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Title: Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem

Abstract

Biofilms represent a metabolically active and structurally complex component of freshwater ecosystems. Ephemeral prairie streams are hydrologically harsh and prone to frequent perturbation. Elucidating both functional and structural community changes over time within prairie streams provides a general understanding of microbial responses to environmental disturbance. In this study, we examined microbial succession of biofilm communities at three sites in a third-order stream at Konza Prairie over a 2- to 64-day period. Microbial abundance (bacterial abundance, chlorophyll a concentrations) increased and never plateaued during the experiment. Net primary productivity (net balance of oxygen consumption and production) of the developing biofilms did not differ statistically from zero until 64 days suggesting a balance of the use of autochthonous and allochthonous energy sources until late succession. Bacterial communities (MiSeq analyses of the V4 region of 16S rRNA) established quickly. Bacterial richness, diversity and evenness were high after 2 days and increased over time. Several dominant bacterial phyla (Beta-, Alphaproteobacteria, Bacteroidetes, Gemmatimonadetes, Acidobacteria, Chloroflexi) and genera ( Luteolibacter, Flavobacterium, Gemmatimonas, Hydrogenophaga) differed in relative abundance over space and time. Bacterial community composition differed across both space and successional time. Pairwise comparisons of phylogenetic turnover in bacterial community composition indicated that early-stage succession (≤16 days)more » was driven by stochastic processes, whereas later stages were driven by deterministic selection regardless of site. Finally, our data suggest that microbial biofilms predictably develop both functionally and structurally indicating distinct successional trajectories of bacterial communities in this ecosystem.« less

Authors:
 [1];  [2];  [3];  [4];  [4]
  1. Kansas State Univ., Manhattan, KS (United States). Division of Biology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
  3. Kansas State Univ., Manhattan, KS (United States). Division of Biology; Univ. of Illinois, Urbana-Champaign, Urbana, IL (United States). Department of Plant Biology
  4. Kansas State Univ., Manhattan, KS (United States). Division of Biology
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1346662
Alternate Identifier(s):
OSTI ID: 1401462
Grant/Contract Number:  
AC05-00OR22725; AC06-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Molecular Ecology
Additional Journal Information:
Journal Volume: 25; Journal Issue: 18; Journal ID: ISSN 0962-1083
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; algae; bacteria; commmunity ecology; DNA barcoding; microbial biology

Citation Formats

Veach, Allison M., Stegen, James C., Brown, Shawn P., Dodds, Walter K., and Jumpponen, Ari. Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem. United States: N. p., 2016. Web. doi:10.1111/mec.13784.
Veach, Allison M., Stegen, James C., Brown, Shawn P., Dodds, Walter K., & Jumpponen, Ari. Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem. United States. doi:10.1111/mec.13784.
Veach, Allison M., Stegen, James C., Brown, Shawn P., Dodds, Walter K., and Jumpponen, Ari. Tue . "Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem". United States. doi:10.1111/mec.13784. https://www.osti.gov/servlets/purl/1346662.
@article{osti_1346662,
title = {Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem},
author = {Veach, Allison M. and Stegen, James C. and Brown, Shawn P. and Dodds, Walter K. and Jumpponen, Ari},
abstractNote = {Biofilms represent a metabolically active and structurally complex component of freshwater ecosystems. Ephemeral prairie streams are hydrologically harsh and prone to frequent perturbation. Elucidating both functional and structural community changes over time within prairie streams provides a general understanding of microbial responses to environmental disturbance. In this study, we examined microbial succession of biofilm communities at three sites in a third-order stream at Konza Prairie over a 2- to 64-day period. Microbial abundance (bacterial abundance, chlorophyll a concentrations) increased and never plateaued during the experiment. Net primary productivity (net balance of oxygen consumption and production) of the developing biofilms did not differ statistically from zero until 64 days suggesting a balance of the use of autochthonous and allochthonous energy sources until late succession. Bacterial communities (MiSeq analyses of the V4 region of 16S rRNA) established quickly. Bacterial richness, diversity and evenness were high after 2 days and increased over time. Several dominant bacterial phyla (Beta-, Alphaproteobacteria, Bacteroidetes, Gemmatimonadetes, Acidobacteria, Chloroflexi) and genera (Luteolibacter, Flavobacterium, Gemmatimonas, Hydrogenophaga) differed in relative abundance over space and time. Bacterial community composition differed across both space and successional time. Pairwise comparisons of phylogenetic turnover in bacterial community composition indicated that early-stage succession (≤16 days) was driven by stochastic processes, whereas later stages were driven by deterministic selection regardless of site. Finally, our data suggest that microbial biofilms predictably develop both functionally and structurally indicating distinct successional trajectories of bacterial communities in this ecosystem.},
doi = {10.1111/mec.13784},
journal = {Molecular Ecology},
issn = {0962-1083},
number = 18,
volume = 25,
place = {United States},
year = {2016},
month = {9}
}

