{"title":"Different Elemental Compositions and Potential Functions of Vacuoles in Bolivina spissa (Foraminifera, Rhizaria) Based on Cryo-SEM-EDS Analyses","authors":"Julien Richirt, Satoshi Okada, Yoshiyuki Ishitani, Nicolaas Glock, Katsuyuki Uematsu, Hidetaka Nomaki","doi":"10.1111/jeu.70044","DOIUrl":null,"url":null,"abstract":"<p>Benthic Foraminifera exhibit diverse adaptations to low oxygen (O<sub>2</sub>) environments, including denitrification, a rare trait among eukaryotes. Denitrifying species store intracellular nitrate (NO<sub>3</sub><sup>−</sup>), possibly within vacuoles, and contribute significantly to the global marine nitrogen (N) cycle. Additionally, widespread phosphate (PO<sub>4</sub><sup>3−</sup>) accumulation suggests a role in supporting metabolism under O<sub>2</sub>-depleted conditions. However, the organelles storing NO<sub>3</sub><sup>−</sup> and PO<sub>4</sub><sup>3−</sup> remain unknown, limiting the mechanistic understanding of these alternative metabolic pathways. To investigate the intracellular NO<sub>3</sub><sup>−</sup> and PO<sub>4</sub><sup>3−</sup> localization in the benthic foraminifera <i>Bolivina spissa</i>, experimental incubations under varying O<sub>2</sub> and NO<sub>3</sub><sup>−</sup> conditions followed by cryogenic fixation and scanning electron microscopy-energy dispersive spectroscopy (SEM-EDS) analyses were carried out. Most vacuoles were enriched in N relative to the surrounding cytoplasm, likely representing the intracellular NO<sub>3</sub><sup>−</sup> reservoir. The elemental mapping also confirmed phosphorus (P) enrichment in organelles resembling acidocalcisomes, likely as PO<sub>4</sub><sup>3−</sup>, which may serve as a readily available energy source used over NO<sub>3</sub><sup>−</sup> storage during the transition between aerobic and anaerobic respiration. Additionally, barium-rich vacuoles of unknown function(s) display a unique spatial distribution. This study emphasizes the effectiveness of cryogenic techniques in elucidating metabolic processes in foraminifers and other large and/or testate unicellular organisms, particularly for studying soluble compounds that have rarely been investigated.</p>","PeriodicalId":15672,"journal":{"name":"Journal of Eukaryotic Microbiology","volume":"72 5","pages":""},"PeriodicalIF":2.6000,"publicationDate":"2025-08-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/jeu.70044","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Eukaryotic Microbiology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/jeu.70044","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Benthic Foraminifera exhibit diverse adaptations to low oxygen (O2) environments, including denitrification, a rare trait among eukaryotes. Denitrifying species store intracellular nitrate (NO3−), possibly within vacuoles, and contribute significantly to the global marine nitrogen (N) cycle. Additionally, widespread phosphate (PO43−) accumulation suggests a role in supporting metabolism under O2-depleted conditions. However, the organelles storing NO3− and PO43− remain unknown, limiting the mechanistic understanding of these alternative metabolic pathways. To investigate the intracellular NO3− and PO43− localization in the benthic foraminifera Bolivina spissa, experimental incubations under varying O2 and NO3− conditions followed by cryogenic fixation and scanning electron microscopy-energy dispersive spectroscopy (SEM-EDS) analyses were carried out. Most vacuoles were enriched in N relative to the surrounding cytoplasm, likely representing the intracellular NO3− reservoir. The elemental mapping also confirmed phosphorus (P) enrichment in organelles resembling acidocalcisomes, likely as PO43−, which may serve as a readily available energy source used over NO3− storage during the transition between aerobic and anaerobic respiration. Additionally, barium-rich vacuoles of unknown function(s) display a unique spatial distribution. This study emphasizes the effectiveness of cryogenic techniques in elucidating metabolic processes in foraminifers and other large and/or testate unicellular organisms, particularly for studying soluble compounds that have rarely been investigated.
期刊介绍:
The Journal of Eukaryotic Microbiology publishes original research on protists, including lower algae and fungi. Articles are published covering all aspects of these organisms, including their behavior, biochemistry, cell biology, chemotherapy, development, ecology, evolution, genetics, molecular biology, morphogenetics, parasitology, systematics, and ultrastructure.