Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics
ABSTRACTNitrogen (N) availability is one of the principal drivers of primary productivity across aquatic ecosystems. However, the microbial communities and emergent metabolisms that govern N cycling in tropical lakes are both distinct from and poorly understood relative to those found in temperate l...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-02-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01059-23 |
| _version_ | 1827346444502171648 |
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| author | J. M. Fadum M. A. Borton R. A. Daly K. C. Wrighton E. K. Hall |
| author_facet | J. M. Fadum M. A. Borton R. A. Daly K. C. Wrighton E. K. Hall |
| author_sort | J. M. Fadum |
| collection | DOAJ |
| description | ABSTRACTNitrogen (N) availability is one of the principal drivers of primary productivity across aquatic ecosystems. However, the microbial communities and emergent metabolisms that govern N cycling in tropical lakes are both distinct from and poorly understood relative to those found in temperate lakes. This latitudinal difference is largely due to the warm (>20°C) temperatures of tropical lake anoxic hypolimnions (deepest portion of a stratified water column), which result in unique anaerobic metabolisms operating without the temperature constraints found in lakes at temperate latitudes. As such, tropical hypolimnions provide a platform for exploring microbial membership and functional diversity. To better understand N metabolism in warm anoxic waters, we combined measurements of geochemistry and water column thermophysical structure with genome-resolved metatranscriptomic analyses of the water column microbiome in Lake Yojoa, Honduras. We sampled above and below the oxycline in June 2021, when the water column was stratified, and again at the same depths and locations in January 2022, when the water column was mixed. We identified 335 different lineages and significantly different microbiome membership between seasons and, when stratified, between depths. Notably, nrfA (indicative of dissimilatory nitrate reduction to ammonium) was upregulated relative to other N metabolism genes in the June hypolimnion. This work highlights the taxonomic and functional diversity of microbial communities in warm and anoxic inland waters, providing insight into the contemporary microbial ecology of tropical ecosystems as well as inland waters at higher latitudes as water columns continue to warm in the face of global change.IMPORTANCEIn aquatic ecosystems where primary productivity is limited by nitrogen (N), whether continuously, seasonally, or in concert with additional nutrient limitations, increased inorganic N availability can reshape ecosystem structure and function, potentially resulting in eutrophication and even harmful algal blooms. Whereas microbial metabolic processes such as mineralization and dissimilatory nitrate reduction to ammonium increase inorganic N availability, denitrification removes bioavailable N from the ecosystem. Therefore, understanding these key microbial mechanisms is critical to the sustainable management and environmental stewardship of inland freshwater resources. This study identifies and characterizes these crucial metabolisms in a warm, seasonally anoxic ecosystem. Results are contextualized by an ecological understanding of the study system derived from a multi-year continuous monitoring effort. This unique data set is the first of its kind in this largely understudied ecosystem (tropical lakes) and also provides insight into microbiome function and associated taxa in warm, anoxic freshwaters. |
| first_indexed | 2024-03-07T23:31:11Z |
| format | Article |
| id | doaj.art-0131d87bb8e840468b3b800101ae321b |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-07T23:31:11Z |
| publishDate | 2024-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-0131d87bb8e840468b3b800101ae321b2024-02-20T14:00:48ZengAmerican Society for MicrobiologymSystems2379-50772024-02-019210.1128/msystems.01059-23Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomicsJ. M. Fadum0M. A. Borton1R. A. Daly2K. C. Wrighton3E. K. Hall4Graduate Degree Program in Ecology, Colorado State University, Fort Collins, Colorado, USADepartment of Soil and Crop Sciences, Colorado State University, Fort Collins, Colorado, USADepartment of Soil and Crop Sciences, Colorado State University, Fort Collins, Colorado, USAGraduate Degree Program in Ecology, Colorado State University, Fort Collins, Colorado, USAGraduate Degree Program in Ecology, Colorado State University, Fort Collins, Colorado, USAABSTRACTNitrogen (N) availability is one of the principal drivers of primary productivity across aquatic ecosystems. However, the microbial communities and emergent metabolisms that govern N cycling in tropical lakes are both distinct from and poorly understood relative to those found in temperate lakes. This latitudinal difference is largely due to the warm (>20°C) temperatures of tropical lake anoxic hypolimnions (deepest portion of a stratified water column), which result in unique anaerobic metabolisms operating without the temperature constraints found in lakes at temperate latitudes. As such, tropical hypolimnions provide a platform for exploring microbial membership and functional diversity. To better understand N metabolism in warm anoxic waters, we combined measurements of geochemistry and water column thermophysical structure with genome-resolved metatranscriptomic analyses of the water column microbiome in Lake Yojoa, Honduras. We sampled above and below the oxycline in June 2021, when the water column was stratified, and again at the same depths and locations in January 2022, when the water column was mixed. We identified 335 different lineages and significantly different microbiome membership between seasons and, when stratified, between depths. Notably, nrfA (indicative of dissimilatory nitrate reduction to ammonium) was upregulated relative to other N metabolism genes in the June hypolimnion. This work highlights the taxonomic and functional diversity of microbial communities in warm and anoxic inland waters, providing insight into the contemporary microbial ecology of tropical ecosystems as well as inland waters at higher latitudes as water columns continue to warm in the face of global change.IMPORTANCEIn aquatic ecosystems where primary productivity is limited by nitrogen (N), whether continuously, seasonally, or in concert with additional nutrient limitations, increased inorganic N availability can reshape ecosystem structure and function, potentially resulting in eutrophication and even harmful algal blooms. Whereas microbial metabolic processes such as mineralization and dissimilatory nitrate reduction to ammonium increase inorganic N availability, denitrification removes bioavailable N from the ecosystem. Therefore, understanding these key microbial mechanisms is critical to the sustainable management and environmental stewardship of inland freshwater resources. This study identifies and characterizes these crucial metabolisms in a warm, seasonally anoxic ecosystem. Results are contextualized by an ecological understanding of the study system derived from a multi-year continuous monitoring effort. This unique data set is the first of its kind in this largely understudied ecosystem (tropical lakes) and also provides insight into microbiome function and associated taxa in warm, anoxic freshwaters.https://journals.asm.org/doi/10.1128/msystems.01059-23microbial ecologybiogeochemistrynitrogen metabolismdenitrificationDNRAlake |
| spellingShingle | J. M. Fadum M. A. Borton R. A. Daly K. C. Wrighton E. K. Hall Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics mSystems microbial ecology biogeochemistry nitrogen metabolism denitrification DNRA lake |
| title | Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics |
| title_full | Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics |
| title_fullStr | Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics |
| title_full_unstemmed | Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics |
| title_short | Dominant nitrogen metabolisms of a warm, seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics |
| title_sort | dominant nitrogen metabolisms of a warm seasonally anoxic freshwater ecosystem revealed using genome resolved metatranscriptomics |
| topic | microbial ecology biogeochemistry nitrogen metabolism denitrification DNRA lake |
| url | https://journals.asm.org/doi/10.1128/msystems.01059-23 |
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