Viral but not bacterial community successional patterns reflect extreme turnover shortly after rewetting dry soils

Santos-Medellín, Christian; Blazewicz, Steven J.; Pett-Ridge, Jennifer; Firestone, Mary K.; Emerson, Joanne B.

doi:10.1038/s41559-023-02207-5

Title: Viral but not bacterial community successional patterns reflect extreme turnover shortly after rewetting dry soils

Journal Article · 27 September 2023 · Nature Ecology and Evolution

DOI: https://doi.org/10.1038/s41559-023-02207-5 · OSTI ID:2283632

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^[3]; Firestone, Mary K. ^[4];

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University of California, Davis, CA (United States)
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); University of California, Merced, CA (United States); University of California, Berkeley, CA (United States)
University of California, Berkeley, CA (United States)

As central members of soil trophic networks, viruses have the potential to drive substantial microbial mortality and nutrient turnover. Pinpointing viral contributions to terrestrial ecosystem processes remains a challenge, as temporal dynamics are difficult to unravel in the spatially and physicochemically heterogeneous soil environment. In Mediterranean grasslands, the first rainfall after seasonal drought provides an ecosystem reset, triggering microbial activity during a tractable window for capturing short-term dynamics. In this report we simulated precipitation in microcosms from four distinct dry grassland soils and generated 144 viromes, 84 metagenomes and 84 16S ribosomal RNA gene amplicon datasets to characterize viral, prokaryotic and relic DNA dynamics over 10 days. Vastly different viral communities in each soil followed remarkably similar successional trajectories. Wet-up triggered a significant increase in viral richness, followed by extensive compositional turnover. Temporal succession in prokaryotic communities was much less pronounced, perhaps suggesting differences in the scales of activity captured by viromes (representing recently produced, ephemeral viral particles) and total DNA. Still, differences in the relative abundances of Actinobacteria (enriched in dry soils) and Proteobacteria (enriched in wetted soils) matched those of their predicted phages, indicating viral predation of dominant bacterial taxa. Rewetting also rapidly depleted relic DNA, which subsequently reaccumulated, indicating substantial new microbial mortality in the days after wet-up, particularly of the taxa putatively under phage predation. Production of abundant, diverse viral particles via microbial host cell lysis appears to be a conserved feature of the early response to soil rewetting, and results suggest the potential for ‘Cull-the-Winner’ dynamics, whereby viruses infect and cull but do not decimate dominant host populations.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC52-07NA27344; SC0020163; SC0021198

OSTI ID:: 2283632

Report Number(s):: LLNL-JRNL-852843; 1080377

Journal Information:: Nature Ecology and Evolution, Journal Name: Nature Ecology and Evolution Journal Issue: 11 Vol. 7; ISSN 2397-334X

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (109)

ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Influence of Drying-Rewetting Frequency on Soil Bacterial Community Structure Fierer, N.; Schimel, J. P.; Holden, P. A. Microbial Ecology, Vol. 45, Issue 1 https://doi.org/10.1007/s00248-002-1007-2	journal	January 2003
Microbial biomass response to a rapid increase in water potential when dry soil is wetted Kieft, Thomas L.; soroker, Edith; firestone, Mary K. Soil Biology and Biochemistry, Vol. 19, Issue 2 https://doi.org/10.1016/0038-0717(87)90070-8	journal	January 1987
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Cycling of extracellular DNA in the soil environment Levy-Booth, David J.; Campbell, Rachel G.; Gulden, Robert H. Soil Biology and Biochemistry, Vol. 39, Issue 12 https://doi.org/10.1016/j.soilbio.2007.06.020	journal	December 2007
Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils Xiang, Shu-Rong; Doyle, Allen; Holden, Patricia A. Soil Biology and Biochemistry, Vol. 40, Issue 9 https://doi.org/10.1016/j.soilbio.2008.05.004	journal	September 2008
Viruses in soil: Nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions Kuzyakov, Yakov; Mason-Jones, Kyle Soil Biology and Biochemistry, Vol. 127 https://doi.org/10.1016/j.soilbio.2018.09.032	journal	December 2018
Rewetting of soil: Revisiting the origin of soil CO2 emissions Barnard, Romain L.; Blazewicz, Steven J.; Firestone, Mary K. Soil Biology and Biochemistry, Vol. 147 https://doi.org/10.1016/j.soilbio.2020.107819	journal	August 2020
The ‘Neglected’ Soil Virome – Potential Role and Impact Pratama, Akbar Adjie; van Elsas, Jan Dirk Trends in Microbiology, Vol. 26, Issue 8 https://doi.org/10.1016/j.tim.2017.12.004	journal	August 2018
Diversity in the soil virosphere: to infinity and beyond? Roux, Simon; Emerson, Joanne B. Trends in Microbiology, Vol. 30, Issue 11 https://doi.org/10.1016/j.tim.2022.05.003	journal	November 2022
Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought Bouskill, Nicholas J.; Lim, Hsiao Chien; Borglin, Sharon The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.113	journal	November 2012
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes Weitz, Joshua S.; Stock, Charles A.; Wilhelm, Steven W. The ISME Journal, Vol. 9, Issue 6 https://doi.org/10.1038/ismej.2014.220	journal	January 2015
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.126	journal	July 2017
Lysogeny in nature: mechanisms, impact and ecology of temperate phages Howard-Varona, Cristina; Hargreaves, Katherine R.; Abedon, Stephen T. The ISME Journal, Vol. 11, Issue 7 https://doi.org/10.1038/ismej.2017.16	journal	March 2017
A communal catalogue reveals Earth’s multiscale microbial diversity Thompson, Luke R.; Sanders, Jon G.; McDonald, Daniel Nature, Vol. 551, Issue 7681 https://doi.org/10.1038/nature24621	journal	November 2017
Minimum Information about an Uncultivated Virus Genome (MIUViG) Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E. Nature Biotechnology, Vol. 37, Issue 1 https://doi.org/10.1038/nbt.4306	journal	December 2018
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Relic DNA is abundant in soil and obscures estimates of soil microbial diversity Carini, Paul; Marsden, Patrick J.; Leff, Jonathan W. Nature Microbiology, Vol. 2, Issue 3 https://doi.org/10.1038/nmicrobiol.2016.242	journal	December 2016
Embracing the unknown: disentangling the complexities of the soil microbiome Fierer, Noah Nature Reviews Microbiology, Vol. 15, Issue 10 https://doi.org/10.1038/nrmicro.2017.87	journal	August 2017
Marine viruses — major players in the global ecosystem Suttle, Curtis A. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1750	journal	October 2007
Microbial seed banks: the ecological and evolutionary implications of dormancy Lennon, Jay T.; Jones, Stuart E. Nature Reviews Microbiology, Vol. 9, Issue 2 https://doi.org/10.1038/nrmicro2504	journal	January 2011
Rising to the challenge: accelerated pace of discovery transforms marine virology Brum, Jennifer R.; Sullivan, Matthew B. Nature Reviews Microbiology, Vol. 13, Issue 3 https://doi.org/10.1038/nrmicro3404	journal	February 2015
