Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification

Abstract Seagrasses are important primary producers in oceans worldwide. They live in shallow coastal waters that are experiencing carbon dioxide enrichment and ocean acidification. Posidonia oceanica, an endemic seagrass species that dominates the Mediterranean Sea, achieves high abundances in seaw...

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Main Authors: Catherine A. Pfister, Ulisse Cardini, Alice Mirasole, Luis M. Montilla, Iva Veseli, Jean-Pierre Gattuso, Nuria Teixido
Format: Article
Language:English
Published: Nature Portfolio 2023-11-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-47126-4
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author Catherine A. Pfister
Ulisse Cardini
Alice Mirasole
Luis M. Montilla
Iva Veseli
Jean-Pierre Gattuso
Nuria Teixido
author_facet Catherine A. Pfister
Ulisse Cardini
Alice Mirasole
Luis M. Montilla
Iva Veseli
Jean-Pierre Gattuso
Nuria Teixido
author_sort Catherine A. Pfister
collection DOAJ
description Abstract Seagrasses are important primary producers in oceans worldwide. They live in shallow coastal waters that are experiencing carbon dioxide enrichment and ocean acidification. Posidonia oceanica, an endemic seagrass species that dominates the Mediterranean Sea, achieves high abundances in seawater with relatively low concentrations of dissolved inorganic nitrogen. Here we tested whether microbial metabolisms associated with P. oceanica and surrounding seawater enhance seagrass access to nitrogen. Using stable isotope enrichments of intact seagrass with amino acids, we showed that ammonification by free-living and seagrass-associated microbes produce ammonium that is likely used by seagrass and surrounding particulate organic matter. Metagenomic analysis of the epiphytic biofilm on the blades and rhizomes support the ubiquity of microbial ammonification genes in this system. Further, we leveraged the presence of natural carbon dioxide vents and show that the presence of P. oceanica enhanced the uptake of nitrogen by water column particulate organic matter, increasing carbon fixation by a factor of 8.6–17.4 with the greatest effect at CO2 vent sites. However, microbial ammonification was reduced at lower pH, suggesting that future ocean climate change will compromise this microbial process. Thus, the seagrass holobiont enhances water column productivity, even in the context of ocean acidification.
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spelling doaj.art-bd0f172ff0934be69360bc51c68d71d02023-11-19T13:00:32ZengNature PortfolioScientific Reports2045-23222023-11-0113111210.1038/s41598-023-47126-4Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidificationCatherine A. Pfister0Ulisse Cardini1Alice Mirasole2Luis M. Montilla3Iva Veseli4Jean-Pierre Gattuso5Nuria Teixido6The Department of Ecology and Evolution, The University of ChicagoIntegrative Marine Ecology Department, Stazione Zoologica Anton Dohrn - National Institute of Marine Biology, Ecology and BiotechnologyIntegrative Marine Ecology Department, Stazione Zoologica Anton Dohrn - National Institute of Marine Biology, Ecology and BiotechnologyIntegrative Marine Ecology Department, Stazione Zoologica Anton Dohrn - National Institute of Marine Biology, Ecology and BiotechnologyBiophysical Sciences Program, The University of ChicagoCNRS, Laboratoire d’Océanographie de Villefranche, Sorbonne UniversitéIntegrative Marine Ecology Department, Stazione Zoologica Anton Dohrn - National Institute of Marine Biology, Ecology and BiotechnologyAbstract Seagrasses are important primary producers in oceans worldwide. They live in shallow coastal waters that are experiencing carbon dioxide enrichment and ocean acidification. Posidonia oceanica, an endemic seagrass species that dominates the Mediterranean Sea, achieves high abundances in seawater with relatively low concentrations of dissolved inorganic nitrogen. Here we tested whether microbial metabolisms associated with P. oceanica and surrounding seawater enhance seagrass access to nitrogen. Using stable isotope enrichments of intact seagrass with amino acids, we showed that ammonification by free-living and seagrass-associated microbes produce ammonium that is likely used by seagrass and surrounding particulate organic matter. Metagenomic analysis of the epiphytic biofilm on the blades and rhizomes support the ubiquity of microbial ammonification genes in this system. Further, we leveraged the presence of natural carbon dioxide vents and show that the presence of P. oceanica enhanced the uptake of nitrogen by water column particulate organic matter, increasing carbon fixation by a factor of 8.6–17.4 with the greatest effect at CO2 vent sites. However, microbial ammonification was reduced at lower pH, suggesting that future ocean climate change will compromise this microbial process. Thus, the seagrass holobiont enhances water column productivity, even in the context of ocean acidification.https://doi.org/10.1038/s41598-023-47126-4
spellingShingle Catherine A. Pfister
Ulisse Cardini
Alice Mirasole
Luis M. Montilla
Iva Veseli
Jean-Pierre Gattuso
Nuria Teixido
Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification
Scientific Reports
title Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification
title_full Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification
title_fullStr Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification
title_full_unstemmed Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification
title_short Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification
title_sort microbial associates of an endemic mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification
url https://doi.org/10.1038/s41598-023-47126-4
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