Estimating taxon-specific population dynamics in diverse microbial communities

Koch, Benjamin J.; McHugh, Theresa A.; Hayer, Michaela; Schwartz, Egbert; Blazewicz, Steven J.; Dijkstra, Paul; van Gestel, Natasja; Marks, Jane C.; Mau, Rebecca L.; Morrissey, Ember M.; Pett-Ridge, Jennifer; Hungate, Bruce A.

doi:10.1002/ecs2.2090

Title: Estimating taxon-specific population dynamics in diverse microbial communities

Journal Article · 29 January 2018 · Ecosphere

DOI: https://doi.org/10.1002/ecs2.2090 · OSTI ID:1418693

Koch, Benjamin J. ^[1]; McHugh, Theresa A. ^[2]; Hayer, Michaela ^[3]; Schwartz, Egbert ^[1]; Blazewicz, Steven J. ^[4]; Dijkstra, Paul ^[1]; van Gestel, Natasja ^[3]; Marks, Jane C. ^[1]; Mau, Rebecca L. ^[3]; Morrissey, Ember M. ^[5]; Pett-Ridge, Jennifer ^[4];

^[1]

Northern Arizona Univ., Flagstaff, AZ (United States). Center for Ecosystem Science and Society and Dept. of Biological Sciences
Northern Arizona Univ., Flagstaff, AZ (United States). Center for Ecosystem Science and Society; U.S. Geological Survey, Moab, UT (United States). Southwest Biological Science Center
Northern Arizona Univ., Flagstaff, AZ (United States). Center for Ecosystem Science and Society
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
West Virginia Univ., Morgantown, WV (United States). Division of Plant and Soil Sciences

Understanding how population-level dynamics contribute to ecosystem-level processes is a primary focus of ecological research and has led to important breakthroughs in the ecology of macroscopic organisms. However, the inability to measure population-specific rates, such as growth, for microbial taxa within natural assemblages has limited ecologists’ understanding of how microbial populations interact to regulate ecosystem processes. In this work, we use isotope incorporation within DNA molecules to model taxon-specific population growth in the presence of ¹⁸O-labeled water. By applying this model to phylogenetic marker sequencing data collected from stable-isotope probing studies, we estimate rates of growth, mortality, and turnover for individual microbial populations within soil assemblages. When summed across the entire bacterial community, our taxon-specific estimates are within the range of other whole-assemblage measurements of bacterial turnover. Because it can be applied to environmental samples, the approach we present is broadly applicable to measuring population growth, mortality, and associated biogeochemical process rates of microbial taxa for a wide range of ecosystems and can help reveal how individual microbial populations drive biogeochemical fluxes.

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

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF); Technology Research Initiative Fund (TRIF)

Grant/Contract Number:: AC52-07NA27344; DEB‐1241094; DEB‐1146449; SC0016207; SCW1024; SCW1590

OSTI ID:: 1418693

Alternate ID(s):: OSTI ID: 1418696; OSTI ID: 1474397

Report Number(s):: LLNL-JRNL-731619; LLNL-JRNL-738626; 891927

Journal Information:: Ecosphere, Vol. 9, Issue 1; ISSN 2150-8925

Publisher:: Ecological Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 55 works

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References (95)