Niche differentiation is spatially and temporally regulated in the rhizosphere Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0582-x	journal	January 2020
Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil Blazewicz, Steven J.; Hungate, Bruce A.; Koch, Benjamin J. The ISME Journal, Vol. 14, Issue 6 https://doi.org/10.1038/s41396-020-0617-3	journal	March 2020
Soil bacterial populations are shaped by recombination and gene-specific selection across a grassland meadow Crits-Christoph, Alexander; Olm, Matthew R.; Diamond, Spencer The ISME Journal, Vol. 14, Issue 7 https://doi.org/10.1038/s41396-020-0655-x	journal	April 2020
Viromes outperform total metagenomes in revealing the spatiotemporal patterns of agricultural soil viral communities Santos-Medellin, Christian; Zinke, Laura A.; ter Horst, Anneliek M. The ISME Journal, Vol. 15, Issue 7 https://doi.org/10.1038/s41396-021-00897-y	journal	February 2021
Plant-associated fungi support bacterial resilience following water limitation Hestrin, Rachel; Kan, Megan; Lafler, Marissa The ISME Journal, Vol. 16, Issue 12 https://doi.org/10.1038/s41396-022-01308-6	journal	September 2022
Propagation of viral genomes by replicating ammonia-oxidising archaea during soil nitrification Lee, Sungeun; Sieradzki, Ella T.; Nicol, Graeme W. The ISME Journal https://doi.org/10.1038/s41396-022-01341-5	journal	November 2022
Principles of seed banks and the emergence of complexity from dormancy Lennon, Jay T.; den Hollander, Frank; Wilke-Berenguer, Maite Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-24733-1	journal	August 2021
Prolonged drought imparts lasting compositional changes to the rice root microbiome Santos-Medellín, Christian; Liechty, Zachary; Edwards, Joseph Nature Plants, Vol. 7, Issue 8 https://doi.org/10.1038/s41477-021-00967-1	journal	July 2021
Host-linked soil viral ecology along a permafrost thaw gradient Emerson, Joanne B.; Roux, Simon; Brum, Jennifer R. Nature Microbiology, Vol. 3, Issue 8 https://doi.org/10.1038/s41564-018-0190-y	journal	July 2018
Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks Bin Jang, Ho; Bolduc, Benjamin; Zablocki, Olivier Nature Biotechnology, Vol. 37, Issue 6 https://doi.org/10.1038/s41587-019-0100-8	journal	May 2019
CheckV assesses the quality and completeness of metagenome-assembled viral genomes Nayfach, Stephen; Camargo, Antonio Pedro; Schulz, Frederik Nature Biotechnology, Vol. 39, Issue 5 https://doi.org/10.1038/s41587-020-00774-7	journal	December 2020
Improved metagenome binning and assembly using deep variational autoencoders Nissen, Jakob Nybo; Johansen, Joachim; Allesøe, Rosa Lundbye Nature Biotechnology, Vol. 39, Issue 5 https://doi.org/10.1038/s41587-020-00777-4	journal	January 2021
RNA-viromics reveals diverse communities of soil RNA viruses with the potential to affect grassland ecosystems across multiple trophic levels Hillary, Luke S.; Adriaenssens, Evelien M.; Jones, David L. ISME Communications, Vol. 2, Issue 1 https://doi.org/10.1038/s43705-022-00110-x	journal	April 2022
Substantial differences in soil viral community composition within and among four Northern California habitats Durham, Devyn M.; Sieradzki, Ella T.; ter Horst, Anneliek M. ISME Communications, Vol. 2, Issue 1 https://doi.org/10.1038/s43705-022-00171-y	journal	October 2022
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups Placella, S. A.; Brodie, E. L.; Firestone, M. K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1204306109	journal	June 2012
Virus decomposition provides an important contribution to benthic deep-sea ecosystem functioning Dell’Anno, Antonio; Corinaldesi, Cinzia; Danovaro, Roberto Proceedings of the National Academy of Sciences, Vol. 112, Issue 16 https://doi.org/10.1073/pnas.1422234112	journal	April 2015
Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria Xu, Ling; Naylor, Dan; Dong, Zhaobin Proceedings of the National Academy of Sciences, Vol. 115, Issue 18 https://doi.org/10.1073/pnas.1717308115	journal	April 2018
Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil Starr, Evan P.; Nuccio, Erin E.; Pett-Ridge, Jennifer Proceedings of the National Academy of Sciences, Vol. 116, Issue 51 https://doi.org/10.1073/pnas.1908291116	journal	November 2019
