Regional biogeography versus intra-annual dynamics of the root and soil microbiome
Abstract
Abstract Background Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil). Results To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were moremore »
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1984110
- Grant/Contract Number:
- SC0014108; SC0018409
- Resource Type:
- Published Article
- Journal Name:
- Environmental Microbiome
- Additional Journal Information:
- Journal Name: Environmental Microbiome Journal Volume: 18 Journal Issue: 1; Journal ID: ISSN 2524-6372
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Bell-Dereske, Lukas P., Benucci, Gian Maria Niccolò, da Costa, Pedro Beschoren, Bonito, Gregory, Friesen, Maren L., Tiemann, Lisa K., and Evans, Sarah E. Regional biogeography versus intra-annual dynamics of the root and soil microbiome. United Kingdom: N. p., 2023.
Web. doi:10.1186/s40793-023-00504-x.
Bell-Dereske, Lukas P., Benucci, Gian Maria Niccolò, da Costa, Pedro Beschoren, Bonito, Gregory, Friesen, Maren L., Tiemann, Lisa K., & Evans, Sarah E. Regional biogeography versus intra-annual dynamics of the root and soil microbiome. United Kingdom. https://doi.org/10.1186/s40793-023-00504-x
Bell-Dereske, Lukas P., Benucci, Gian Maria Niccolò, da Costa, Pedro Beschoren, Bonito, Gregory, Friesen, Maren L., Tiemann, Lisa K., and Evans, Sarah E. Wed .
"Regional biogeography versus intra-annual dynamics of the root and soil microbiome". United Kingdom. https://doi.org/10.1186/s40793-023-00504-x.
@article{osti_1984110,
title = {Regional biogeography versus intra-annual dynamics of the root and soil microbiome},
author = {Bell-Dereske, Lukas P. and Benucci, Gian Maria Niccolò and da Costa, Pedro Beschoren and Bonito, Gregory and Friesen, Maren L. and Tiemann, Lisa K. and Evans, Sarah E.},
abstractNote = {Abstract Background Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil). Results To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community. Conclusions Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions.},
doi = {10.1186/s40793-023-00504-x},
journal = {Environmental Microbiome},
number = 1,
volume = 18,
place = {United Kingdom},
year = {Wed Jun 07 00:00:00 EDT 2023},
month = {Wed Jun 07 00:00:00 EDT 2023}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s40793-023-00504-x
https://doi.org/10.1186/s40793-023-00504-x
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild
journal, April 2016
- Nguyen, Nhu H.; Song, Zewei; Bates, Scott T.
- Fungal Ecology, Vol. 20
How do fungal partners affect the evolution and habitat preferences of mycoheterotrophic plants? A case study in Gastrodia
journal, February 2016
- Kinoshita, A.; Ogura-Tsujita, Y.; Umata, H.
- American Journal of Botany, Vol. 103, Issue 2
Metacoder: An R package for visualization and manipulation of community taxonomic diversity data
journal, February 2017
- Foster, Zachary S. L.; Sharpton, Thomas J.; Grünwald, Niklaus J.
- PLOS Computational Biology, Vol. 13, Issue 2
Dissimilar responses of fungal and bacterial communities to soil transplantation simulating abrupt climate changes
journal, April 2019
- Zhao, Mengxin; Sun, Bo; Wu, Linwei
- Molecular Ecology, Vol. 28, Issue 7
CONSTAX2: improved taxonomic classification of environmental DNA markers
journal, May 2021
- Liber, Julian A.; Bonito, Gregory; Benucci, Gian Maria Niccolò
- Bioinformatics, Vol. 37, Issue 21
Temporal turnover of the soil microbiome composition is guild‐specific
journal, September 2021
- Martinović, Tijana; Odriozola, Iñaki; Mašínová, Tereza
- Ecology Letters, Vol. 24, Issue 12
Global negative effects of nitrogen deposition on soil microbes
journal, March 2018
- Zhang, Tian’an; Chen, Han Y. H.; Ruan, Honghua
- The ISME Journal, Vol. 12, Issue 7
Crop Management Impacts the Soybean (Glycine max) Microbiome
journal, June 2020
- Longley, Reid; Noel, Zachary A.; Benucci, Gian Maria Niccolò
- Frontiers in Microbiology, Vol. 11
Power and sample-size estimation for microbiome studies using pairwise distances and PERMANOVA
journal, March 2015
- Kelly, Brendan J.; Gross, Robert; Bittinger, Kyle
- Bioinformatics, Vol. 31, Issue 15
Abundance-occupancy distributions to prioritize plant core microbiome membership
journal, June 2019
- Shade, Ashley; Stopnisek, Nejc
- Current Opinion in Microbiology, Vol. 49
Switchgrass cropping systems affect soil carbon and nitrogen and microbial diversity and activity on marginal lands
journal, May 2022
- Li, Xiufen; Petipas, Renee H.; Antoch, Amanda A.