Enumeration and biovolume determination of microbial cells - a methodological review and recommendations for applications in ecological research Bölter, Manfred; Bloem, Jaap; Meiners, Klaus Biology and Fertility of Soils, Vol. 36, Issue 4 https://doi.org/10.1007/s00374-002-0537-6	journal	October 2002
The Trophic-Dynamic Aspect of Ecology Lindeman, Raymond L. Ecology, Vol. 23, Issue 4 https://doi.org/10.2307/1930126	journal	October 1942
Turnover of biomass C and P in soil following incorporation of glucose or ryegrass Kouno, K.; Wu, J.; Brookes, P. C. Soil Biology and Biochemistry, Vol. 34, Issue 5 https://doi.org/10.1016/S0038-0717(01)00218-8	journal	May 2002
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
Stable-isotope probing as a tool in microbial ecology Radajewski, Stefan; Ineson, Philip; Parekh, Nisha R. Nature, Vol. 403, Issue 6770, p. 646-649 https://doi.org/10.1038/35001054	journal	February 2000
Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil Blazewicz, Steven J.; Schwartz, Egbert; Firestone, Mary K. Ecology, Vol. 95, Issue 5 https://doi.org/10.1890/13-1031.1	journal	May 2014
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory Nature Biotechnology, Vol. 31, Issue 9 https://doi.org/10.1038/nbt.2676	journal	August 2013
Targeted metagenomics of active microbial populations with stable-isotope probing Coyotzi, Sara; Pratscher, Jennifer; Murrell, J. Colin Current Opinion in Biotechnology, Vol. 41 https://doi.org/10.1016/j.copbio.2016.02.017	journal	October 2016
Potential C and N mineralization and microbial biomass from intact and increasingly disturbed soils of varying texture Franzluebbers, A. Soil Biology and Biochemistry, Vol. 31, Issue 8 https://doi.org/10.1016/S0038-0717(99)00022-X	journal	July 1999
Identification of a complete methane monooxygenase operon from soil by combining stable isotope probing and metagenomic analysis Dumont, Marc G.; Radajewski, Stefan M.; Miguez, Carlos B. Environmental Microbiology, Vol. 8, Issue 7 https://doi.org/10.1111/j.1462-2920.2006.01018.x	journal	July 2006
Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J. Nature Methods, Vol. 10, Issue 1 https://doi.org/10.1038/nmeth.2276	journal	December 2012
Cultivation of unculturable soil bacteria Pham, Van H. T.; Kim, Jaisoo Trends in Biotechnology, Vol. 30, Issue 9 https://doi.org/10.1016/j.tibtech.2012.05.007	journal	September 2012
Organic Production and Turnover in Old Field Succession Odum, Eugene P. Ecology, Vol. 41, Issue 1 https://doi.org/10.2307/1931937	journal	January 1960
Rapid nutrient cycling in leaf litter from invasive plants in Hawai?i Allison, Steven D.; Vitousek, Peter M. Oecologia, Vol. 141, Issue 4 https://doi.org/10.1007/s00442-004-1679-z	journal	August 2004
Organism Size, Life History, and N:P Stoichiometry Elser, James J.; Dobberfuhl, Dean R.; MacKay, Neil A. BioScience, Vol. 46, Issue 9 https://doi.org/10.2307/1312897	journal	October 1996
Loss of Foundation Species: Consequences for the Structure and Dynamics of Forested Ecosystems Ellison, Aaron M.; Bank, Michael S.; Clinton, Barton D. Frontiers in Ecology and the Environment, Vol. 3, Issue 9 https://doi.org/10.2307/3868635	journal	November 2005
Phylogenetic organization of bacterial activity Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.28	journal	March 2016
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
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
Use of radiolabelled thymidine and leucine to estimate bacterial production in soils from continental antarctica. Tibbles, B. J.; Harris, J. M. Applied and environmental microbiology, Vol. 62, Issue 2 https://doi.org/10.1128/AEM.62.2.694-701.1996	journal	January 1996
IMG: the integrated microbial genomes database and comparative analysis system Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1044	journal	December 2011
