaki for their guidance on experimental set-up and sample preparation for stable isotope analysis. Funding for the JC073 cruise was provided by the Natural Environment Research Council (NERC) UK Ocean Acidification (UKOA) research programme{\textquoteright}s Benthic Consortium project (NE/H017305/1 to J Murray Roberts). Funding for the field work and analytical costs was provided by the Marine Alliance for Science and Technology for Scotland (MASTS) (Biodiversity Grant to UW, 140 SF10003-10, Deep-Sea Forum Small Grant DSSG4 awarded to GK) and by the Netherlands Organisation for Scientific Research (awarded to DvO). GK was funded by a MASTS PhD scholarship. The ATLAS project has received funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under grant agreement No 678760 (ATLAS). This output reflects only the author{\textquoteright}s views, and the European Union cannot be held responsible for any use that may be made of the information contained therein. The funding sources had no involvement in study design, the collection, analysis and interpretation of data, in the writing of the report, and in the decision to submit the article for publication. The authors would like to thank the two reviewers of the manuscript for their constructive comments.",

year = "2018",

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doi = "10.1016/j.dsr.2018.07.009",

language = "English",

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journal = "Deep Sea Research Part I: Oceanographic Research Papers",

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T1 - Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915)

AU - Kazanidis, Georgios

AU - van Oevelen, Dick

AU - Veuger, Bart

AU - Witte, Ursula F. M.

N1 - Thanks to Bill Richardson (Master) and the crew of the Royal Research Ship “James Cook” during the JC073 “Changing Oceans” expedition, Will Handley and the Holland-I ROV team. Also thanks to Dr Christina Mueller and Dr Evina Gontikaki for their guidance on experimental set-up and sample preparation for stable isotope analysis. Funding for the JC073 cruise was provided by the Natural Environment Research Council (NERC) UK Ocean Acidification (UKOA) research programme’s Benthic Consortium project (NE/H017305/1 to J Murray Roberts). Funding for the field work and analytical costs was provided by the Marine Alliance for Science and Technology for Scotland (MASTS) (Biodiversity Grant to UW, 140 SF10003-10, Deep-Sea Forum Small Grant DSSG4 awarded to GK) and by the Netherlands Organisation for Scientific Research (awarded to DvO). GK was funded by a MASTS PhD scholarship. The ATLAS project has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No 678760 (ATLAS). This output reflects only the author’s views, and the European Union cannot be held responsible for any use that may be made of the information contained therein. The funding sources had no involvement in study design, the collection, analysis and interpretation of data, in the writing of the report, and in the decision to submit the article for publication. The authors would like to thank the two reviewers of the manuscript for their constructive comments.

PY - 2018/11

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N2 - Sponges are often major players in the functioning of shallow-water ecosystems through their high biomass and high capacity in filter feeding. In comparison, little is known about the feeding and metabolic strategies of deep-sea sponges, although they can also form dense aggregations with high biomass. This situation hinders our understanding about how some sponge species thrive under the often food-limited conditions of the deep sea. In the present study we examined the feeding and metabolic strategies of 1) the massive demosponge Spongosorites coralliophaga, which was recently described as an important ecosystem engineer in cold-water coral reefs (CWCRs) and 2) the anthozoan Parazoanthus anguicomus and the ophiuroid Ophiura ophiura, i.e. two dominant epibionts on S. coralliophaga. All three benthic species have high density at CWCRs of the North-East Atlantic and knowing their feeding strategies facilitates future studies on carbon (C) and nitrogen (N) cycling at CWCRs. The on-board feeding experiments examined the processing of four isotopically-labelled food sources, namely 15N-ammonium chloride, 13C-glucose, 13C/15N-labelled microalgae, 13C/15N-labelled bacteria by S. coralliophaga and its symbiotic bacteria and the epibionts P. anguicomus and O. ophiura from the Mingulay reef complex and the Logachev mound (North-East Atlantic). There were no significant differences among the three species in terms of biomass-specific C and N assimilation rates; however, there were differences among S. coralliophaga, P. anguicomus and O. ophiura in how they processed the food sources and this is may be linked to interspecific variability in metabolic needs. S. coralliophaga preferentially assimilated particulate organic N (PON) over particulate organic C (POC) while this was not the case for P. anguicomus and O. ophiura. We did not detect the 15N tracer in the bacterial biomarker D-Alanine suggesting that the preferential assimilation of N over C in S. coralliophaga was mediated by sponge cells instead of the bacterial symbionts. S. coralliophaga assimilated C and N from all four food sources and this versatile feeding strategy was accompanied by an ability for de novo synthesis of essential and non-essential hydrolysable amino acids (HAAs). We suggest that the recorded feeding and metabolic flexibility of S. coralliophaga plays an important role in the survival of this massive sponge under food-limited conditions in the deep sea.

AB - Sponges are often major players in the functioning of shallow-water ecosystems through their high biomass and high capacity in filter feeding. In comparison, little is known about the feeding and metabolic strategies of deep-sea sponges, although they can also form dense aggregations with high biomass. This situation hinders our understanding about how some sponge species thrive under the often food-limited conditions of the deep sea. In the present study we examined the feeding and metabolic strategies of 1) the massive demosponge Spongosorites coralliophaga, which was recently described as an important ecosystem engineer in cold-water coral reefs (CWCRs) and 2) the anthozoan Parazoanthus anguicomus and the ophiuroid Ophiura ophiura, i.e. two dominant epibionts on S. coralliophaga. All three benthic species have high density at CWCRs of the North-East Atlantic and knowing their feeding strategies facilitates future studies on carbon (C) and nitrogen (N) cycling at CWCRs. The on-board feeding experiments examined the processing of four isotopically-labelled food sources, namely 15N-ammonium chloride, 13C-glucose, 13C/15N-labelled microalgae, 13C/15N-labelled bacteria by S. coralliophaga and its symbiotic bacteria and the epibionts P. anguicomus and O. ophiura from the Mingulay reef complex and the Logachev mound (North-East Atlantic). There were no significant differences among the three species in terms of biomass-specific C and N assimilation rates; however, there were differences among S. coralliophaga, P. anguicomus and O. ophiura in how they processed the food sources and this is may be linked to interspecific variability in metabolic needs. S. coralliophaga preferentially assimilated particulate organic N (PON) over particulate organic C (POC) while this was not the case for P. anguicomus and O. ophiura. We did not detect the 15N tracer in the bacterial biomarker D-Alanine suggesting that the preferential assimilation of N over C in S. coralliophaga was mediated by sponge cells instead of the bacterial symbionts. S. coralliophaga assimilated C and N from all four food sources and this versatile feeding strategy was accompanied by an ability for de novo synthesis of essential and non-essential hydrolysable amino acids (HAAs). We suggest that the recorded feeding and metabolic flexibility of S. coralliophaga plays an important role in the survival of this massive sponge under food-limited conditions in the deep sea.

KW - cold-water reefs (CWCRs)

KW - sponges

KW - epibionts

KW - essential amino acids

KW - bentho-pelagic coupling

KW - marine food webs

U2 - 10.1016/j.dsr.2018.07.009

DO - 10.1016/j.dsr.2018.07.009

M3 - Article

SN - 0967-0637

VL - 141

SP - 71

EP - 82

JO - Deep Sea Research Part I: Oceanographic Research Papers

JF - Deep Sea Research Part I: Oceanographic Research Papers

ER -

Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915)

Abstract

Bibliographical note

Keywords

UN SDGs

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Ursula Witte

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