Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development
ABSTRACT Interactions between plant roots and rhizosphere bacteria modulate nitrogen (N)-cycling processes and create habitats rich in low molecular weight compounds (exudates) and complex organic molecules (decaying root litter) compared to those of bulk soil. Microbial N-cycling is regulated by ed...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-10-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00315-23 |
| _version_ | 1797617648896311296 |
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| author | Ella T. Sieradzki Erin E. Nuccio Jennifer Pett-Ridge Mary K. Firestone |
| author_facet | Ella T. Sieradzki Erin E. Nuccio Jennifer Pett-Ridge Mary K. Firestone |
| author_sort | Ella T. Sieradzki |
| collection | DOAJ |
| description | ABSTRACT Interactions between plant roots and rhizosphere bacteria modulate nitrogen (N)-cycling processes and create habitats rich in low molecular weight compounds (exudates) and complex organic molecules (decaying root litter) compared to those of bulk soil. Microbial N-cycling is regulated by edaphic conditions and genes from many interconnected metabolic pathways, but most studies of soil N-cycling gene expression have focused on single pathways. Currently, we lack a comprehensive understanding of the interplay between soil N-cycling gene regulation, spatial habitat, and time. We present results from a replicated time series of soil metatranscriptomes; we followed gene expression of multiple N transformations in four soil habitats (rhizosphere, detritusphere, rhizo-detritusphere, and bulk soil) during active root growth for the annual grass, Avena fatua. The presence of root litter and living roots significantly altered the trajectories of N-cycling gene expression. Upregulation of assimilatory nitrate reduction in the rhizosphere suggests that rhizosphere bacteria were actively competing with roots for nitrate. Simultaneously, ammonium assimilatory pathways were upregulated in both rhizosphere and detritusphere soil, which could have limited N availability to plants. The detritusphere supported dissimilatory processes DNRA and denitrification. Expression of nitrification genes was dominated by three phylotypes of Thaumarchaeota and was upregulated in bulk soil. Unidirectional ammonium assimilation and its regulatory genes (GS/GOGAT) were upregulated near relatively young roots and highly decayed root litter, suggesting N may have been limiting in these habitats (GS/GOGAT is typically activated under N limitation). Our comprehensive analysis indicates that differences in carbon and inorganic N availability control contemporaneous transcription of N-cycling pathways in soil habitats. IMPORTANCE Plant roots modulate microbial nitrogen (N) cycling by regulating the supply of root-derived carbon and nitrogen uptake. These differences in resource availability cause distinct micro-habitats to develop: soil near living roots, decaying roots, near both, or outside the direct influence of roots. While many environmental factors and genes control the microbial processes involved in the nitrogen cycle, most research has focused on single genes and pathways, neglecting the interactive effects these pathways have on each other. The processes controlled by these pathways determine consumption and production of N by soil microorganisms. We followed the expression of N-cycling genes in four soil microhabitats over a period of active root growth for an annual grass. We found that the presence of root litter and living roots significantly altered gene expression involved in multiple nitrogen pathways, as well as tradeoffs between pathways, which ultimately regulate N availability to plants. |
| first_indexed | 2024-03-11T07:58:50Z |
| format | Article |
| id | doaj.art-7acff0c287e44e3daacc6c6eb5c23c13 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-11T07:58:50Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-7acff0c287e44e3daacc6c6eb5c23c132023-11-17T03:22:37ZengAmerican Society for MicrobiologymSystems2379-50772023-10-018510.1128/msystems.00315-23Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant developmentElla T. Sieradzki0Erin E. Nuccio1Jennifer Pett-Ridge2Mary K. Firestone3Department of Environmental Science, Policy and Management, University of California Berkeley , Berkeley, California, USAPhysical and Life Sciences Directorate, Lawrence Livermore National Laboratory , Livermore, California, USAPhysical and Life Sciences Directorate, Lawrence Livermore National Laboratory , Livermore, California, USADepartment of Environmental Science, Policy and Management, University of California Berkeley , Berkeley, California, USAABSTRACT Interactions between plant roots and rhizosphere bacteria modulate nitrogen (N)-cycling processes and create habitats rich in low molecular weight compounds (exudates) and complex organic molecules (decaying root litter) compared to those of bulk soil. Microbial N-cycling is regulated by edaphic conditions and genes from many interconnected metabolic pathways, but most studies of soil N-cycling gene expression have focused on single pathways. Currently, we lack a comprehensive understanding of the interplay between soil N-cycling gene regulation, spatial habitat, and time. We present results from a replicated time series of soil metatranscriptomes; we followed gene expression of multiple N transformations in four soil habitats (rhizosphere, detritusphere, rhizo-detritusphere, and bulk soil) during active root growth for the annual grass, Avena fatua. The presence of root litter and living roots significantly altered the trajectories of N-cycling gene expression. Upregulation of assimilatory nitrate reduction in the rhizosphere suggests that rhizosphere bacteria were actively competing with roots for nitrate. Simultaneously, ammonium assimilatory pathways were upregulated in both rhizosphere and detritusphere soil, which could have limited N availability to plants. The detritusphere supported dissimilatory processes DNRA and denitrification. Expression of nitrification genes was dominated by three phylotypes of Thaumarchaeota and was upregulated in bulk soil. Unidirectional ammonium assimilation and its regulatory genes (GS/GOGAT) were upregulated near relatively young roots and highly decayed root litter, suggesting N may have been limiting in these habitats (GS/GOGAT is typically activated under N limitation). Our comprehensive analysis indicates that differences in carbon and inorganic N availability control contemporaneous transcription of N-cycling pathways in soil habitats. IMPORTANCE Plant roots modulate microbial nitrogen (N) cycling by regulating the supply of root-derived carbon and nitrogen uptake. These differences in resource availability cause distinct micro-habitats to develop: soil near living roots, decaying roots, near both, or outside the direct influence of roots. While many environmental factors and genes control the microbial processes involved in the nitrogen cycle, most research has focused on single genes and pathways, neglecting the interactive effects these pathways have on each other. The processes controlled by these pathways determine consumption and production of N by soil microorganisms. We followed the expression of N-cycling genes in four soil microhabitats over a period of active root growth for an annual grass. We found that the presence of root litter and living roots significantly altered gene expression involved in multiple nitrogen pathways, as well as tradeoffs between pathways, which ultimately regulate N availability to plants.https://journals.asm.org/doi/10.1128/msystems.00315-23soil microbiomesoil nitrogenrhizospheregene expressionmetatranscriptomicsnitrification |
| spellingShingle | Ella T. Sieradzki Erin E. Nuccio Jennifer Pett-Ridge Mary K. Firestone Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development mSystems soil microbiome soil nitrogen rhizosphere gene expression metatranscriptomics nitrification |
| title | Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development |
| title_full | Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development |
| title_fullStr | Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development |
| title_full_unstemmed | Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development |
| title_short | Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development |
| title_sort | rhizosphere and detritusphere habitats modulate expression of soil n cycling genes during plant development |
| topic | soil microbiome soil nitrogen rhizosphere gene expression metatranscriptomics nitrification |
| url | https://journals.asm.org/doi/10.1128/msystems.00315-23 |
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