Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment
Abstract Background In hot deserts daily/seasonal fluctuations pose great challenges to the resident organisms. However, these extreme ecosystems host unique microenvironments, such as the rhizosheath–root system of desert speargrasses in which biological activities and interactions are facilitated...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-04-01
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| Series: | Environmental Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40793-022-00407-3 |
| _version_ | 1811272260509499392 |
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| author | Ramona Marasco Marco Fusi Maria Mosqueira Jenny Marie Booth Federico Rossi Massimiliano Cardinale Grégoire Michoud Eleonora Rolli Gianmarco Mugnai Lorenzo Vergani Sara Borin Roberto De Philippis Ameur Cherif Daniele Daffonchio |
| author_facet | Ramona Marasco Marco Fusi Maria Mosqueira Jenny Marie Booth Federico Rossi Massimiliano Cardinale Grégoire Michoud Eleonora Rolli Gianmarco Mugnai Lorenzo Vergani Sara Borin Roberto De Philippis Ameur Cherif Daniele Daffonchio |
| author_sort | Ramona Marasco |
| collection | DOAJ |
| description | Abstract Background In hot deserts daily/seasonal fluctuations pose great challenges to the resident organisms. However, these extreme ecosystems host unique microenvironments, such as the rhizosheath–root system of desert speargrasses in which biological activities and interactions are facilitated by milder conditions and reduced fluctuations. Here, we examined the bacterial microbiota associated with this structure and its surrounding sand in the desert speargrass Stipagrostis pungens under the contrasting environmental conditions of summer and winter in the Sahara Desert. Results The belowground rhizosheath–root system has higher nutrient and humidity contents, and cooler temperatures than the surrounding sand. The plant responds to the harsh environmental conditions of the summer by increasing the abundance and diversity of extracellular polymeric substances (EPS) compared to the winter. On the contrary, the bacterial community associated with the rhizosheath–root system and its interactome remain stable and, unlike the bulk sand, are unaffected by the seasonal environmental variations. The rhizosheath–root system bacterial communities are consistently dominated by Actinobacteria and Alphaproteobacteria and form distinct bacteria communities from those of bulk sand in the two seasons. The microbiome-stabilization mediated by the plant host acts to consistently retain beneficial bacteria with multiple plant growth promoting functions, including those capable to produce EPS, which increase the sand water holding capacity ameliorating the rhizosheath micro-environment. Conclusions Our results reveal the capability of plants in desert ecosystems to stabilize their below ground microbial community under seasonal contrasting environmental conditions, minimizing the heterogeneity of the surrounding bulk sand and contributing to the overall holobiont resilience under poly-extreme conditions. |
| first_indexed | 2024-04-12T22:37:10Z |
| format | Article |
| id | doaj.art-4a5c30950a744d629aa077010845b840 |
| institution | Directory Open Access Journal |
| issn | 2524-6372 |
| language | English |
| last_indexed | 2024-04-12T22:37:10Z |
| publishDate | 2022-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Environmental Microbiome |
| spelling | doaj.art-4a5c30950a744d629aa077010845b8402022-12-22T03:13:50ZengBMCEnvironmental Microbiome2524-63722022-04-0117111910.1186/s40793-022-00407-3Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environmentRamona Marasco0Marco Fusi1Maria Mosqueira2Jenny Marie Booth3Federico Rossi4Massimiliano Cardinale5Grégoire Michoud6Eleonora Rolli7Gianmarco Mugnai8Lorenzo Vergani9Sara Borin10Roberto De Philippis11Ameur Cherif12Daniele Daffonchio13Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST)Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST)Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST)Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST)Department of Agriculture, Food, Environment and Forestry (DAGRI), University of FlorenceDepartment of Biological and Environmental Sciences and Technologies, University of SalentoBiological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST)Department of Food, Environmental and Nutritional Sciences (DeFENS), University of MilanoInstitute of BioEconomy, CNRDepartment of Food, Environmental and Nutritional Sciences (DeFENS), University of MilanoDepartment of Food, Environmental and Nutritional Sciences (DeFENS), University of MilanoDepartment of Agriculture, Food, Environment and Forestry (DAGRI), University of FlorenceInstitut Supérieur de Biotechnologie Sidi Thabet (ISBST), BVBGR-LR11ES31, Biotechpole Sidi Thabet, University ManoubaBiological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST)Abstract Background In hot deserts daily/seasonal fluctuations pose great challenges to the resident organisms. However, these extreme ecosystems host unique microenvironments, such as the rhizosheath–root system of desert speargrasses in which biological activities and interactions are facilitated by milder conditions and reduced fluctuations. Here, we examined the bacterial microbiota associated with this structure and its surrounding sand in the desert speargrass Stipagrostis pungens under the contrasting environmental conditions of summer and winter in the Sahara Desert. Results The belowground rhizosheath–root system has higher nutrient and humidity contents, and cooler temperatures than the surrounding sand. The plant responds to the harsh environmental conditions of the summer by increasing the abundance and diversity of extracellular polymeric substances (EPS) compared to the winter. On the contrary, the bacterial community associated with the rhizosheath–root system and its interactome remain stable and, unlike the bulk sand, are unaffected by the seasonal environmental variations. The rhizosheath–root system bacterial communities are consistently dominated by Actinobacteria and Alphaproteobacteria and form distinct bacteria communities from those of bulk sand in the two seasons. The microbiome-stabilization mediated by the plant host acts to consistently retain beneficial bacteria with multiple plant growth promoting functions, including those capable to produce EPS, which increase the sand water holding capacity ameliorating the rhizosheath micro-environment. Conclusions Our results reveal the capability of plants in desert ecosystems to stabilize their below ground microbial community under seasonal contrasting environmental conditions, minimizing the heterogeneity of the surrounding bulk sand and contributing to the overall holobiont resilience under poly-extreme conditions.https://doi.org/10.1186/s40793-022-00407-3RhizosheathPlant-microbiomeDesertExtracellular polymeric substances (EPS)Plant legacyEnvironmental fluctuation |
| spellingShingle | Ramona Marasco Marco Fusi Maria Mosqueira Jenny Marie Booth Federico Rossi Massimiliano Cardinale Grégoire Michoud Eleonora Rolli Gianmarco Mugnai Lorenzo Vergani Sara Borin Roberto De Philippis Ameur Cherif Daniele Daffonchio Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment Environmental Microbiome Rhizosheath Plant-microbiome Desert Extracellular polymeric substances (EPS) Plant legacy Environmental fluctuation |
| title | Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment |
| title_full | Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment |
| title_fullStr | Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment |
| title_full_unstemmed | Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment |
| title_short | Rhizosheath–root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment |
| title_sort | rhizosheath root system changes exopolysaccharide content but stabilizes bacterial community across contrasting seasons in a desert environment |
| topic | Rhizosheath Plant-microbiome Desert Extracellular polymeric substances (EPS) Plant legacy Environmental fluctuation |
| url | https://doi.org/10.1186/s40793-022-00407-3 |
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