Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates Degradation
In the dark ocean, the balance between the heterotrophic carbon demand and the supply of sinking carbon through the biological carbon pump remains poorly constrained. In situ tracking of the dynamics of microbial degradation processes occurring on the gravitational sinking particles is still challen...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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MDPI AG
2021-09-01
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| Series: | Water |
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| Online Access: | https://www.mdpi.com/2073-4441/13/19/2616 |
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| author | Christian Tamburini Marc Garel Aude Barani Dominique Boeuf Patricia Bonin Nagib Bhairy Sophie Guasco Stéphanie Jacquet Frédéric A. C. Le Moigne Christos Panagiotopoulos Virginie Riou Sandrine Veloso Chiara Santinelli Fabrice Armougom |
| author_facet | Christian Tamburini Marc Garel Aude Barani Dominique Boeuf Patricia Bonin Nagib Bhairy Sophie Guasco Stéphanie Jacquet Frédéric A. C. Le Moigne Christos Panagiotopoulos Virginie Riou Sandrine Veloso Chiara Santinelli Fabrice Armougom |
| author_sort | Christian Tamburini |
| collection | DOAJ |
| description | In the dark ocean, the balance between the heterotrophic carbon demand and the supply of sinking carbon through the biological carbon pump remains poorly constrained. In situ tracking of the dynamics of microbial degradation processes occurring on the gravitational sinking particles is still challenging. Our particle sinking simulator system (PASS) intends to mimic as closely as possible the in situ variations in pressure and temperature experienced by gravitational sinking particles. Here, we used the PASS to simultaneously track geochemical and microbial changes that occurred during the sinking through the mesopelagic zone of laboratory-grown <i>Emiliania huxleyi</i> aggregates amended by a natural microbial community sampled at 105 m depth in the North Atlantic Ocean. The impact of pressure on the prokaryotic degradation of POC and dissolution of <i>E. huxleyi</i>-derived calcite was not marked compared to atmospheric pressure. In contrast, using global O<sub>2</sub> consumption monitored in real-time inside the high-pressure bottles using planar optodes via a sapphire window, a reduction of respiration rate was recorded in surface-originated community assemblages under increasing pressure conditions. Moreover, using a 16S rRNA metabarcoding survey, we demonstrated a drastic difference in transcriptionally active prokaryotes associated with particles, incubated either at atmospheric pressure or under linearly increasing hydrostatic pressure conditions. The increase in hydrostatic pressure reduced both the phylogenetic diversity and the species richness. The incubation at atmospheric pressure, however, promoted an opportunistic community of “fast” degraders from the surface (<i>Saccharospirillaceae</i>, <i>Hyphomonadaceae,</i> and <i>Pseudoalteromonadaceae</i>), known to be associated with surface phytoplankton blooms. In contrast, the incubation under increasing pressure condition incubations revealed an increase in the particle colonizer families <i>Flavobacteriaceae</i> and <i>Rhodobacteraceae</i>, and also <i>Colwelliaceae,</i> which are known to be adapted to high hydrostatic pressure. Altogether, our results underline the need to perform biodegradation experiments of particles in conditions that mimic pressure and temperature encountered during their sinking along the water column to be ecologically relevant. |
| first_indexed | 2024-03-10T06:49:36Z |
| format | Article |
| id | doaj.art-d167a2cf0a0e4c328ce631cb7ee80015 |
| institution | Directory Open Access Journal |
| issn | 2073-4441 |
| language | English |
| last_indexed | 2024-03-10T06:49:36Z |
| publishDate | 2021-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Water |