Zebra Mussel Invasion in a Large, Turbid River: Phytoplankton Response to Increased Grazing Caraco, Nina F.; Cole, Jonathan J.; Raymond, Peter A. Ecology, Vol. 78, Issue 2 https://doi.org/10.1890/0012-9658(1997)078[0588:ZMIIAL]2.0.CO;2	journal	March 1997
Natural History's Place in Science and Society Tewksbury, Joshua J.; Anderson, John G. T.; Bakker, Jonathan D. BioScience, Vol. 64, Issue 4 https://doi.org/10.1093/biosci/biu032	journal	March 2014
Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes Kozarewa, Iwanka; Ning, Zemin; Quail, Michael A. Nature Methods, Vol. 6, Issue 4 https://doi.org/10.1038/nmeth.1311	journal	March 2009
Transformation of Freshwater Ecosystems by Bivalves Strayer, David L.; Caraco, Nina F.; Cole, Jonathan J. BioScience, Vol. 49, Issue 1 https://doi.org/10.2307/1313490	journal	January 1999
Mechanisms of Primary Succession Following Deglaciation at Glacier Bay, Alaska Chapin, F. Stuart; Walker, Lawrence R.; Fastie, Christopher L. Ecological Monographs, Vol. 64, Issue 2 https://doi.org/10.2307/2937039	journal	February 1994
Examining the global distribution of dominant archaeal populations in soil Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory The ISME Journal, Vol. 5, Issue 5 https://doi.org/10.1038/ismej.2010.171	journal	November 2010
Use of 16S rRNA and rpoB Genes as Molecular Markers for Microbial Ecology Studies Case, R. J.; Boucher, Y.; Dahllof, I. Applied and Environmental Microbiology, Vol. 73, Issue 1 https://doi.org/10.1128/AEM.01177-06	journal	October 2006
Measurement of bacterial growth rates in soil Harris, D.; Paul, E. A. Applied Soil Ecology, Vol. 1, Issue 4 https://doi.org/10.1016/0929-1393(94)90005-1	journal	December 1994
Bias and artifacts in multitemplate polymerase chain reactions (PCR) Kanagawa, Takahiro Journal of Bioscience and Bioengineering, Vol. 96, Issue 4 https://doi.org/10.1016/S1389-1723(03)90130-7	journal	January 2003
Understanding Bias in Microbial Community Analysis Techniques due to rrn Operon Copy Number Heterogeneity Crosby, Laurel D.; Criddle, Craig S. BioTechniques, Vol. 34, Issue 4 https://doi.org/10.2144/03344rr01	journal	April 2003
Quantitative Microbial Ecology through Stable Isotope Probing Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 81, Issue 21 https://doi.org/10.1128/AEM.02280-15	journal	August 2015
Growth rate of bacteria is affected by soil texture and extraction procedure Uhlı́řová, E.; Šantrůčková, H. Soil Biology and Biochemistry, Vol. 35, Issue 2 https://doi.org/10.1016/S0038-0717(02)00254-7	journal	February 2003
Microbial numbers and activity in dried and rewetted arable soil under integrated and conventional management Bloem, Jaap; de Ruiter, Peter C.; Koopman, Gerrit J. Soil Biology and Biochemistry, Vol. 24, Issue 7 https://doi.org/10.1016/0038-0717(92)90044-X	journal	July 1992
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.43	journal	April 2017
Rhizosphere priming effect: Its functional relationships with microbial turnover, evapotranspiration, and C–N budgets Cheng, Weixin Soil Biology and Biochemistry, Vol. 41, Issue 9 https://doi.org/10.1016/j.soilbio.2008.04.018	journal	September 2009
Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture Rohland, N.; Reich, D. Genome Research, Vol. 22, Issue 5 https://doi.org/10.1101/gr.128124.111	journal	January 2012
Growing Unculturable Bacteria Stewart, E. J. Journal of Bacteriology, Vol. 194, Issue 16 https://doi.org/10.1128/JB.00345-12	journal	June 2012
Community assembly and food web stability Post, W. M.; Pimm, S. L. Mathematical Biosciences, Vol. 64, Issue 2 https://doi.org/10.1016/0025-5564(83)90002-0	journal	June 1983
Growth dynamics of gut microbiota in health and disease inferred from single metagenomic samples Korem, T.; Zeevi, D.; Suez, J. Science, Vol. 349, Issue 6252 https://doi.org/10.1126/science.aac4812	journal	July 2015