Methane-derived carbon flows into host–virus networks at different trophic levels in soil Lee, Sungeun; Sieradzki, Ella T.; Nicolas, Alexa M. Proceedings of the National Academy of Sciences, Vol. 118, Issue 32 https://doi.org/10.1073/pnas.2105124118	journal	August 2021
Spatial turnover of soil viral populations and genotypes overlain by cohesive responses to moisture in grasslands Santos-Medellín, Christian; Estera-Molina, Katerina; Yuan, Mengting Proceedings of the National Academy of Sciences, Vol. 119, Issue 45 https://doi.org/10.1073/pnas.2209132119	journal	November 2022
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
UpSetR: an R package for the visualization of intersecting sets and their properties Conway, Jake R.; Lex, Alexander; Gehlenborg, Nils Bioinformatics, Vol. 33, Issue 18 https://doi.org/10.1093/bioinformatics/btx364	journal	June 2017
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip Bioinformatics https://doi.org/10.1093/bioinformatics/btz848	journal	November 2019
GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy Parks, Donovan H.; Chuvochina, Maria; Rinke, Christian Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab776	journal	September 2021
Crass: identification and reconstruction of CRISPR from unassembled metagenomic data Skennerton, Connor T.; Imelfort, Michael; Tyson, Gene W. Nucleic Acids Research, Vol. 41, Issue 10 https://doi.org/10.1093/nar/gkt183	journal	March 2013
Black box of phage–bacterium interactions: exploring alternative phage infection strategies Mäntynen, Sari; Laanto, Elina; Oksanen, Hanna M. Open Biology, Vol. 11, Issue 9 https://doi.org/10.1098/rsob.210188	journal	September 2021
Dormancy dampens the microbial distance–decay relationship Locey, K. J.; Muscarella, M. E.; Larsen, M. L. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798 https://doi.org/10.1098/rstb.2019.0243	journal	March 2020
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data Yu, Guangchuang; Smith, David K.; Zhu, Huachen Methods in Ecology and Evolution, Vol. 8, Issue 1 https://doi.org/10.1111/2041-210X.12628	journal	September 2016
The metavirome of a hypersaline environment: The metavirome of a hypersaline environment Santos, Fernando; Yarza, Pablo; Parro, Víctor Environmental Microbiology, Vol. 12, Issue 11 https://doi.org/10.1111/j.1462-2920.2010.02273.x	journal	November 2010
Phage-host interactions in soil Marsh, P.; Wellington, E. M. H. FEMS Microbiology Ecology, Vol. 15, Issue 1-2 https://doi.org/10.1111/j.1574-6941.1994.tb00234.x	journal	November 1994
Viral decay and viral production rates in continental-shelf and deep-sea sediments of the Mediterranean Sea Corinaldesi, Cinzia; Dell'Anno, Antonio; Magagnini, Mirko FEMS Microbiology Ecology, Vol. 72, Issue 2 https://doi.org/10.1111/j.1574-6941.2010.00840.x	journal	May 2010
Marine viruses and global climate change Danovaro, Roberto; Corinaldesi, Cinzia; Dell'Anno, Antonio FEMS Microbiology Reviews, Vol. 35, Issue 6 https://doi.org/10.1111/j.1574-6976.2010.00258.x	journal	November 2011
Ecology of viruses in soils: Past, present and future perspectives Kimura, Makoto; Jia, Zhong-Jun; Nakayama, Natsuko Soil Science and Plant Nutrition, Vol. 54, Issue 1 https://doi.org/10.1111/j.1747-0765.2007.00197.x	journal	February 2008
Extracellular DNA Plays a Key Role in Deep-Sea Ecosystem Functioning Dell'Anno, A. Science, Vol. 309, Issue 5744 https://doi.org/10.1126/science.1117475	journal	September 2005
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Transcriptional Response of Nitrifying Communities to Wetting of Dry Soil Placella, Sarah A.; Firestone, Mary K. Applied and Environmental Microbiology, Vol. 79, Issue 10 https://doi.org/10.1128/AEM.00404-13	journal	March 2013
Prevalence of Lysogeny among Soil Bacteria and Presence of 16S rRNA and trzN Genes in Viral-Community DNA Ghosh, D.; Roy, K.; Williamson, K. E. Applied and Environmental Microbiology, Vol. 74, Issue 2 https://doi.org/10.1128/AEM.01435-07	journal	November 2007
New Approaches Indicate Constant Viral Diversity despite Shifts in Assemblage Structure in an Australian Hypersaline Lake Emerson, Joanne B.; Thomas, Brian C.; Andrade, Karen Applied and Environmental Microbiology, Vol. 79, Issue 21 https://doi.org/10.1128/AEM.01946-13	journal	August 2013
