Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs
The oceanic dissolved organic phosphorus (DOP) pool is mainly composed of P-esters and, to a lesser extent, equally abundant phosphonate and P-anhydride molecules. In phosphate-limited ocean regions, diazotrophs are thought to rely on DOP compounds as an alternative source of phosphorus (P). While b...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-07-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2022.923765/full |
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| author | Alba Filella Alba Filella Lasse Riemann France Van Wambeke Elvira Pulido-Villena Angela Vogts Sophie Bonnet Olivier Grosso Julia M. Diaz Solange Duhamel Mar Benavides Mar Benavides |
| author_facet | Alba Filella Alba Filella Lasse Riemann France Van Wambeke Elvira Pulido-Villena Angela Vogts Sophie Bonnet Olivier Grosso Julia M. Diaz Solange Duhamel Mar Benavides Mar Benavides |
| author_sort | Alba Filella |
| collection | DOAJ |
| description | The oceanic dissolved organic phosphorus (DOP) pool is mainly composed of P-esters and, to a lesser extent, equally abundant phosphonate and P-anhydride molecules. In phosphate-limited ocean regions, diazotrophs are thought to rely on DOP compounds as an alternative source of phosphorus (P). While both P-esters and phosphonates effectively promote dinitrogen (N2) fixation, the role of P-anhydrides for diazotrophs is unknown. Here we explore the effect of P-anhydrides on N2 fixation at two stations with contrasting biogeochemical conditions: one located in the Tonga trench volcanic arc region (“volcano,” with low phosphate and high iron concentrations), and the other in the South Pacific Gyre (“gyre,” with moderate phosphate and low iron). We incubated surface seawater with AMP (P-ester), ATP (P-ester and P-anhydride), or 3polyP (P-anhydride) and determined cell-specific N2 fixation rates, nifH gene abundance, and transcription in Crocosphaera and Trichodesmium. Trichodesmium did not respond to any DOP compounds added, suggesting that they were not P-limited at the volcano station and were outcompeted by the low iron conditions at the gyre station. Conversely, Crocosphaera were numerous at both stations and their specific N2 fixation rates were stimulated by AMP at the volcano station and slightly by 3polyP at both stations. Heterotrophic bacteria responded to ATP and 3polyP additions similarly at both stations, despite the contrasting phosphate and iron availability. The use of 3polyP by Crocosphaera and heterotrophic bacteria at both low and moderate phosphate concentrations suggests that this compound, in addition to being a source of P, can be used to acquire energy for which both groups compete. P-anhydrides may thus leverage energy restrictions to diazotrophs in the future stratified and nutrient-impoverished ocean. |
| first_indexed | 2024-04-10T17:00:45Z |
| format | Article |
| id | doaj.art-7c339fba8fad40fc9852456e364ee7ed |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-04-10T17:00:45Z |
| publishDate | 2022-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-7c339fba8fad40fc9852456e364ee7ed2023-02-06T15:06:15ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-07-01910.3389/fmars.2022.923765923765Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine DiazotrophsAlba Filella0Alba Filella1Lasse Riemann2France Van Wambeke3Elvira Pulido-Villena4Angela Vogts5Sophie Bonnet6Olivier Grosso7Julia M. Diaz8Solange Duhamel9Mar Benavides10Mar Benavides11Aix Marseille Univ, Université de Toulon, CNRS, IRD, Marseille, FranceTuring Center for Living Systems, Aix-Marseille University, Marseille, FranceMarine Biological Section, Department of Biology, University of Copenhagen, Helsingør, DenmarkAix Marseille Univ, Université de Toulon, CNRS, IRD, Marseille, FranceAix Marseille Univ, Université de Toulon, CNRS, IRD, Marseille, FranceDepartment of Biological Oceanography, Leibniz Institute for Baltic Sea Research, Rostock, GermanyAix Marseille Univ, Université de Toulon, CNRS, IRD, Marseille, FranceAix Marseille Univ, Université de Toulon, CNRS, IRD, Marseille, FranceScripps Institution of Oceanography, University of California San Diego, La Jolla, CA, United StatesDepartment of Molecular and Cellular Biology, The University of Arizona, Tucson, AZ, United StatesAix Marseille Univ, Université de Toulon, CNRS, IRD, Marseille, FranceTuring Center for Living Systems, Aix-Marseille University, Marseille, FranceThe oceanic dissolved organic phosphorus (DOP) pool is mainly composed of P-esters and, to a lesser extent, equally abundant phosphonate and P-anhydride molecules. In phosphate-limited ocean regions, diazotrophs are thought to rely on DOP compounds as an alternative source of phosphorus (P). While both P-esters and phosphonates effectively promote dinitrogen (N2) fixation, the role of P-anhydrides for diazotrophs is unknown. Here we explore the effect of P-anhydrides on N2 fixation at two stations with contrasting biogeochemical conditions: one located in the Tonga trench volcanic arc region (“volcano,” with low phosphate and high iron concentrations), and the other in the South Pacific Gyre (“gyre,” with moderate phosphate and low iron). We incubated surface seawater with AMP (P-ester), ATP (P-ester and P-anhydride), or 3polyP (P-anhydride) and determined cell-specific N2 fixation rates, nifH gene abundance, and transcription in Crocosphaera and Trichodesmium. Trichodesmium did not respond to any DOP compounds added, suggesting that they were not P-limited at the volcano station and were outcompeted by the low iron conditions at the gyre station. Conversely, Crocosphaera were numerous at both stations and their specific N2 fixation rates were stimulated by AMP at the volcano station and slightly by 3polyP at both stations. Heterotrophic bacteria responded to ATP and 3polyP additions similarly at both stations, despite the contrasting phosphate and iron availability. The use of 3polyP by Crocosphaera and heterotrophic bacteria at both low and moderate phosphate concentrations suggests that this compound, in addition to being a source of P, can be used to acquire energy for which both groups compete. P-anhydrides may thus leverage energy restrictions to diazotrophs in the future stratified and nutrient-impoverished ocean.https://www.frontiersin.org/articles/10.3389/fmars.2022.923765/fullnitrogen fixationTrichodesmiumCrocosphaerapolyphosphatephosphoanhydridephosphoester |
| spellingShingle | Alba Filella Alba Filella Lasse Riemann France Van Wambeke Elvira Pulido-Villena Angela Vogts Sophie Bonnet Olivier Grosso Julia M. Diaz Solange Duhamel Mar Benavides Mar Benavides Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs Frontiers in Marine Science nitrogen fixation Trichodesmium Crocosphaera polyphosphate phosphoanhydride phosphoester |
| title | Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs |
| title_full | Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs |
| title_fullStr | Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs |
| title_full_unstemmed | Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs |
| title_short | Contrasting Roles of DOP as a Source of Phosphorus and Energy for Marine Diazotrophs |
| title_sort | contrasting roles of dop as a source of phosphorus and energy for marine diazotrophs |
| topic | nitrogen fixation Trichodesmium Crocosphaera polyphosphate phosphoanhydride phosphoester |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2022.923765/full |
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