Minor Changes in Soil Bacterial and Fungal Community Composition Occur in Response to Monsoon Precipitation in a Semiarid Grassland McHugh, Theresa A.; Koch, George W.; Schwartz, Egbert Microbial Ecology, Vol. 68, Issue 2 https://doi.org/10.1007/s00248-014-0416-3	journal	April 2014
Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat Kirk Harris, J.; Gregory Caporaso, J.; Walker, Jeffrey J. The ISME Journal, Vol. 7, Issue 1 https://doi.org/10.1038/ismej.2012.79	journal	July 2012
Thymidine incorporation into macromolecules of bacteria extracted from soil by homogenization-centrifugation Bååth, E. Soil Biology and Biochemistry, Vol. 24, Issue 11 https://doi.org/10.1016/0038-0717(92)90066-7	journal	November 1992
The role of ecological theory in microbial ecology Prosser, James I.; Bohannan, Brendan J. M.; Curtis, Tom P. Nature Reviews Microbiology, Vol. 5, Issue 5 https://doi.org/10.1038/nrmicro1643	journal	May 2007
Regulation of Lake Primary Productivity by Food Web Structure Carpenter, S. R.; Kitchell, J. F.; Hodgson, J. R. Ecology, Vol. 68, Issue 6 https://doi.org/10.2307/1939878	journal	December 1987
Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons Acinas, S. G.; Marcelino, L. A.; Klepac-Ceraj, V. Journal of Bacteriology, Vol. 186, Issue 9 https://doi.org/10.1128/JB.186.9.2629-2635.2004	journal	April 2004
Measurement of protein synthesis by soil bacterial assemblages with the leucine incorporation technique B��th, E. Biology and Fertility of Soils, Vol. 17, Issue 2 https://doi.org/10.1007/BF00337747	journal	February 1994
DNA Extraction from Soils: Old Bias for New Microbial Diversity Analysis Methods Martin-Laurent, F.; Philippot, L.; Hallet, S. Applied and Environmental Microbiology, Vol. 67, Issue 5 https://doi.org/10.1128/AEM.67.5.2354-2359.2001	journal	May 2001
Mechanisms of Succession in Natural Communities and Their Role in Community Stability and Organization Connell, Joseph H.; Slatyer, Ralph O. The American Naturalist, Vol. 111, Issue 982 https://doi.org/10.1086/283241	journal	November 1977
Increasing aridity reduces soil microbial diversity and abundance in global drylands Maestre, Fernando T.; Delgado-Baquerizo, Manuel; Jeffries, Thomas C. Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1516684112	journal	December 2015
Diversity in Tropical Rain Forests and Coral Reefs Connell, J. H. Science, Vol. 199, Issue 4335 https://doi.org/10.1126/science.199.4335.1302	journal	March 1978
Measurement of bacterial replication rates in microbial communities Brown, Christopher T.; Olm, Matthew R.; Thomas, Brian C. Nature Biotechnology, Vol. 34, Issue 12 https://doi.org/10.1038/nbt.3704	journal	November 2016
Forest Ecosystem Responses to Exotic Pests and Pathogens in Eastern North America Lovett, Gary M.; Canham, Charles D.; Arthur, Mary A. BioScience, Vol. 56, Issue 5 https://doi.org/10.1641/0006-3568(2006)056[0395:FERTEP]2.0.CO;2	journal	January 2006
Microbial carbon use efficiency and biomass turnover times depending on soil depth – Implications for carbon cycling Spohn, Marie; Klaus, Karoline; Wanek, Wolfgang Soil Biology and Biochemistry, Vol. 96 https://doi.org/10.1016/j.soilbio.2016.01.016	journal	May 2016
Biological Invasion by Myrica Faya in Hawai'i: Plant Demography, Nitrogen Fixation, Ecosystem Effects Vitousek, Peter M.; Walker, Lawrence R. Ecological Monographs, Vol. 59, Issue 3 https://doi.org/10.2307/1942601	journal	February 1989
The Importance of Meiofauna in food Webs: Evidence from an acid Stream Schmid-Araya, J. M.; Hildrew, A. G.; Robertson, A. Ecology, Vol. 83, Issue 5 https://doi.org/10.1890/0012-9658(2002)083[1271:TIOMIF]2.0.CO;2	journal	May 2002
Challenges in the Quest for Keystones Power, Mary E.; Tilman, David; Estes, James A. BioScience, Vol. 46, Issue 8 https://doi.org/10.2307/1312990	journal	September 1996
