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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Main Authors: Patrick O. Sorensen, Harry R. Beller, Markus Bill, Nicholas J. Bouskill, Susan S. Hubbard, Ulas Karaoz, Alexander Polussa, Heidi Steltzer, Shi Wang, Kenneth H. Williams, Yuxin Wu, Eoin L. Brodie
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Microbiology
Subjects:
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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