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Cited by: 2 works
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Works referenced in this record:

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Stochastic and deterministic assembly processes in subsurface microbial communities
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Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
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Ironing out the wrinkles in the rare biosphere through improved OTU clustering: Ironing out the wrinkles in the rare biosphere
journal, March 2010


Woody plant encroachment, and its removal, impact bacterial and fungal communities across stream and terrestrial habitats in a tallgrass prairie ecosystem
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The under-recognized dominance of Verrucomicrobia in soil bacterial communities
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Unexpected Diversity during Community Succession in the Apple Flower Microbiome
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Effects of floods on fish assemblages in an intermittent prairie stream
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Disentangling the importance of ecological niches from stochastic processes across scales
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  • DOI: 10.1098/rstb.2011.0063

Search and clustering orders of magnitude faster than BLAST
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Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils
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Influential Observations in Linear Regression
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Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis
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Stochasticity, succession, and environmental perturbations in a fluidic ecosystem
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Plant Succession on Pumice at Mount St. Helens, Washington
journal, January 1999


Microbial Biofilms: from Ecology to Molecular Genetics
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Pioneering bacterial and algal communities and potential extracellular enzyme activities of stream biofilms
journal, March 2010


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Temporal Succession in a Desert Stream Ecosystem Following Flash Flooding
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  • DOI: 10.2307/2937346

Biophysical Controls on Community Succession in Stream Biofilms
journal, June 2007

  • Besemer, K.; Singer, G.; Limberger, R.
  • Applied and Environmental Microbiology, Vol. 73, Issue 15
  • DOI: 10.1128/AEM.00588-07

Advances, challenges and a developing synthesis of ecological community assembly theory
journal, August 2011

  • Weiher, Evan; Freund, Deborah; Bunton, Tyler
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1576
  • DOI: 10.1098/rstb.2011.0056

Successional Changes in Bacterial Assemblage Structure During Epilithic Biofilm Development
journal, February 2001


Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Quantifying community assembly processes and identifying features that impose them
journal, June 2013

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  • The ISME Journal, Vol. 7, Issue 11
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Distribution of Runoff and Rivers Related to Vegetative Characteristics, Latitude, and Slope: A Global Perspective
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  • DOI: 10.2307/1468248

QIIME allows analysis of high-throughput community sequencing data
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Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
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Biofouling in water systems
journal, May 1997


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Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils
journal, March 2012

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  • The ISME Journal, Vol. 6, Issue 9
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Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Picante: R tools for integrating phylogenies and ecology
journal, April 2010


Bacterial Community Succession in Natural River Biofilm Assemblages
journal, November 2005


Contributions of microbial biofilms to ecosystem processes in stream mesocosms
journal, November 2003

  • Battin, Tom J.; Kaplan, Louis A.; Denis Newbold, J.
  • Nature, Vol. 426, Issue 6965
  • DOI: 10.1038/nature02152

Data from: Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem
dataset, July 2016

  • Veach, Allison M.; Stegen, James C.; Brown, Shawn P.
  • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1111/mec.13784, 4 files
  • DOI: 10.5061/dryad.m2r17

Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
journal, December 2011

  • Berry, David; Ben Mahfoudh, Karim; Wagner, Michael
  • Applied and Environmental Microbiology, Vol. 78, Issue 2
  • DOI: 10.1128/aem.07448-11

Influential Observations in Linear Regression
journal, March 1979

  • Cook, R. Dennis
  • Journal of the American Statistical Association, Vol. 74, Issue 365
  • DOI: 10.2307/2286747

Comparisons of Nitrification and Denitrification in Prairie and Agriculturally Influenced Streams
journal, August 2002

  • Kemp, Melody J.; Dodds, Walter K.
  • Ecological Applications, Vol. 12, Issue 4
  • DOI: 10.2307/3061032

    Works referencing / citing this record:

    Data from: Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem
    dataset, July 2016

    • Veach, Allison M.; Stegen, James C.; Brown, Shawn P.
    • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1111/mec.13784, 4 files
    • DOI: 10.5061/dryad.m2r17

    The relationship of floods, drying, flow and light to primary production and producer biomass in a prairie stream
    journal, October 1996

    • Dodds, Walter K.; Hutson, Ruth E.; Eichem, Angela C.
    • Hydrobiologia, Vol. 333, Issue 3
    • DOI: 10.1007/bf00013429

    Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis
    journal, July 1984

    • Sartory, D. P.; Grobbelaar, J. U.
    • Hydrobiologia, Vol. 114, Issue 3
    • DOI: 10.1007/bf00031869

    Bacterial Community Succession in Natural River Biofilm Assemblages
    journal, November 2005


