Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities
In the Western Tropical South Pacific (WTSP) Ocean, a hotspot of dinitrogen fixation has been identified. The survival of diazotrophs depends, among others, on the availability of dissolved iron (DFe) largely originating, as recently revealed, from shallow hydrothermal sources located along the Tong...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2023.1082077/full |
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| author | Chloé Tilliette Frédéric Gazeau Gemma Portlock Mar Benavides Sophie Bonnet Catherine Guigue Nathalie Leblond Caroline Lory Dominique Marie Maryline Montanes Elvira Pulido-Villena Géraldine Sarthou Marc Tedetti Maria-Elena Vorrath Hannah Whitby Cécile Guieu |
| author_facet | Chloé Tilliette Frédéric Gazeau Gemma Portlock Mar Benavides Sophie Bonnet Catherine Guigue Nathalie Leblond Caroline Lory Dominique Marie Maryline Montanes Elvira Pulido-Villena Géraldine Sarthou Marc Tedetti Maria-Elena Vorrath Hannah Whitby Cécile Guieu |
| author_sort | Chloé Tilliette |
| collection | DOAJ |
| description | In the Western Tropical South Pacific (WTSP) Ocean, a hotspot of dinitrogen fixation has been identified. The survival of diazotrophs depends, among others, on the availability of dissolved iron (DFe) largely originating, as recently revealed, from shallow hydrothermal sources located along the Tonga-Kermadec arc that fertilize the Lau Basin with this element. On the opposite, these fluids, released directly close to the photic layer, can introduce numerous trace metals at concentrations that can be toxic to surface communities. Here, we performed an innovative 9-day experiment in 300 L reactors onboard the TONGA expedition, to examine the effects of hydrothermal fluids on natural plankton communities in the WTSP Ocean. Different volumes of fluids were mixed with non-hydrothermally influenced surface waters (mixing ratio from 0 to 14.5%) and the response of the communities was studied by monitoring numerous stocks and fluxes (phytoplankton biomass, community composition, net community production, N2 fixation, thiol production, organic carbon and metal concentrations in exported material). Despite an initial toxic effect of hydrothermal fluids on phytoplankton communities, these inputs led to higher net community production and N2 fixation rates, as well as elevated export of organic matter relative to control. This fertilizing effect was achieved through detoxification of the environment, rich in potentially toxic elements (e.g., Cu, Cd, Hg), likely by resistant Synechococcus ecotypes able to produce strong binding ligands, especially thiols (thioacetamide-like and glutathione-like compounds). The striking increase of thiols quickly after fluid addition likely detoxified the environment, rendering it more favorable for phytoplankton growth. Indeed, phytoplankton groups stressed by the addition of fluids were then able to recover important growth rates, probably favored by the supply of numerous fertilizing trace metals (notably Fe) from hydrothermal fluids and new nitrogen provided by N2 fixation. These experimental results are in good agreement with in-situ observations, proving the causal link between the supply of hydrothermal fluids emitted at shallow depth into the surface layer and the intense biological productivity largely supported by diazotrophs in the WTSP Ocean. This study highlights the importance of considering shallow hydrothermal systems for a better understanding of the biological carbon pump. |
| first_indexed | 2024-04-09T13:13:30Z |
| format | Article |
| id | doaj.art-78c106a3572e4d51bd5b1695461cf395 |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-04-09T13:13:30Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-78c106a3572e4d51bd5b1695461cf3952023-05-12T05:49:55ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452023-05-011010.3389/fmars.2023.10820771082077Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communitiesChloé Tilliette0Frédéric Gazeau1Gemma Portlock2Mar Benavides3Sophie Bonnet4Catherine Guigue5Nathalie Leblond6Caroline Lory7Dominique Marie8Maryline Montanes9Elvira Pulido-Villena10Géraldine Sarthou11Marc Tedetti12Maria-Elena Vorrath13Hannah Whitby14Cécile Guieu15Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche, LOV, Villefranche-sur-Mer, FranceSorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche, LOV, Villefranche-sur-Mer, FranceDepartment of Earth, Ocean and Ecological Sciences, School of Environmental Sciences, University of Liverpool, Liverpool, United KingdomAix Marseille Univ., Université de Toulon, CNRS, IRD, MIO, Marseille, FranceAix Marseille Univ., Université de Toulon, CNRS, IRD, MIO, Marseille, FranceAix Marseille Univ., Université de