- GCB Bioenergy, Vol. 14, Issue 8
Accelerated temporal turnover of the soil nematode community under alpine grassland degradation
journal, December 2022
- Wang, Kui; Xue, Kai; Wang, Zongsong
- Land Degradation & Development, Vol. 34, Issue 4
Global patterns in endemicity and vulnerability of soil fungi
journal, September 2022
- Tedersoo, Leho; Mikryukov, Vladimir; Zizka, Alexander
- Global Change Biology, Vol. 28, Issue 22
Lack of belowground mutualisms hinders Pinaceae invasions
journal, September 2009
- Nuñez, Martin A.; Horton, Thomas R.; Simberloff, Daniel
- Ecology, Vol. 90, Issue 9
The bacterial community inhabiting temperate deciduous forests is vertically stratified and undergoes seasonal dynamics
journal, August 2015
- López-Mondéjar, Rubén; Voříšková, Jana; Větrovský, Tomáš
- Soil Biology and Biochemistry, Vol. 87
The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks
journal, November 2013
- Yilmaz, Pelin; Parfrey, Laura Wegener; Yarza, Pablo
- Nucleic Acids Research, Vol. 42, Issue D1
MissForest--non-parametric missing value imputation for mixed-type data
journal, October 2011
- Stekhoven, D. J.; Buhlmann, P.
- Bioinformatics, Vol. 28, Issue 1
PROTEST: A PROcrustean Randomization TEST of community environment concordance
journal, January 1995
- Jackson, Donald A.
- Écoscience, Vol. 2, Issue 3
Applied Spatial Data Analysis with R
book, January 2013
- Bivand, Roger S.; Pebesma, Edzer; Gómez-Rubio, Virgilio
- Springer New York, NY
Tracking of the activity of individual bacteria in temperate forest soils shows guild-specific responses to seasonality
journal, August 2019
- Lladó, Salvador; Větrovský, Tomáš; Baldrian, Petr
- Soil Biology and Biochemistry, Vol. 135
Cellulosic biofuel contributions to a sustainable energy future: Choices and outcomes
journal, June 2017
- Robertson, G. Philip; Hamilton, Stephen K.; Barham, Bradford L.
- Science, Vol. 356, Issue 6345
A meta-analysis of global fungal distribution reveals climate-driven patterns
journal, November 2019
- Větrovský, Tomáš; Kohout, Petr; Kopecký, Martin
- Nature Communications, Vol. 10, Issue 1
Seasonal variation in functional properties of microbial communities in beech forest soil
journal, May 2013
- Koranda, Marianne; Kaiser, Christina; Fuchslueger, Lucia
- Soil Biology and Biochemistry, Vol. 60
Microbial hotspots and hot moments in soil: Concept & review
journal, April 2015
- Kuzyakov, Yakov; Blagodatskaya, Evgenia
- Soil Biology and Biochemistry, Vol. 83
Fitting Linear Mixed-Effects Models Using lme4
journal, January 2015
- Bates, Douglas; Mächler, Martin; Bolker, Ben
- Journal of Statistical Software, Vol. 67, Issue 1
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development
journal, August 2015
- Burns, Adam R.; Stephens, W. Zac; Stagaman, Keaton
- The ISME Journal, Vol. 10, Issue 3
Vertical and temporal variations of soil bacterial and archaeal communities in wheat-soybean rotation agroecosystem
journal, February 2022
- Yokota, Mika; Guan, Yupeng; Fan, Yi
- PeerJ, Vol. 10
Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils
journal, September 2013
- Brown, Shawn P.; Jumpponen, Ari
- Molecular Ecology, Vol. 23, Issue 2
lmerTest Package: Tests in Linear Mixed Effects Models
journal, January 2017
- Kuznetsova, Alexandra; Brockhoff, Per B.; Christensen, Rune H. B.
- Journal of Statistical Software, Vol. 82, Issue 13
UNITE USEARCH/UTAX release for eukaryotes
dataset, January 2020
- Abarenkov, Kessy; Zirk, Allan; Piirmann, Timo
- UNITE Community
Island biogeography of soil bacteria and fungi: similar patterns, but different mechanisms
journal, April 2020
- Li, Shao-peng; Wang, Pandeng; Chen, Yongjian
- The ISME Journal, Vol. 14, Issue 7
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Moving pictures of the human microbiome
journal, January 2011
- Caporaso, J. Gregory; Lauber, Christian L.; Costello, Elizabeth K.