| spelling | doaj.art-d167a2cf0a0e4c328ce631cb7ee800152023-11-22T16:59:53ZengMDPI AGWater2073-44412021-09-011319261610.3390/w13192616Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates DegradationChristian Tamburini0Marc Garel1Aude Barani2Dominique Boeuf3Patricia Bonin4Nagib Bhairy5Sophie Guasco6Stéphanie Jacquet7Frédéric A. C. Le Moigne8Christos Panagiotopoulos9Virginie Riou10Sandrine Veloso11Chiara Santinelli12Fabrice Armougom13Aix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceSorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologies Microbiennes, USR3579, Observatoire Océanologique, 66650 Banyuls-sur-Mer, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceC.N.R., Istituto di Biofisica, 56124 Pisa, ItalyAix Marseille Univ., Universite de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, FranceIn the dark ocean, the balance between the heterotrophic carbon demand and the supply of sinking carbon through the biological carbon pump remains poorly constrained. In situ tracking of the dynamics of microbial degradation processes occurring on the gravitational sinking particles is still challenging. Our particle sinking simulator system (PASS) intends to mimic as closely as possible the in situ variations in pressure and temperature experienced by gravitational sinking particles. Here, we used the PASS to simultaneously track geochemical and microbial changes that occurred during the sinking through the mesopelagic zone of laboratory-grown <i>Emiliania huxleyi</i> aggregates amended by a natural microbial community sampled at 105 m depth in the North Atlantic Ocean. The impact of pressure on the prokaryotic degradation of POC and dissolution of <i>E. huxleyi</i>-derived calcite was not marked compared to atmospheric pressure. In contrast, using global O<sub>2</sub> consumption monitored in real-time inside the high-pressure bottles using planar optodes via a sapphire window, a reduction of respiration rate was recorded in surface-originated community assemblages under increasing pressure conditions. Moreover, using a 16S rRNA metabarcoding survey, we demonstrated a drastic difference in transcriptionally active prokaryotes associated with particles, incubated either at atmospheric pressure or under linearly increasing hydrostatic pressure conditions. The increase in hydrostatic pressure reduced both the phylogenetic diversity and the species richness. The incubation at atmospheric pressure, however, promoted an opportunistic community of “fast” degraders from the surface (<i>Saccharospirillaceae</i>, <i>Hyphomonadaceae,</i> and <i>Pseudoalteromonadaceae</i>), known to be associated with surface phytoplankton blooms. In contrast, the incubation under increasing pressure condition incubations revealed an increase in the particle colonizer families <i>Flavobacteriaceae</i> and <i>Rhodobacteraceae</i>, and also <i>Colwelliaceae,</i> which are known to be adapted to high hydrostatic pressure. Altogether, our results underline the need to perform biodegradation experiments of particles in conditions that mimic pressure and temperature encountered during their sinking along the water column to be ecologically relevant.https://www.mdpi.com/2073-4441/13/19/2616biological carbon pumpcarbon cyclemesopelagicmineral ballastcoccolithophorid<i>Emiliania huxleyi</i> |
| spellingShingle | Christian Tamburini Marc Garel Aude Barani Dominique Boeuf Patricia Bonin Nagib Bhairy Sophie Guasco Stéphanie Jacquet Frédéric A. C. Le Moigne Christos Panagiotopoulos Virginie Riou Sandrine Veloso Chiara Santinelli Fabrice Armougom Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates Degradation Water biological carbon pump carbon cycle mesopelagic mineral ballast coccolithophorid <i>Emiliania huxleyi</i> |
| title | Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates Degradation |
| title_full | Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates Degradation |
| title_fullStr | Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates Degradation |
| title_full_unstemmed | Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates Degradation |
| title_short | Increasing Hydrostatic Pressure Impacts the Prokaryotic Diversity during <i>Emiliania huxleyi</i> Aggregates Degradation |
| title_sort | increasing hydrostatic pressure impacts the prokaryotic diversity during i emiliania huxleyi i aggregates degradation |
| topic | biological carbon pump carbon cycle mesopelagic mineral ballast coccolithophorid <i>Emiliania huxleyi</i> |
| url | https://www.mdpi.com/2073-4441/13/19/2616 |
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