Fungal and Bacterial Production during the Breakdown of Yellow Poplar Leaves in 2 Streams Weyers, Holly S.; Suberkropp, Keller Journal of the North American Benthological Society, Vol. 15, Issue 4 https://doi.org/10.2307/1467795	journal	December 1996
Loss of foundation species: consequences for the structure and dynamics of forested ecosystems Ellison, Aaron M.; Bank, Michael S.; Clinton, Barton D. Frontiers in Ecology and the Environment, Vol. 3, Issue 9 https://doi.org/10.1890/1540-9295(2005)003[0479:LOFSCF]2.0.CO;2	journal	November 2005
Thymidine incorporation into soil bacteria Bååth, E. Soil Biology and Biochemistry, Vol. 22, Issue 6 https://doi.org/10.1016/0038-0717(90)90160-2	journal	January 1990
Microbial immobilisation and turnover of C labelled substrates in two arable soils under field and laboratory conditions Perelo, L.; Munch, J. Soil Biology and Biochemistry, Vol. 37, Issue 12 https://doi.org/10.1016/j.soilbio.2005.02.039	journal	December 2005
Deciphering microbial interactions and detecting keystone species with co-occurrence networks Berry, David; Widder, Stefanie Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00219	journal	May 2014
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification Berry, David; Ben Mahfoudh, Karim; Wagner, Michael Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/AEM.05220-11	journal	September 2011
Growth of saprotrophic fungi and bacteria in soil: Growth of saprotrophic fungi and bacteria in soil Rousk, Johannes; Bååth, Erland FEMS Microbiology Ecology, Vol. 78, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01106.x	journal	April 2011
Resource Competition between Plankton Algae: An Experimental and Theoretical Approach Tilman, David Ecology, Vol. 58, Issue 2 https://doi.org/10.2307/1935608	journal	March 1977
Thymidine and leucine incorporation in soil bacteria with different cell size B��th, E. Microbial Ecology, Vol. 27, Issue 3 https://doi.org/10.1007/BF00182410	journal	May 1994
The Resource-Ratio Hypothesis of Plant Succession Tilman, David The American Naturalist, Vol. 125, Issue 6 https://doi.org/10.1086/284382	journal	June 1985
Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes: Bacterial biogeography in arctic soils Chu, Haiyan; Fierer, Noah; Lauber, Christian L. Environmental Microbiology, Vol. 12, Issue 11 https://doi.org/10.1111/j.1462-2920.2010.02277.x	journal	November 2010
Biological invasions of fresh water: Empirical rules and assembly theory Moyle, Peter B.; Light, Theo Biological Conservation, Vol. 78, Issue 1-2 https://doi.org/10.1016/0006-3207(96)00024-9	journal	October 1996
Comparison of different standards for real-time PCR-based absolute quantification Dhanasekaran, S.; Doherty, T. Mark; Kenneth, John Journal of Immunological Methods, Vol. 354, Issue 1-2 https://doi.org/10.1016/j.jim.2010.01.004	journal	March 2010
454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases Tedersoo, Leho; Nilsson, R. Henrik; Abarenkov, Kessy New Phytologist, Vol. 188, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03373.x	journal	July 2010
Stable isotope probing with 18O-water to investigate microbial growth and death in environmental samples Schwartz, Egbert; Hayer, Michaela; Hungate, Bruce A. Current Opinion in Biotechnology, Vol. 41 https://doi.org/10.1016/j.copbio.2016.03.003	journal	October 2016
Response of Terrestrial CH4 Uptake to Interactive Changes in Precipitation and Temperature Along a Climatic Gradient Blankinship, Joseph C.; Brown, Jamie R.; Dijkstra, Paul Ecosystems, Vol. 13, Issue 8 https://doi.org/10.1007/s10021-010-9391-9	journal	October 2010
Identification of growing bacteria during litter decomposition in freshwater through H218O quantitative stable isotope probing: Growing bacteria during litter decomposition in freshwater Hayer, Michaela; Schwartz, Egbert; Marks, Jane C. Environmental Microbiology Reports, Vol. 8, Issue 6 https://doi.org/10.1111/1758-2229.12475	journal	October 2016