- Genome Biology, Vol. 12, Issue 5
Century long fertilization reduces stochasticity controlling grassland microbial community succession
journal, December 2020
- Liang, Yuting; Ning, Daliang; Lu, Zhenmei
- Soil Biology and Biochemistry, Vol. 151
Indirect Effects of Nitrogen Amendments on Organic Substrate Quality Increase Enzymatic Activity Driving Decomposition in a Mesic Grassland
journal, December 2010
- Tiemann, Lisa K.; Billings, Sharon A.
- Ecosystems, Vol. 14, Issue 2
Dynamics of Soil Bacterial and Fungal Communities During the Secondary Succession Following Swidden Agriculture IN Lowland Forests
journal, June 2021
- Lin, Qiang; Baldrian, Petr; Li, Lingjuan
- Frontiers in Microbiology, Vol. 12
Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro-ecosystems across the globe
journal, April 2018
- Dai, Zhongmin; Su, Weiqin; Chen, Huaihai
- Global Change Biology, Vol. 24, Issue 8
Plant and Soil Drivers of Whole-Plant Microbiomes: Variation in Switchgrass Fungi from Coastal to Mountain Sites
journal, January 2021
- Lee, Marissa R.; Hawkes, Christine V.
- Phytobiomes Journal, Vol. 5, Issue 1
Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment
journal, May 2007
- Ferrier, Simon; Manion, Glenn; Elith, Jane
- Diversity and Distributions, Vol. 13, Issue 3
Global diversity and geography of soil fungi
journal, November 2014
- Tedersoo, Leho; Bahram, Mohammad; Põlme, Sergei
- Science, Vol. 346, Issue 6213
Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients
journal, December 2011
- Fierer, Noah; Lauber, Christian L.; Ramirez, Kelly S.
- The ISME Journal, Vol. 6, Issue 5
Long-term effects of mineral fertilizers on soil microorganisms – A review
journal, August 2014
- Geisseler, Daniel; Scow, Kate M.
- Soil Biology and Biochemistry, Vol. 75
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
journal, July 2019
- Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R.
- Nature Biotechnology, Vol. 37, Issue 8
Rates of weathering and chemical depletion in soils across a chronosequence of Lake Michigan sand dunes
journal, September 1998
- Lichter, John
- Geoderma, Vol. 85, Issue 4
Secret lifestyles of Neurospora crassa
journal, May 2014
- Kuo, Hsiao-Che; Hui, Sun; Choi, Jaeyoung
- Scientific Reports, Vol. 4, Issue 1
Seasonal dynamics of soil microbial diversity and functions along elevations across the treeline
journal, November 2021
- Shen, Congcong; He, Ji-Zheng; Ge, Yuan
- Science of The Total Environment, Vol. 794
When mutualisms matter: Rhizobia effects on plant communities depend on host plant population and soil nitrogen availability
journal, March 2018
- Keller, Kane R.; Lau, Jennifer A.
- Journal of Ecology, Vol. 106, Issue 3
Nitrogen fertilization challenges the climate benefit of cellulosic biofuels
journal, June 2016
- Ruan, Leilei; Bhardwaj, Ajay K.; Hamilton, Stephen K.
- Environmental Research Letters, Vol. 11, Issue 6
Global distribution of earthworm diversity
journal, October 2019
- Phillips, Helen R. P.; Guerra, Carlos A.; Bartz, Marie L. C.
- Science, Vol. 366, Issue 6464
Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient
journal, June 2018
- Roley, Sarah S.; Duncan, David S.; Liang, Di
- PLOS ONE, Vol. 13, Issue 6
Burkholderia phytofirmans strain PsJN advanced development and altered leaf level physiology of switchgrass
journal, December 2015
- Wang, Bingxue; Seiler, John R.; Mei, Chuansheng
- Biomass and Bioenergy, Vol. 83
Structure and function of the global topsoil microbiome
journal, August 2018
- Bahram, Mohammad; Hildebrand, Falk; Forslund, Sofia K.
