Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry
Arbuscular mycorrhizal fungi are obligate symbionts of land plants; furthermore, some of the species harbor endobacteria. Although the molecular approach increased our knowledge of the diversity and origin of the endosymbiosis and its metabolic possibilities, experiments to address the functions of...
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MDPI AG
2021-12-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/9/12/2597 |
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| author | Yukari Kuga Ting-Di Wu Naoya Sakamoto Chie Katsuyama Hisayoshi Yurimoto |
| author_facet | Yukari Kuga Ting-Di Wu Naoya Sakamoto Chie Katsuyama Hisayoshi Yurimoto |
| author_sort | Yukari Kuga |
| collection | DOAJ |
| description | Arbuscular mycorrhizal fungi are obligate symbionts of land plants; furthermore, some of the species harbor endobacteria. Although the molecular approach increased our knowledge of the diversity and origin of the endosymbiosis and its metabolic possibilities, experiments to address the functions of the fungal host have been limited. In this study, a C flow of the fungus to the bacteria was investigated. Onion seedlings colonized with <i>Gigaspora margarita</i>, possessing <i>Candidatus</i> Glomeribacter gigasporarum (<i>Ca</i>Gg, Gram-negative, resides in vacuole) and <i>Candidatus</i> Moeniiplasma glomeromycotorum (<i>Ca</i>Mg, Gram-positive, resides in the cytoplasm,) were labelled with <sup>13</sup>CO<sub>2</sub>. The <sup>13</sup>C localization within the mycorrhiza was analyzed using high-resolution secondary ion mass spectrometry (SIMS). Correlative TEM-SIMS analysis of the fungal cells revealed that the <sup>13</sup>C/<sup>12</sup>C ratio of <i>Ca</i>Gg was the lowest among <i>Ca</i>Mg and mitochondria and was the highest in the cytoplasm. By contrast, the plant cells, mitochondria, plastids, and fungal cytoplasm, which are contributors to the host, showed significantly higher <sup>13</sup>C enrichment than the host cytoplasm. The C allocation patterns implied that <i>Ca</i>Mg has a greater impact than <i>Ca</i>Gg on <i>G. margarita</i>, but both seemed to be less burdensome to the host fungus in terms of C cost. |
| first_indexed | 2024-03-10T03:31:41Z |
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| language | English |
| last_indexed | 2024-03-10T03:31:41Z |
| publishDate | 2021-12-01 |
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| spelling | doaj.art-ca93eb5b921145628b37196bffee40cd2023-11-23T09:40:25ZengMDPI AGMicroorganisms2076-26072021-12-01912259710.3390/microorganisms9122597Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass SpectrometryYukari Kuga0Ting-Di Wu1Naoya Sakamoto2Chie Katsuyama3Hisayoshi Yurimoto4Graduate School of Integrated Sciences for Life, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521, Hiroshima, JapanInstitut Curie, Université PSL, CNRS UMS2016, Inserm US43, Université Paris-Saclay, Multimodal Imaging Center, 91400 Orsay, FranceIsotope Imaging Laboratory, Creative Research Institution, Hokkaido University, Kita-21 Nishi-11, Kita-ku, Sapporo 001-0021, Hokkaido, JapanGraduate School of Integrated Sciences for Life, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521, Hiroshima, JapanDepartment of Natural History Sciences, Hokkaido University, Kita-21 Nishi-11, Kita-ku, Sapporo 001-0021, Hokkaido, JapanArbuscular mycorrhizal fungi are obligate symbionts of land plants; furthermore, some of the species harbor endobacteria. Although the molecular approach increased our knowledge of the diversity and origin of the endosymbiosis and its metabolic possibilities, experiments to address the functions of the fungal host have been limited. In this study, a C flow of the fungus to the bacteria was investigated. Onion seedlings colonized with <i>Gigaspora margarita</i>, possessing <i>Candidatus</i> Glomeribacter gigasporarum (<i>Ca</i>Gg, Gram-negative, resides in vacuole) and <i>Candidatus</i> Moeniiplasma glomeromycotorum (<i>Ca</i>Mg, Gram-positive, resides in the cytoplasm,) were labelled with <sup>13</sup>CO<sub>2</sub>. The <sup>13</sup>C localization within the mycorrhiza was analyzed using high-resolution secondary ion mass spectrometry (SIMS). Correlative TEM-SIMS analysis of the fungal cells revealed that the <sup>13</sup>C/<sup>12</sup>C ratio of <i>Ca</i>Gg was the lowest among <i>Ca</i>Mg and mitochondria and was the highest in the cytoplasm. By contrast, the plant cells, mitochondria, plastids, and fungal cytoplasm, which are contributors to the host, showed significantly higher <sup>13</sup>C enrichment than the host cytoplasm. The C allocation patterns implied that <i>Ca</i>Mg has a greater impact than <i>Ca</i>Gg on <i>G. margarita</i>, but both seemed to be less burdensome to the host fungus in terms of C cost.https://www.mdpi.com/2076-2607/9/12/2597arbuscular mycorrhizaendobacteriastable isotope labellingsecondary ion mass spectrometry |
| spellingShingle | Yukari Kuga Ting-Di Wu Naoya Sakamoto Chie Katsuyama Hisayoshi Yurimoto Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry Microorganisms arbuscular mycorrhiza endobacteria stable isotope labelling secondary ion mass spectrometry |
| title | Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry |
| title_full | Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry |
| title_fullStr | Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry |
| title_full_unstemmed | Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry |
| title_short | Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, <i>Gigaspora margarita</i>, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry |
| title_sort | allocation of carbon from an arbuscular mycorrhizal fungus i gigaspora margarita i to its gram negative and positive endobacteria revealed by high resolution secondary ion mass spectrometry |
| topic | arbuscular mycorrhiza endobacteria stable isotope labelling secondary ion mass spectrometry |
| url | https://www.mdpi.com/2076-2607/9/12/2597 |
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