Diversity and Metabolism of Marine Bacteria Cultivated on Dissolved DNA Lennon, J. T. Applied and Environmental Microbiology, Vol. 73, Issue 9 https://doi.org/10.1128/AEM.02674-06	journal	March 2007
Validation of Heavy-Water Stable Isotope Probing for the Characterization of Rapidly Responding Soil Bacteria Aanderud, Zachary T.; Lennon, Jay T. Applied and Environmental Microbiology, Vol. 77, Issue 13 https://doi.org/10.1128/AEM.02735-10	journal	May 2011
Biogeography and Degree of Endemicity of Fluorescent Pseudomonas Strains in Soil Cho, J. -C.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5448-5456.2000	journal	December 2000
Viral Production, Decay Rates, and Life Strategies along a Trophic Gradient in the North Adriatic Sea Bongiorni, Lucia; Magagnini, Mirko; Armeni, Monica Applied and Environmental Microbiology, Vol. 71, Issue 11 https://doi.org/10.1128/AEM.71.11.6644-6650.2005	journal	November 2005
Virus decay and its causes in coastal waters Noble, R. T.; Fuhrman, J. A. Applied and Environmental Microbiology, Vol. 63, Issue 1 https://doi.org/10.1128/aem.63.1.77-83.1997	journal	January 1997
How, When, and Where Relic DNA Affects Microbial Diversity Lennon, J. T.; Muscarella, M. E.; Placella, S. A. mBio, Vol. 9, Issue 3 https://doi.org/10.1128/mBio.00637-18	journal	June 2018
Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust Van Goethem, Marc W.; Swenson, Tami L.; Trubl, Gareth mBio, Vol. 10, Issue 6 https://doi.org/10.1128/mBio.02287-19	journal	December 2019
DNA Viral Diversity, Abundance, and Functional Potential Vary across Grassland Soils with a Range of Historical Moisture Regimes Wu, Ruonan; Davison, Michelle R.; Nelson, William C. mBio, Vol. 12, Issue 6 https://doi.org/10.1128/mBio.02595-21	journal	December 2021
Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities Carini, Paul; Delgado-Baquerizo, Manuel; Hinckley, Eve-Lyn S. mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mBio.02776-19	journal	January 2020
Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing Trubl, Gareth; Jang, Ho Bin; Roux, Simon mSystems, Vol. 3, Issue 5 https://doi.org/10.1128/mSystems.00076-18	journal	October 2018
Soil Viruses: A New Hope Emerson, Joanne B. mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/mSystems.00120-19	journal	May 2019
DNase Treatment Improves Viral Enrichment in Agricultural Soil Viromes Sorensen, Jackson W.; Zinke, Laura A.; ter Horst, Anneliek M. mSystems, Vol. 6, Issue 5 https://doi.org/10.1128/mSystems.00614-21	journal	October 2021
Phage-Encoded Sigma Factors Alter Bacterial Dormancy Schwartz, D. A.; Lehmkuhl, B. K.; Lennon, J. T. mSphere, Vol. 7, Issue 4 https://doi.org/10.1128/msphere.00297-22	journal	August 2022
Viruses: unlocking the greatest biodiversity on Earth Suttle, Curtis A. Genome, Vol. 56, Issue 10 https://doi.org/10.1139/gen-2013-0152	journal	October 2013
Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory Williamson, Kurt E.; Fuhrmann, Jeffry J.; Wommack, K. Eric Annual Review of Virology, Vol. 4, Issue 1 https://doi.org/10.1146/annurev-virology-101416-041639	journal	September 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity Tian, Renmao; Ning, Daliang; He, Zhili Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00825-w	journal	April 2020
VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences Kieft, Kristopher; Zhou, Zhichao; Anantharaman, Karthik Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00867-0	journal	June 2020
Uncovering a hidden diversity: optimized protocols for the extraction of dsDNA bacteriophages from soil Göller, Pauline C.; Haro-Moreno, Jose M.; Rodriguez-Valera, Francisco Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-0795-2	journal	February 2020
Active virus-host interactions at sub-freezing temperatures in Arctic peat soil Trubl, Gareth; Kimbrel, Jeffrey A.; Liquet-Gonzalez, Jose Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-021-01154-2	journal	October 2021
Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations ter Horst, Anneliek M.; Santos-Medellín, Christian; Sorensen, Jackson W. Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-021-01156-0	journal	November 2021
iPHoP: An integrated machine learning framework to maximize host prediction for metagenome-derived viruses of archaea and bacteria Roux, Simon; Camargo, Antonio Pedro; Coutinho, Felipe H. PLOS Biology, Vol. 21, Issue 4 https://doi.org/10.1371/journal.pbio.3002083	journal	April 2023
Soil Bacterial Community Structure Responses to Precipitation Reduction and Forest Management in Forest Ecosystems across Germany Felsmann, Katja; Baudis, Mathias; Gimbel, Katharina PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0122539	journal	April 2015
Welcome to the Tidyverse Wickham, Hadley; Averick, Mara; Bryan, Jennifer Journal of Open Source Software, Vol. 4, Issue 43 https://doi.org/10.21105/joss.01686	journal	November 2019
Extraction and 16S rRNA Sequence Analysis of Microbiomes Associated with Rice Roots Edwards, Joseph; Santos-Medellín, Christian; Sundaresan, Venkatesan BIO-PROTOCOL, Vol. 8, Issue 12 https://doi.org/10.21769/BioProtoc.2884	journal	January 2018
Population Dynamics of Bacteriophage and Bacillus Subtilis in Soil Pantastico-Caldas, Marissa; Duncan, Kathleen E.; Istock, Conrad A. Ecology, Vol. 73, Issue 5 https://doi.org/10.2307/1940040	journal	October 1992
Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography Ter Horst, Anneliek; Sones, Jacqueline; Fudyma, Jane Dryad https://doi.org/10.25338/b8c934	dataset	January 2023
emmeans: Estimated Marginal Means, aka Least-Squares Means Lenth, Russell V. The American Statistician, Vol. 34, Issue 4, p. 216-221 https://doi.org/10.32614/CRAN.package.emmeans	dataset	March 2025
Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand Thingstad, Tf; Lignell, R. Aquatic Microbial Ecology, Vol. 13 https://doi.org/10.3354/ame013019	journal	January 1997
Production and decay of viruses in aquatic environments Heldal, M.; Bratbak, G. Marine Ecology Progress Series, Vol. 72 https://doi.org/10.3354/meps072205	journal	January 1991
Is the Genetic Landscape of the Deep Subsurface Biosphere Affected by Viruses? Anderson, Rika E.; Brazelton, William J.; Baross, John A. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00219	journal	January 2011
Resuscitation of the rare biosphere contributes to pulses of ecosystem activity Aanderud, Zachary T.; Jones, Stuart E.; Fierer, Noah Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00024	journal	January 2015
Temporal Dynamics of Soil Virus and Bacterial Populations in Agricultural and Early Plant Successional Soils Roy, Krishnakali; Ghosh, Dhritiman; DeBruyn, Jennifer M. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01494	journal	July 2020
Coming-of-Age Characterization of Soil Viruses: A User’s Guide to Virus Isolation, Detection within Metagenomes, and Viromics Trubl, Gareth; Hyman, Paul; Roux, Simon Soil Systems, Vol. 4, Issue 2 https://doi.org/10.3390/soilsystems4020023	journal	April 2020
The generation and maintenance of diversity in microbial communities Fierer, Noah; Lennon, Jay T. American Journal of Botany, Vol. 98, Issue 3 https://doi.org/10.3732/ajb.1000498	journal	March 2011
Databases of dereplicated vOTUs and MAGs recovered from a rewetting experiment on grassland soils Santos-Medellin, Christian Zenodo https://doi.org/10.5281/zenodo.7510627	dataset	January 2023
Uncovering a hidden diversity: optimized protocols for the extraction of dsDNA bacteriophages from soil Göller, Pauline; Haro-Moreno, Jose; Rodriguez-Valera, Francisco figshare https://doi.org/10.6084/m9.figshare.c.4852809	collection	January 2020
VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences Kieft, Kristopher; Zhou, Zhichao; Anantharaman, Karthik figshare https://doi.org/10.6084/m9.figshare.c.5016656.v1	collection	January 2020
Benchmarking viromics: an in silico evaluation of metagenome-enabled estimates of viral community composition and diversity Roux, Simon; Emerson, Joanne B.; Eloe-Fadrosh, Emiley A. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3817	journal	January 2017
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019

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