The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After Winter
Soil microbial biomass can reach its annual maximum pool size beneath the winter snowpack and is known to decline abruptly following snowmelt in seasonally snow-covered ecosystems. Observed differences in winter versus summer microbial taxonomic composition also suggests that phylogenetically conser...
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Frontiers Media S.A.
2020-05-01
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Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.00871/full |
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author | Patrick O. Sorensen Harry R. Beller Markus Bill Nicholas J. Bouskill Susan S. Hubbard Ulas Karaoz Alexander Polussa Alexander Polussa Heidi Steltzer Heidi Steltzer Shi Wang Kenneth H. Williams Kenneth H. Williams Yuxin Wu Eoin L. Brodie Eoin L. Brodie |
author_facet | Patrick O. Sorensen Harry R. Beller Markus Bill Nicholas J. Bouskill Susan S. Hubbard Ulas Karaoz Alexander Polussa Alexander Polussa Heidi Steltzer Heidi Steltzer Shi Wang Kenneth H. Williams Kenneth H. Williams Yuxin Wu Eoin L. Brodie Eoin L. Brodie |
author_sort | Patrick O. Sorensen |
collection | DOAJ |
description | Soil microbial biomass can reach its annual maximum pool size beneath the winter snowpack and is known to decline abruptly following snowmelt in seasonally snow-covered ecosystems. Observed differences in winter versus summer microbial taxonomic composition also suggests that phylogenetically conserved traits may permit winter- versus summer-adapted microorganisms to occupy distinct niches. In this study, we sought to identify archaea, bacteria, and fungi that are associated with the soil microbial bloom overwinter and the subsequent biomass collapse following snowmelt at a high-altitude watershed in central Colorado, United States. Archaea, bacteria, and fungi were categorized into three life strategies (Winter-Adapted, Snowmelt-Specialist, Spring-Adapted) based upon changes in abundance during winter, the snowmelt period, and after snowmelt in spring. We calculated indices of phylogenetic relatedness (archaea and bacteria) or assigned functional attributes (fungi) to organisms within life strategies to infer whether phylogenetically conserved traits differentiate Winter-Adapted, Snowmelt-Specialist, and Spring-Adapted groups. We observed that the soil microbial bloom was correlated in time with a pulse of snowmelt infiltration, which commenced 65 days prior to soils becoming snow-free. A pulse of nitrogen (N, as nitrate) occurred after snowmelt, along with a collapse in the microbial biomass pool size, and an increased abundance of nitrifying archaea and bacteria (e.g., Thaumarchaeota, Nitrospirae). Winter- and Spring-Adapted archaea and bacteria were phylogenetically clustered, suggesting that phylogenetically conserved traits allow Winter- and Spring-Adapted archaea and bacteria to occupy distinct niches. In contrast, Snowmelt-Specialist archaea and bacteria were phylogenetically overdispersed, suggesting that the key mechanism(s) of the microbial biomass crash are likely to be density-dependent (e.g., trophic interactions, competitive exclusion) and affect organisms across a broad phylogenetic spectrum. Saprotrophic fungi were the dominant functional group across fungal life strategies, however, ectomycorrhizal fungi experienced a large increase in abundance in spring. If well-coupled plant-mycorrhizal phenology currently buffers ecosystem N losses in spring, then changes in snowmelt timing may alter ecosystem N retention potential. Overall, we observed that snowmelt separates three distinct soil niches that are occupied by ecologically distinct groups of microorganisms. This ecological differentiation is of biogeochemical importance, particularly with respect to the mobilization of nitrogen during winter, before and after snowmelt. |