Growth Rates of Bacterial Communities in Soils at Varying pH: A Comparison of the Thymidine and Leucine Incorporation Techniques Bååth, E. Microbial Ecology, Vol. 36, Issue 3 https://doi.org/10.1007/s002489900118	journal	November 1998
Constraining bacterial production, conversion efficiency and respiration in the Ross Sea, Antarctica, January–February, 1997 Ducklow, Hugh W.; Dickson, Mary-Lynn; Kirchman, David L. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 47, Issue 15-16 https://doi.org/10.1016/S0967-0645(00)00066-7	journal	January 2000
Food Web Complexity and Species Diversity Paine, Robert T. The American Naturalist, Vol. 100, Issue 910 https://doi.org/10.1086/282400	journal	January 1966
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Toward A Method For Measuring Instantaneous Fungal Growth Rates In Field Samples Newell, S. Y.; Fallon, R. D. Ecology, Vol. 72, Issue 5 https://doi.org/10.2307/1940954	journal	October 1991
Characterization of Growing Microorganisms in Soil by Stable Isotope Probing with H218O Schwartz, E. Applied and Environmental Microbiology, Vol. 73, Issue 8 https://doi.org/10.1128/AEM.02021-06	journal	February 2007
Experimental studies on predation: Dispersion factors and predator-prey oscillations Huffaker, C. B. Hilgardia, Vol. 27, Issue 14 https://doi.org/10.3733/hilg.v27n14p343	journal	August 1958
The Order Cytophagales Reichenbach, Hans The Prokaryotes https://doi.org/10.1007/0-387-30747-8_20	book	January 2006
Natural History, Microbes and Sequences: Shouldn't We Look Back Again to Organisms? Lazcano, Antonio PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0021334	journal	August 2011
The detrital food web in a shortgrass prairie Hunt, H. W.; Coleman, D. C.; Ingham, E. R. Biology and Fertility of Soils, Vol. 3-3, Issue 1-2 https://doi.org/10.1007/BF00260580	journal	February 1987
THE ECOLOGICAL CONSEQUENCES OF CHANGES IN BIODIVERSITY: A SEARCH FOR GENERAL PRINCIPLES ¹⁰¹ Tilman, David Ecology, Vol. 80, Issue 5 https://doi.org/10.1890/0012-9658(1999)080[1455:TECOCI]2.0.CO;2	journal	July 1999
Microbial Dysbiosis During Simian Immunodeficiency Virus Infection is Partially Reverted with Combination Anti-retroviral Therapy Blum, Faith C.; Hardy, Britney L.; Bishop-Lilly, Kimberly A. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-63196-0	journal	April 2020
Fungal diversity driven by bark features affects phorophyte preference in epiphytic orchids from southern China Pecoraro, Lorenzo; Rasmussen, Hanne N.; Gomes, Sofia I. F. Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-90877-1	journal	May 2021
DNA Extraction from Soils: Old Bias for New Microbial Diversity Analysis Methods Martin-Laurent, F.; Philippot, L.; Hallet, S. Applied and Environmental Microbiology, Vol. 67, Issue 9 https://doi.org/10.1128/aem.67.9.4397-4397.2001	journal	September 2001
The trophic-dynamic aspect of ecology Lindeman, R. Bulletin of Mathematical Biology, Vol. 53, Issue 1-2 https://doi.org/10.1016/s0092-8240(05)80045-x	journal	January 1991
The Order Cytophagales Reichenbach, Hans The Prokaryotes https://doi.org/10.1007/978-1-4757-2191-1_37	book	January 1992
Bias and Artifacts in Multitemplate Polymerase Chain Reactions(PCR) Kanagawa, Takahiro Journal of Bioscience and Bioengineering, Vol. 96, Issue 4 https://doi.org/10.1263/jbb.96.317	journal	January 2003
The trophic-dynamic aspect of ecology Lindeman, Raymond L. Bulletin of Mathematical Biology, Vol. 53, Issue 1-2 https://doi.org/10.1007/bf02464428	journal	March 1991

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Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
population growth rate
population mortality rate
quantitative stable-isotope probing (qSIP)
rewetting
soil bacteria
turnover