Toulon, CNRS, IRD, MIO, Marseille, FranceSorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche, LOV, Villefranche-sur-Mer, FranceAix Marseille Univ., Université de Toulon, CNRS, IRD, MIO, Marseille, FranceCNRS, Sorbonne Université, UMR7144, Team ECOMAP, Station Biologique de Roscoff, Roscoff, FranceSorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche, LOV, Villefranche-sur-Mer, FranceAix Marseille Univ., Université de Toulon, CNRS, IRD, MIO, Marseille, FranceUniversity of Brest, CNRS, IRD, Ifremer, LEMAR, Plouzané, FranceAix Marseille Univ., Université de Toulon, CNRS, IRD, MIO, Marseille, FranceIntitut für Geologie, University Hamburg, Hamburg, GermanyDepartment of Earth, Ocean and Ecological Sciences, School of Environmental Sciences, University of Liverpool, Liverpool, United KingdomSorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche, LOV, Villefranche-sur-Mer, FranceIn the Western Tropical South Pacific (WTSP) Ocean, a hotspot of dinitrogen fixation has been identified. The survival of diazotrophs depends, among others, on the availability of dissolved iron (DFe) largely originating, as recently revealed, from shallow hydrothermal sources located along the Tonga-Kermadec arc that fertilize the Lau Basin with this element. On the opposite, these fluids, released directly close to the photic layer, can introduce numerous trace metals at concentrations that can be toxic to surface communities. Here, we performed an innovative 9-day experiment in 300 L reactors onboard the TONGA expedition, to examine the effects of hydrothermal fluids on natural plankton communities in the WTSP Ocean. Different volumes of fluids were mixed with non-hydrothermally influenced surface waters (mixing ratio from 0 to 14.5%) and the response of the communities was studied by monitoring numerous stocks and fluxes (phytoplankton biomass, community composition, net community production, N2 fixation, thiol production, organic carbon and metal concentrations in exported material). Despite an initial toxic effect of hydrothermal fluids on phytoplankton communities, these inputs led to higher net community production and N2 fixation rates, as well as elevated export of organic matter relative to control. This fertilizing effect was achieved through detoxification of the environment, rich in potentially toxic elements (e.g., Cu, Cd, Hg), likely by resistant Synechococcus ecotypes able to produce strong binding ligands, especially thiols (thioacetamide-like and glutathione-like compounds). The striking increase of thiols quickly after fluid addition likely detoxified the environment, rendering it more favorable for phytoplankton growth. Indeed, phytoplankton groups stressed by the addition of fluids were then able to recover important growth rates, probably favored by the supply of numerous fertilizing trace metals (notably Fe) from hydrothermal fluids and new nitrogen provided by N2 fixation. These experimental results are in good agreement with in-situ observations, proving the causal link between the supply of hydrothermal fluids emitted at shallow depth into the surface layer and the intense biological productivity largely supported by diazotrophs in the WTSP Ocean. This study highlights the importance of considering shallow hydrothermal systems for a better understanding of the biological carbon pump. https://www.frontiersin.org/articles/10.3389/fmars.2023.1082077/fullhydrothermal fluidsphytoplankton communitiestrace metalfertilizing effecttoxic effectWestern Tropical South Pacific |
| spellingShingle | Chloé Tilliette Frédéric Gazeau Gemma Portlock Mar Benavides Sophie Bonnet Catherine Guigue Nathalie Leblond Caroline Lory Dominique Marie Maryline Montanes Elvira Pulido-Villena Géraldine Sarthou Marc Tedetti Maria-Elena Vorrath Hannah Whitby Cécile Guieu Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities Frontiers in Marine Science hydrothermal fluids phytoplankton communities trace metal fertilizing effect toxic effect Western Tropical South Pacific |
| title | Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities |
| title_full | Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities |
| title_fullStr | Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities |
| title_full_unstemmed | Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities |
| title_short | Influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities |
| title_sort | influence of shallow hydrothermal fluid release on the functioning of phytoplankton communities |
| topic | hydrothermal fluids phytoplankton communities trace metal fertilizing effect toxic effect Western Tropical South Pacific |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2023.1082077/full |
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