Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities

ABSTRACT Few studies have comprehensively investigated the temporal variability in soil microbial communities despite widespread recognition that the belowground environment is dynamic. In part, this stems from the challenges associated with the high degree of spatial heterogeneity in soil microbial...

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Autores principales: Paul Carini, Manuel Delgado-Baquerizo, Eve-Lyn S. Hinckley, Hannah Holland‐Moritz, Tess E. Brewer, Garrett Rue, Caihong Vanderburgh, Diane McKnight, Noah Fierer
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Publicado: American Society for Microbiology 2020
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Acceso en línea:https://doaj.org/article/6a87ccfb46104e45926f91d53eaecdf3
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spelling oai:doaj.org-article:6a87ccfb46104e45926f91d53eaecdf32021-11-15T15:56:58ZEffects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities10.1128/mBio.02776-192150-7511https://doaj.org/article/6a87ccfb46104e45926f91d53eaecdf32020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02776-19https://doaj.org/toc/2150-7511ABSTRACT Few studies have comprehensively investigated the temporal variability in soil microbial communities despite widespread recognition that the belowground environment is dynamic. In part, this stems from the challenges associated with the high degree of spatial heterogeneity in soil microbial communities and because the presence of relic DNA (DNA from dead cells or secreted extracellular DNA) may dampen temporal signals. Here, we disentangle the relationships among spatial, temporal, and relic DNA effects on prokaryotic and fungal communities in soils collected from contrasting hillslopes in Colorado, USA. We intensively sampled plots on each hillslope over 6 months to discriminate between temporal variability, intraplot spatial heterogeneity, and relic DNA effects on the soil prokaryotic and fungal communities. We show that the intraplot spatial variability in microbial community composition was strong and independent of relic DNA effects and that these spatial patterns persisted throughout the study. When controlling for intraplot spatial variability, we identified significant temporal variability in both plots over the 6-month study. These microbial communities were more dissimilar over time after relic DNA was removed, suggesting that relic DNA hinders the detection of important temporal dynamics in belowground microbial communities. We identified microbial taxa that exhibited shared temporal responses and show that these responses were often predictable from temporal changes in soil conditions. Our findings highlight approaches that can be used to better characterize temporal shifts in soil microbial communities, information that is critical for predicting the environmental preferences of individual soil microbial taxa and identifying linkages between soil microbial community composition and belowground processes. IMPORTANCE Nearly all microbial communities are dynamic in time. Understanding how temporal dynamics in microbial community structure affect soil biogeochemistry and fertility are key to being able to predict the responses of the soil microbiome to environmental perturbations. Here, we explain the effects of soil spatial structure and relic DNA on the determination of microbial community fluctuations over time. We found that intensive spatial sampling was required to identify temporal effects in microbial communities because of the high degree of spatial heterogeneity in soil and that DNA from nonliving sources masks important temporal patterns. We identified groups of microbes with shared temporal responses and show that these patterns were predictable from changes in soil characteristics. These results provide insight into the environmental preferences and temporal relationships between individual microbial taxa and highlight the importance of considering relic DNA when trying to detect temporal dynamics in belowground communities.Paul CariniManuel Delgado-BaquerizoEve-Lyn S. HinckleyHannah Holland‐MoritzTess E. BrewerGarrett RueCaihong VanderburghDiane McKnightNoah FiererAmerican Society for Microbiologyarticlemicrobial seasonalitysoil microbial ecologymicrobial interactionssoil bacterial and fungal communitieshillslope aspectnitrogen cyclingMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution DOAJ
collection DOAJ
language EN
topic microbial seasonality
soil microbial ecology
microbial interactions
soil bacterial and fungal communities
hillslope aspect
nitrogen cycling
Microbiology
QR1-502
spellingShingle microbial seasonality
soil microbial ecology
microbial interactions
soil bacterial and fungal communities
hillslope aspect
nitrogen cycling
Microbiology
QR1-502
Paul Carini
Manuel Delgado-Baquerizo
Eve-Lyn S. Hinckley
Hannah Holland‐Moritz
Tess E. Brewer
Garrett Rue
Caihong Vanderburgh
Diane McKnight
Noah Fierer
Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities
description ABSTRACT Few studies have comprehensively investigated the temporal variability in soil microbial communities despite widespread recognition that the belowground environment is dynamic. In part, this stems from the challenges associated with the high degree of spatial heterogeneity in soil microbial communities and because the presence of relic DNA (DNA from dead cells or secreted extracellular DNA) may dampen temporal signals. Here, we disentangle the relationships among spatial, temporal, and relic DNA effects on prokaryotic and fungal communities in soils collected from contrasting hillslopes in Colorado, USA. We intensively sampled plots on each hillslope over 6 months to discriminate between temporal variability, intraplot spatial heterogeneity, and relic DNA effects on the soil prokaryotic and fungal communities. We show that the intraplot spatial variability in microbial community composition was strong and independent of relic DNA effects and that these spatial patterns persisted throughout the study. When controlling for intraplot spatial variability, we identified significant temporal variability in both plots over the 6-month study. These microbial communities were more dissimilar over time after relic DNA was removed, suggesting that relic DNA hinders the detection of important temporal dynamics in belowground microbial communities. We identified microbial taxa that exhibited shared temporal responses and show that these responses were often predictable from temporal changes in soil conditions. Our findings highlight approaches that can be used to better characterize temporal shifts in soil microbial communities, information that is critical for predicting the environmental preferences of individual soil microbial taxa and identifying linkages between soil microbial community composition and belowground processes. IMPORTANCE Nearly all microbial communities are dynamic in time. Understanding how temporal dynamics in microbial community structure affect soil biogeochemistry and fertility are key to being able to predict the responses of the soil microbiome to environmental perturbations. Here, we explain the effects of soil spatial structure and relic DNA on the determination of microbial community fluctuations over time. We found that intensive spatial sampling was required to identify temporal effects in microbial communities because of the high degree of spatial heterogeneity in soil and that DNA from nonliving sources masks important temporal patterns. We identified groups of microbes with shared temporal responses and show that these patterns were predictable from changes in soil characteristics. These results provide insight into the environmental preferences and temporal relationships between individual microbial taxa and highlight the importance of considering relic DNA when trying to detect temporal dynamics in belowground communities.
format article
author Paul Carini
Manuel Delgado-Baquerizo
Eve-Lyn S. Hinckley
Hannah Holland‐Moritz
Tess E. Brewer
Garrett Rue
Caihong Vanderburgh
Diane McKnight
Noah Fierer
author_facet Paul Carini
Manuel Delgado-Baquerizo
Eve-Lyn S. Hinckley
Hannah Holland‐Moritz
Tess E. Brewer
Garrett Rue
Caihong Vanderburgh
Diane McKnight
Noah Fierer
author_sort Paul Carini
title Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities
title_short Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities
title_full Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities
title_fullStr Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities
title_full_unstemmed Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities
title_sort effects of spatial variability and relic dna removal on the detection of temporal dynamics in soil microbial communities
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/6a87ccfb46104e45926f91d53eaecdf3
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