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Crocosphaera as a Major Consumer of Fixed Nitrogen

Crocosphaera watsonii (hereafter referred to as Crocosphaera) is a key nitrogen (N) fixer in the ocean, but its ability to consume combined-N sources is still unclear. Using in situ microcosm incubations with an ecological model, we show that Crocosphaera has high competitive capability both under l...

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Autores principales: Masuda, Takako, Inomura, Keisuke, Kodama, Taketoshi, Shiozaki, Takuhei, Kitajima, Satoshi, Armin, Gabrielle, Matsui, Takato, Suzuki, Koji, Takeda, Shigenobu, Sato, Mitsuhide, Prášil, Ondřej, Furuya, Ken
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9431459/
https://www.ncbi.nlm.nih.gov/pubmed/35770981
http://dx.doi.org/10.1128/spectrum.02177-21
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author Masuda, Takako
Inomura, Keisuke
Kodama, Taketoshi
Shiozaki, Takuhei
Kitajima, Satoshi
Armin, Gabrielle
Matsui, Takato
Suzuki, Koji
Takeda, Shigenobu
Sato, Mitsuhide
Prášil, Ondřej
Furuya, Ken
author_facet Masuda, Takako
Inomura, Keisuke
Kodama, Taketoshi
Shiozaki, Takuhei
Kitajima, Satoshi
Armin, Gabrielle
Matsui, Takato
Suzuki, Koji
Takeda, Shigenobu
Sato, Mitsuhide
Prášil, Ondřej
Furuya, Ken
author_sort Masuda, Takako
collection PubMed
description Crocosphaera watsonii (hereafter referred to as Crocosphaera) is a key nitrogen (N) fixer in the ocean, but its ability to consume combined-N sources is still unclear. Using in situ microcosm incubations with an ecological model, we show that Crocosphaera has high competitive capability both under low and moderately high combined-N concentrations. In field incubations, Crocosphaera accounted for the highest consumption of ammonium and nitrate, followed by picoeukaryotes. The model analysis shows that cells have a high ammonium uptake rate (~7 mol N [mol N](−1) d(−1) at the maximum), which allows them to compete against picoeukaryotes and nondiazotrophic cyanobacteria when combined N is sufficiently available. Even when combined N is depleted, their capability of nitrogen fixation allows higher growth rates compared to potential competitors. These results suggest the high fitness of Crocosphaera in combined-N limiting, oligotrophic oceans heightening its potential significance in its ecosystem and in biogeochemical cycling. IMPORTANCE Crocosphaera watsonii is as a key nitrogen (N) supplier in marine ecosystems, and it has been estimated to contribute up to half of oceanic N(2) fixation. Conversely, a recent study reported that Crocosphaera can assimilate combined N and proposed that unicellular diazotrophs can be competitors with non-N(2) fixing phytoplankton for combined N. Despite its importance in nitrogen cycling, the methods by which Crocosphaera compete are not currently fully understood. Here, we present a new role of Crocosphaera as a combined-N consumer: a competitor against nondiazotrophic phytoplankton for combined N. In this study, we combined in situ microcosm experiments and an ecosystem model to quantitatively evaluate the combined-N consumption by Crocosphaera and other non-N(2) fixing phytoplankton. Our results suggest the high fitness of Crocosphaera in combined-N limiting, oligotrophic oceans and, thus, heightens its potential significance in its ecosystem and in biogeochemical cycling.
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spelling pubmed-94314592022-09-01 Crocosphaera as a Major Consumer of Fixed Nitrogen Masuda, Takako Inomura, Keisuke Kodama, Taketoshi Shiozaki, Takuhei Kitajima, Satoshi Armin, Gabrielle Matsui, Takato Suzuki, Koji Takeda, Shigenobu Sato, Mitsuhide Prášil, Ondřej Furuya, Ken Microbiol Spectr Research Article Crocosphaera watsonii (hereafter referred to as Crocosphaera) is a key nitrogen (N) fixer in the ocean, but its ability to consume combined-N sources is still unclear. Using in situ microcosm incubations with an ecological model, we show that Crocosphaera has high competitive capability both under low and moderately high combined-N concentrations. In field incubations, Crocosphaera accounted for the highest consumption of ammonium and nitrate, followed by picoeukaryotes. The model analysis shows that cells have a high ammonium uptake rate (~7 mol N [mol N](−1) d(−1) at the maximum), which allows them to compete against picoeukaryotes and nondiazotrophic cyanobacteria when combined N is sufficiently available. Even when combined N is depleted, their capability of nitrogen fixation allows higher growth rates compared to potential competitors. These results suggest the high fitness of Crocosphaera in combined-N limiting, oligotrophic oceans heightening its potential significance in its ecosystem and in biogeochemical cycling. IMPORTANCE Crocosphaera watsonii is as a key nitrogen (N) supplier in marine ecosystems, and it has been estimated to contribute up to half of oceanic N(2) fixation. Conversely, a recent study reported that Crocosphaera can assimilate combined N and proposed that unicellular diazotrophs can be competitors with non-N(2) fixing phytoplankton for combined N. Despite its importance in nitrogen cycling, the methods by which Crocosphaera compete are not currently fully understood. Here, we present a new role of Crocosphaera as a combined-N consumer: a competitor against nondiazotrophic phytoplankton for combined N. In this study, we combined in situ microcosm experiments and an ecosystem model to quantitatively evaluate the combined-N consumption by Crocosphaera and other non-N(2) fixing phytoplankton. Our results suggest the high fitness of Crocosphaera in combined-N limiting, oligotrophic oceans and, thus, heightens its potential significance in its ecosystem and in biogeochemical cycling. American Society for Microbiology 2022-06-30 /pmc/articles/PMC9431459/ /pubmed/35770981 http://dx.doi.org/10.1128/spectrum.02177-21 Text en Copyright © 2022 Masuda et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Masuda, Takako
Inomura, Keisuke
Kodama, Taketoshi
Shiozaki, Takuhei
Kitajima, Satoshi
Armin, Gabrielle
Matsui, Takato
Suzuki, Koji
Takeda, Shigenobu
Sato, Mitsuhide
Prášil, Ondřej
Furuya, Ken
Crocosphaera as a Major Consumer of Fixed Nitrogen
title Crocosphaera as a Major Consumer of Fixed Nitrogen
title_full Crocosphaera as a Major Consumer of Fixed Nitrogen
title_fullStr Crocosphaera as a Major Consumer of Fixed Nitrogen
title_full_unstemmed Crocosphaera as a Major Consumer of Fixed Nitrogen
title_short Crocosphaera as a Major Consumer of Fixed Nitrogen
title_sort crocosphaera as a major consumer of fixed nitrogen
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9431459/
https://www.ncbi.nlm.nih.gov/pubmed/35770981
http://dx.doi.org/10.1128/spectrum.02177-21
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