- Nature, Vol. 560, Issue 7717
Long‐term stability of soil bacterial and fungal community structures revealed in their abundant and rare fractions
journal, July 2021
- Gschwend, Florian; Hartmann, Martin; Hug, Anna‐Sofia
- Molecular Ecology, Vol. 30, Issue 17
Much beyond Mantel: Bringing Procrustes Association Metric to the Plant and Soil Ecologist’s Toolbox
journal, June 2014
- Lisboa, Francy Junio Gonçalves; Peres-Neto, Pedro R.; Chaer, Guilherme Montandon
- PLoS ONE, Vol. 9, Issue 6
Host genotype controls ecological change in the leaf fungal microbiome
journal, August 2022
- VanWallendael, Acer; Benucci, Gian Maria Niccolo; da Costa, Pedro Beschoren
- PLOS Biology, Vol. 20, Issue 8
Global-scale patterns of assemblage structure of soil nematodes in relation to climate and ecosystem properties: Global-scale patterns of soil nematode assemblage structure
journal, April 2014
- Nielsen, Uffe N.; Ayres, Edward; Wall, Diana H.
- Global Ecology and Biogeography, Vol. 23, Issue 9
Sustainable bioenergy production from marginal lands in the US Midwest
journal, January 2013
- Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong
- Nature, Vol. 493, Issue 7433
Malassezia Fungi Are Specialized to Live on Skin and Associated with Dandruff, Eczema, and Other Skin Diseases
journal, June 2012
- Saunders, Charles W.; Scheynius, Annika; Heitman, Joseph
- PLoS Pathogens, Vol. 8, Issue 6
Seasonal, sub-seasonal and diurnal variation of soil bacterial community composition in a temperate deciduous forest
journal, January 2019
- Landesman, William J.; Freedman, Zachary B.; Nelson, David M.
- FEMS Microbiology Ecology, Vol. 95, Issue 2
Managing Plant Microbiomes for Sustainable Biofuel Production
journal, January 2021
- Zhalnina, Kateryna; Hawkes, Christine; Shade, Ashley
- Phytobiomes Journal, Vol. 5, Issue 1
The diversity and biogeography of soil bacterial communities
journal, January 2006
- Fierer, N.; Jackson, R. B.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences
preprint, September 2016
- Edgar, Robert C.
Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly
journal, April 2022
- Beschoren da Costa, Pedro; Benucci, Gian Maria Niccolò; Chou, Ming-Yi
- mBio, Vol. 13, Issue 2
Perenniality and diversity drive output stability and resilience in a 26-year cropping systems experiment
journal, April 2021
- Sanford, Gregg R.; Jackson, Randall D.; Booth, Eric G.
- Field Crops Research, Vol. 263
Temporal dynamics of free‐living nitrogen fixation in the switchgrass rhizosphere
journal, September 2021
- Smercina, Darian N.; Evans, Sarah E.; Friesen, Maren L.
- GCB Bioenergy, Vol. 13, Issue 11
Spatio-temporal dynamics of soil bacterial communities as a function of Amazon forest phenology
journal, March 2018
- Buscardo, Erika; Geml, József; Schmidt, Steven K.
- Scientific Reports, Vol. 8, Issue 1
Endemism and functional convergence across the North American soil mycobiome
journal, April 2014
- Talbot, J. M.; Bruns, T. D.; Taylor, J. W.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
Impacts of nitrogen addition on switchgrass root-associated diazotrophic community structure and function
journal, October 2020
- Smercina, Darian N.; Evans, Sarah E.; Friesen, Maren L.
- FEMS Microbiology Ecology, Vol. 96, Issue 12
Seasonal dynamics of fungal communities in a temperate oak forest soil
journal, September 2013
- Voříšková, Jana; Brabcová, Vendula; Cajthaml, Tomáš
- New Phytologist, Vol. 201, Issue 1
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016
- Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
- Ecology Letters, Vol. 19, Issue 8
Do bacterial and fungal communities assemble differently during primary succession?
journal, January 2014
- Schmidt, S. K.; Nemergut, D. R.; Darcy, J. L.
- Molecular Ecology, Vol. 23, Issue 2
The global soil community and its influence on biogeochemistry
journal, August 2019
- Crowther, T. W.; van den Hoogen, J.; Wan, J.
- Science, Vol. 365, Issue 6455
Long-term excess nitrogen fertilizer increases sensitivity of soil microbial community to seasonal change revealed by ecological network and metagenome analyses
journal, September 2021
- Li, Bing-Bing; Roley, Sarah S.; Duncan, David S.
- Soil Biology and Biochemistry, Vol. 160
Climate warming leads to divergent succession of grassland microbial communities
journal, August 2018
- Guo, Xue; Feng, Jiajie; Shi, Zhou
- Nature Climate Change, Vol. 8, Issue 9