Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth
Abstract Background Despite the knowledge that the soil–plant–microbiome nexus is shaped by interactions amongst its members, very little is known about how individual symbioses regulate this shaping. Even less is known about how the agriculturally important symbiosis of nitrogen-fixing rhizobia wit...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-07-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01592-0 |
| _version_ | 1797784508653633536 |
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| author | Beatriz Lagunas Luke Richards Chrysi Sergaki Jamie Burgess Alonso Javier Pardal Rana M. F. Hussain Bethany L. Richmond Laura Baxter Proyash Roy Anastasia Pakidi Gina Stovold Saúl Vázquez Sascha Ott Patrick Schäfer Miriam L. Gifford |
| author_facet | Beatriz Lagunas Luke Richards Chrysi Sergaki Jamie Burgess Alonso Javier Pardal Rana M. F. Hussain Bethany L. Richmond Laura Baxter Proyash Roy Anastasia Pakidi Gina Stovold Saúl Vázquez Sascha Ott Patrick Schäfer Miriam L. Gifford |
| author_sort | Beatriz Lagunas |
| collection | DOAJ |
| description | Abstract Background Despite the knowledge that the soil–plant–microbiome nexus is shaped by interactions amongst its members, very little is known about how individual symbioses regulate this shaping. Even less is known about how the agriculturally important symbiosis of nitrogen-fixing rhizobia with legumes is impacted according to soil type, yet this knowledge is crucial if we are to harness or improve it. We asked how the plant, soil and microbiome are modulated by symbiosis between the model legume Medicago truncatula and different strains of Sinorhizobium meliloti or Sinorhizobium medicae whose nitrogen-fixing efficiency varies, in three distinct soil types that differ in nutrient fertility, to examine the role of the soil environment upon the plant–microbe interaction during nodulation. Results The outcome of symbiosis results in installment of a potentially beneficial microbiome that leads to increased nutrient uptake that is not simply proportional to soil nutrient abundance. A number of soil edaphic factors including Zn and Mo, and not just the classical N/P/K nutrients, group with microbial community changes, and alterations in the microbiome can be seen across different soil fertility types. Root endosphere emerged as the plant microhabitat more affected by this rhizobial efficiency-driven community reshaping, manifested by the accumulation of members of the phylum Actinobacteria. The plant in turn plays an active role in regulating its root community, including sanctioning low nitrogen efficiency rhizobial strains, leading to nodule senescence in particular plant–soil–rhizobia strain combinations. Conclusions The microbiome–soil–rhizobial dynamic strongly influences plant nutrient uptake and growth, with the endosphere and rhizosphere shaped differentially according to plant–rhizobial interactions with strains that vary in nitrogen-fixing efficiency levels. These results open up the possibility to select inoculation partners best suited for plant, soil type and microbial community. Video Abstract |
| first_indexed | 2024-03-13T00:40:55Z |
| format | Article |
| id | doaj.art-b2b47b981e384843a6c090786c7a6730 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-13T00:40:55Z |
| publishDate | 2023-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-b2b47b981e384843a6c090786c7a67302023-07-09T11:19:33ZengBMCMicrobiome2049-26182023-07-0111112210.1186/s40168-023-01592-0Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growthBeatriz Lagunas0Luke Richards1Chrysi Sergaki2Jamie Burgess3Alonso Javier Pardal4Rana M. F. Hussain5Bethany L. Richmond6Laura Baxter7Proyash Roy8Anastasia Pakidi9Gina Stovold10Saúl Vázquez11Sascha Ott12Patrick Schäfer13Miriam L. Gifford14School of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickWarwick Medical School, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickUniversity of NottinghamWarwick Medical School, University of WarwickSchool of Life Sciences, University of WarwickSchool of Life Sciences, University of WarwickAbstract Background Despite the knowledge that the soil–plant–microbiome nexus is shaped by interactions amongst its members, very little is known about how individual symbioses regulate this shaping. Even less is known about how the agriculturally important symbiosis of nitrogen-fixing rhizobia with legumes is impacted according to soil type, yet this knowledge is crucial if we are to harness or improve it. We asked how the plant, soil and microbiome are modulated by symbiosis between the model legume Medicago truncatula and different strains of Sinorhizobium meliloti or Sinorhizobium medicae whose nitrogen-fixing efficiency varies, in three distinct soil types that differ in nutrient fertility, to examine the role of the soil environment upon the plant–microbe interaction during nodulation. Results The outcome of symbiosis results in installment of a potentially beneficial microbiome that leads to increased nutrient uptake that is not simply proportional to soil nutrient abundance. A number of soil edaphic factors including Zn and Mo, and not just the classical N/P/K nutrients, group with microbial community changes, and alterations in the microbiome can be seen across different soil fertility types. Root endosphere emerged as the plant microhabitat more affected by this rhizobial efficiency-driven community reshaping, manifested by the accumulation of members of the phylum Actinobacteria. The plant in turn plays an active role in regulating its root community, including sanctioning low nitrogen efficiency rhizobial strains, leading to nodule senescence in particular plant–soil–rhizobia strain combinations. Conclusions The microbiome–soil–rhizobial dynamic strongly influences plant nutrient uptake and growth, with the endosphere and rhizosphere shaped differentially according to plant–rhizobial interactions with strains that vary in nitrogen-fixing efficiency levels. These results open up the possibility to select inoculation partners best suited for plant, soil type and microbial community. Video Abstracthttps://doi.org/10.1186/s40168-023-01592-0Medicago truncatulaNodulationPlant–rhizobial interactionNitrogen fixation efficiencySoilEndosphere |
| spellingShingle | Beatriz Lagunas Luke Richards Chrysi Sergaki Jamie Burgess Alonso Javier Pardal Rana M. F. Hussain Bethany L. Richmond Laura Baxter Proyash Roy Anastasia Pakidi Gina Stovold Saúl Vázquez Sascha Ott Patrick Schäfer Miriam L. Gifford Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth Microbiome Medicago truncatula Nodulation Plant–rhizobial interaction Nitrogen fixation efficiency Soil Endosphere |
| title | Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth |
| title_full | Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth |
| title_fullStr | Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth |
| title_full_unstemmed | Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth |
| title_short | Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth |
| title_sort | rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and medicago truncatula host growth |
| topic | Medicago truncatula Nodulation Plant–rhizobial interaction Nitrogen fixation efficiency Soil Endosphere |
| url | https://doi.org/10.1186/s40168-023-01592-0 |
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