Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution
Holobionts formed by a host organism and associated symbionts are key biological units in marine ecosystems where they are responsible for fundamental ecosystem services. Therefore, understanding anthropogenic impacts on holobionts is essential. Sponges (Phylum Porifera) are ideal holobiont models....
| Main Authors: | , , , , |
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| Format: | Journal Article |
| Language: | English |
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2022
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| Online Access: | https://hdl.handle.net/10356/163823 |
| _version_ | 1811692047119155200 |
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| author | Vad, Johanne Suja, Laura Duran Summers, Stephen Henry, Theodore B. Roberts, J. Murray |
| author2 | Singapore Centre for Environmental Life Sciences and Engineering |
| author_facet | Singapore Centre for Environmental Life Sciences and Engineering Vad, Johanne Suja, Laura Duran Summers, Stephen Henry, Theodore B. Roberts, J. Murray |
| author_sort | Vad, Johanne |
| collection | NTU |
| description | Holobionts formed by a host organism and associated symbionts are key biological units in marine ecosystems where they are responsible for fundamental ecosystem services. Therefore, understanding anthropogenic impacts on holobionts is essential. Sponges (Phylum Porifera) are ideal holobiont models. They host a complex microbial community and provide ecosystem services including nutrient cycling. At bathyal depths, sponges can accumulate forming dense sponge ground habitats supporting biodiverse associated communities. However, the impacts of spilled oil and dispersants on sponge grounds cannot be understood without considering exposures mediated through sponge filtration of marine snow particles. To examine this, we exposed the model sponge Halichondria panicea to oil, dispersant and "marine oil snow" contaminated seawater and elucidate the complex molecular response of the holobiont through metatranscriptomics. While the host response included detoxification and immune response pathways, the bacterial symbiotic response differed and was at least partially the result of a change in the host environment rather than a direct response to hydrocarbon exposure. As the sponge host reduced its pumping activity and internal tissue oxygen levels declined, the symbionts changed their metabolism from aerobic to anaerobic pathways possibly via quorum sensing. Furthermore, we found evidence of hydrocarbon degradation by sponge symbionts, but sponge mortality (even when exposed to low concentrations of hydrocarbons) implied this may not provide the holobiont with sufficient resilience against contaminants. Given the continued proposed expansion of hydrocarbon production into deep continental shelf and slope settings where sponge grounds form significant habitats it is important that dispersant use is minimised and that environmental impact assessments carefully consider the vulnerability of sponge holobionts. |
| first_indexed | 2024-10-01T06:29:34Z |
| format | Journal Article |
| id | ntu-10356/163823 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2024-10-01T06:29:34Z |
| publishDate | 2022 |
| record_format | dspace |
| spelling | ntu-10356/1638232022-12-24T23:31:48Z Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution Vad, Johanne Suja, Laura Duran Summers, Stephen Henry, Theodore B. Roberts, J. Murray Singapore Centre for Environmental Life Sciences and Engineering Engineering::Environmental engineering Holobiont Marine Snow Holobionts formed by a host organism and associated symbionts are key biological units in marine ecosystems where they are responsible for fundamental ecosystem services. Therefore, understanding anthropogenic impacts on holobionts is essential. Sponges (Phylum Porifera) are ideal holobiont models. They host a complex microbial community and provide ecosystem services including nutrient cycling. At bathyal depths, sponges can accumulate forming dense sponge ground habitats supporting biodiverse associated communities. However, the impacts of spilled oil and dispersants on sponge grounds cannot be understood without considering exposures mediated through sponge filtration of marine snow particles. To examine this, we exposed the model sponge Halichondria panicea to oil, dispersant and "marine oil snow" contaminated seawater and elucidate the complex molecular response of the holobiont through metatranscriptomics. While the host response included detoxification and immune response pathways, the bacterial symbiotic response differed and was at least partially the result of a change in the host environment rather than a direct response to hydrocarbon exposure. As the sponge host reduced its pumping activity and internal tissue oxygen levels declined, the symbionts changed their metabolism from aerobic to anaerobic pathways possibly via quorum sensing. Furthermore, we found evidence of hydrocarbon degradation by sponge symbionts, but sponge mortality (even when exposed to low concentrations of hydrocarbons) implied this may not provide the holobiont with sufficient resilience against contaminants. Given the continued proposed expansion of hydrocarbon production into deep continental shelf and slope settings where sponge grounds form significant habitats it is important that dispersant use is minimised and that environmental impact assessments carefully consider the vulnerability of sponge holobionts. Published version This study received support from the Marine Alliance for Science and Technology for Scotland (grant number OGSG14) and from the NERC Natural Environment Research Council Centre for Doctoral Training in Oil & Gas. This study was part of the European Union’s Horizon 2020 Research and Innovation Programme under grant agreement No. 678760 (ATLAS) and No. 818123 (iAtlantic). 2022-12-19T05:26:33Z 2022-12-19T05:26:33Z 2022 Journal Article Vad, J., Suja, L. D., Summers, S., Henry, T. B. & Roberts, J. M. (2022). Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution. Frontiers in Microbiology, 13, 909853-. https://dx.doi.org/10.3389/fmicb.2022.909853 1664-302X https://hdl.handle.net/10356/163823 10.3389/fmicb.2022.909853 35910618 2-s2.0-85135152826 13 909853 en Frontiers in Microbiology © 2022 Vad, Duran Suja, Summers, Henry and Roberts. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. application/pdf |
| spellingShingle | Engineering::Environmental engineering Holobiont Marine Snow Vad, Johanne Suja, Laura Duran Summers, Stephen Henry, Theodore B. Roberts, J. Murray Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution |
| title | Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution |
| title_full | Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution |
| title_fullStr | Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution |
| title_full_unstemmed | Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution |
| title_short | Marine sponges in a snowstorm - extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution |
| title_sort | marine sponges in a snowstorm extreme sensitivity of a sponge holobiont to marine oil snow and chemically dispersed oil pollution |
| topic | Engineering::Environmental engineering Holobiont Marine Snow |
| url | https://hdl.handle.net/10356/163823 |
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