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spelling | doaj.art-82d02f7a6d044b9290529b777b4b928d2022-12-21T23:46:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-05-011110.3389/fmicb.2020.00871510829The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After WinterPatrick O. Sorensen0Harry R. Beller1Markus Bill2Nicholas J. Bouskill3Susan S. Hubbard4Ulas Karaoz5Alexander Polussa6Alexander Polussa7Heidi Steltzer8Heidi Steltzer9Shi Wang10Kenneth H. Williams11Kenneth H. Williams12Yuxin Wu13Eoin L. Brodie14Eoin L. Brodie15Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesSchool of Forestry and Environmental Studies, Yale University, New Haven, CT, United StatesFort Lewis College, Durango, CO, United StatesRocky Mountain Biological Laboratory, Gothic, CO, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesRocky Mountain Biological Laboratory, Gothic, CO, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesDepartment of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA, United StatesSoil microbial biomass can reach its annual maximum pool size beneath the winter snowpack and is known to decline abruptly following snowmelt in seasonally snow-covered ecosystems. Observed differences in winter versus summer microbial taxonomic composition also suggests that phylogenetically conserved traits may permit winter- versus summer-adapted microorganisms to occupy distinct niches. In this study, we sought to identify archaea, bacteria, and fungi that are associated with the soil microbial bloom overwinter and the subsequent biomass collapse following snowmelt at a high-altitude watershed in central Colorado, United States. Archaea, bacteria, and fungi were categorized into three life strategies (Winter-Adapted, Snowmelt-Specialist, Spring-Adapted) based upon changes in abundance during winter, the snowmelt period, and after snowmelt in spring. We calculated indices of phylogenetic relatedness (archaea and bacteria) or assigned functional attributes (fungi) to organisms within life strategies to infer whether phylogenetically conserved traits differentiate Winter-Adapted, Snowmelt-Specialist, and Spring-Adapted groups. We observed that the soil microbial bloom was correlated in time with a pulse of snowmelt infiltration, which commenced 65 days prior to soils becoming snow-free. A pulse of nitrogen (N, as nitrate) occurred after snowmelt, along with a collapse in the microbial biomass pool size, and an increased abundance of nitrifying archaea and bacteria (e.g., Thaumarchaeota, Nitrospirae). Winter- and Spring-Adapted archaea and bacteria were phylogenetically clustered, suggesting that phylogenetically conserved traits allow Winter- and Spring-Adapted archaea and bacteria to occupy distinct niches. In contrast, Snowmelt-Specialist archaea and bacteria were phylogenetically overdispersed, suggesting that the key mechanism(s) of the microbial biomass crash are likely to be density-dependent (e.g., trophic interactions, competitive exclusion) and affect organisms across a broad phylogenetic spectrum. Saprotrophic fungi were the dominant functional group across fungal life strategies, however, ectomycorrhizal fungi experienced a large increase in abundance in spring. If well-coupled plant-mycorrhizal phenology currently buffers ecosystem N losses in spring, then changes in snowmelt timing may alter ecosystem N retention potential. Overall, we observed that snowmelt separates three distinct soil niches that are occupied by ecologically distinct groups of microorganisms. This ecological differentiation is of biogeochemical importance, particularly with respect to the mobilization of nitrogen during winter, before and after snowmelt.https://www.frontiersin.org/article/10.3389/fmicb.2020.00871/fullsnowmeltwatershedlife history strategysoil nitrogensoil archaea and bacteriasoil fungi |
spellingShingle | Patrick O. Sorensen Harry R. Beller Markus Bill Nicholas J. Bouskill Susan S. Hubbard Ulas Karaoz Alexander Polussa Alexander Polussa Heidi Steltzer Heidi Steltzer Shi Wang Kenneth H. Williams Kenneth H. Williams Yuxin Wu Eoin L. Brodie Eoin L. Brodie The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After Winter Frontiers in Microbiology snowmelt watershed life history strategy soil nitrogen soil archaea and bacteria soil fungi |
title | The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After Winter |
title_full | The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After Winter |
title_fullStr | The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After Winter |
title_full_unstemmed | The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After Winter |
title_short | The Snowmelt Niche Differentiates Three Microbial Life Strategies That Influence Soil Nitrogen Availability During and After Winter |
title_sort | snowmelt niche differentiates three microbial life strategies that influence soil nitrogen availability during and after winter |
topic | snowmelt watershed life history strategy soil nitrogen soil archaea and bacteria soil fungi |
url | https://www.frontiersin.org/article/10.3389/fmicb.2020.00871/full |
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