    Microbial Community Succession in an Unvegetated, Recently Deglaciated Soil
    journal, December 2006

    • Nemergut, Diana R.; Anderson, Suzanne P.; Cleveland, Cory C.
    • Microbial Ecology, Vol. 53, Issue 1
    • DOI: 10.1007/s00248-006-9144-7

    Bacterial Succession on the Leaf Surface: A Novel System for Studying Successional Dynamics
    journal, February 2009


    Fundamental spatial and temporal disconnections in the hydrology of an intermittent prairie headwater network
    journal, March 2015


    Changes through time: integrating microorganisms into the study of succession
    journal, October 2010


    The under-recognized dominance of Verrucomicrobia in soil bacterial communities
    journal, July 2011


    Biofouling in water systems
    journal, May 1997


    Modeling the Effects of Hydrodynamic Regimes on Microbial Communities within Fluvial Biofilms: Combining Deterministic and Stochastic Processes
    journal, October 2015

    • Li, Yi; Wang, Chao; Zhang, Wenlong
    • Environmental Science & Technology, Vol. 49, Issue 21
    • DOI: 10.1021/acs.est.5b03277

    Unraveling assembly of stream biofilm communities
    journal, January 2012

    • Besemer, Katharina; Peter, Hannes; Logue, Jürg B.
    • The ISME Journal, Vol. 6, Issue 8
    • DOI: 10.1038/ismej.2011.205

    Stochastic and deterministic assembly processes in subsurface microbial communities
    journal, March 2012

    • Stegen, James C.; Lin, Xueju; Konopka, Allan E.
    • The ISME Journal, Vol. 6, Issue 9
    • DOI: 10.1038/ismej.2012.22

    Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
    journal, March 2012

    • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
    • The ISME Journal, Vol. 6, Issue 8
    • DOI: 10.1038/ismej.2012.8

    Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils
    journal, March 2012

    • Crump, Byron C.; Amaral-Zettler, Linda A.; Kling, George W.
    • The ISME Journal, Vol. 6, Issue 9
    • DOI: 10.1038/ismej.2012.9

    Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes
    journal, February 2013


    Quantifying community assembly processes and identifying features that impose them
    journal, June 2013

    • Stegen, James C.; Lin, Xueju; Fredrickson, Jim K.
    • The ISME Journal, Vol. 7, Issue 11
    • DOI: 10.1038/ismej.2013.93

    Contributions of microbial biofilms to ecosystem processes in stream mesocosms
    journal, November 2003

    • Battin, Tom J.; Kaplan, Louis A.; Denis Newbold, J.
    • Nature, Vol. 426, Issue 6965
    • DOI: 10.1038/nature02152

    Stream denitrification across biomes and its response to anthropogenic nitrate loading
    journal, March 2008

    • Mulholland, Patrick J.; Helton, Ashley M.; Poole, Geoffrey C.
    • Nature, Vol. 452, Issue 7184
    • DOI: 10.1038/nature06686

    QIIME allows analysis of high-throughput community sequencing data
    journal, April 2010

    • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
    • Nature Methods, Vol. 7, Issue 5
    • DOI: 10.1038/nmeth.f.303

    Nitrous oxide emission from denitrification in stream and river networks
    journal, December 2010

    • Beaulieu, Jake J.; Tank, Jennifer L.; Hamilton, Stephen K.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 1
    • DOI: 10.1073/pnas.1011464108

    Stochasticity, succession, and environmental perturbations in a fluidic ecosystem
    journal, February 2014

    • Zhou, Jizhong; Deng, Ye; Zhang, Ping
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
    • DOI: 10.1073/pnas.1324044111

    Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession
    journal, March 2015

    • Dini-Andreote, Francisco; Stegen, James C.; van Elsas, Jan Dirk
    • Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
    • DOI: 10.1073/pnas.1414261112

    Influential Observations in Linear Regression
    journal, March 1979


    Mechanisms of Succession in Natural Communities and Their Role in Community Stability and Organization
    journal, November 1977

    • Connell, Joseph H.; Slatyer, Ralph O.
    • The American Naturalist, Vol. 111, Issue 982
    • DOI: 10.1086/283241

    Conceptual Synthesis in Community Ecology
    journal, June 2010

    • Vellend, Mark
    • The Quarterly Review of Biology, Vol. 85, Issue 2
    • DOI: 10.1086/652373

    Picante: R tools for integrating phylogenies and ecology
    journal, April 2010


    Search and clustering orders of magnitude faster than BLAST
    journal, August 2010


    Woody plant encroachment, and its removal, impact bacterial and fungal communities across stream and terrestrial habitats in a tallgrass prairie ecosystem
    journal, September 2015

    • Veach, Allison M.; Dodds, Walter K.; Jumpponen, Ari
    • FEMS Microbiology Ecology, Vol. 91, Issue 10
    • DOI: 10.1093/femsec/fiv109

    FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
    journal, April 2009

    • Price, M. N.; Dehal, P. S.; Arkin, A. P.
    • Molecular Biology and Evolution, Vol. 26, Issue 7
    • DOI: 10.1093/molbev/msp077

    Advances, challenges and a developing synthesis of ecological community assembly theory
    journal, August 2011

    • Weiher, Evan; Freund, Deborah; Bunton, Tyler
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1576
    • DOI: 10.1098/rstb.2011.0056

    Disentangling the importance of ecological niches from stochastic processes across scales
    journal, August 2011

    • Chase, Jonathan M.; Myers, Jonathan A.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1576
    • DOI: 10.1098/rstb.2011.0063

    Effects of floods on fish assemblages in an intermittent prairie stream
    journal, November 2006


    Ironing out the wrinkles in the rare biosphere through improved OTU clustering: Ironing out the wrinkles in the rare biosphere
    journal, March 2010


    Pioneering bacterial and algal communities and potential extracellular enzyme activities of stream biofilms
    journal, March 2010


    Conditioning film and initial biofilm formation on ceramics tiles in the marine environment
    journal, September 2007


    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
    • DOI: 10.1111/mec.12487

    Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
    journal, October 2013


    Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
    journal, June 2007

    • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
    • Applied and Environmental Microbiology, Vol. 73, Issue 16
    • DOI: 10.1128/aem.00062-07

    Biophysical Controls on Community Succession in Stream Biofilms
    journal, June 2007

    • Besemer, K.; Singer, G.; Limberger, R.
    • Applied and Environmental Microbiology, Vol. 73, Issue 15
    • DOI: 10.1128/aem.00588-07

    Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
    journal, October 2009

    • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
    • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
    • DOI: 10.1128/aem.01541-09

    Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
    journal, September 2011

    • Berry, David; Ben Mahfoudh, Karim; Wagner, Michael
    • Applied and Environmental Microbiology, Vol. 77, Issue 21
    • DOI: 10.1128/aem.05220-11

    Unexpected Diversity during Community Succession in the Apple Flower Microbiome
    journal, February 2013


    Microbial Biofilms: from Ecology to Molecular Genetics
    journal, December 2000


    Permutation tests for univariate or multivariate analysis of variance and regression
    journal, March 2001

    • Anderson, Marti J.
    • Canadian Journal of Fisheries and Aquatic Sciences, Vol. 58, Issue 3
    • DOI: 10.1139/f01-004

    What Are Species Pools and When Are They Important?
    journal, November 2014


    Climate Change Effects on Aquatic Biota, Ecosystem Structure and Function
    journal, November 2006


    Life on the Edge: The Ecology of Great Plains Prairie Streams
    journal, January 2004


    Plant Succession on Pumice at Mount St. Helens, Washington
    journal, January 1999


    Successional Changes in Bacterial Assemblage Structure During Epilithic Biofilm Development
    journal, February 2001


    Comparisons of Nitrification and Denitrification in Prairie and Agriculturally Influenced Streams
    journal, August 2002


    Dynamic influences of nutrients and grazing fish on periphyton during recovery from flood
    journal, June 2011

    • Murdock, Justin N.; Dodds, Walter K.; Gido, Keith B.
    • Journal of the North American Benthological Society, Vol. 30, Issue 2
    • DOI: 10.1899/10-039.1

    Distribution of Runoff and Rivers Related to Vegetative Characteristics, Latitude, and Slope: A Global Perspective
    journal, March 1997

    • Dodds, Walter K.
    • Journal of the North American Benthological Society, Vol. 16, Issue 1
    • DOI: 10.2307/1468248

    Experimental Investigations of Disturbance and Ecological Succession in a Rocky Intertidal Algal Community
    journal, February 1979

    • Sousa, Wayne P.
    • Ecological Monographs, Vol. 49, Issue 3
    • DOI: 10.2307/1942484

    The Individualistic Concept of the Plant Association
    journal, January 1926

    • Gleason, H. A.
    • Bulletin of the Torrey Botanical Club, Vol. 53, Issue 1
    • DOI: 10.2307/2479933

    Temporal Succession in a Desert Stream Ecosystem Following Flash Flooding
    journal, February 1982

    • Fisher, Stuart G.; Gray, Lawrence J.; Grimm, Nancy B.
    • Ecological Monographs, Vol. 52, Issue 1
    • DOI: 10.2307/2937346

    Distinct Taxonomic and Functional Profiles of the Microbiome Associated With Different Soil Horizons of a Moist Tussock Tundra in Alaska
    journal, June 2019


    Distinct Taxonomic and Functional Profiles of the Microbiome Associated With Different Soil Horizons of a Moist Tussock Tundra in Alaska
    journal, June 2019