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Title: Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity

Abstract

Microbial communities typically contain many rare taxa that make up the majority of the observed membership, yet the contribution of this microbial “rare biosphere” to community dynamics is unclear. Using 16S rRNA amplicon sequencing of 3,237 samples from 42 time series of microbial communities from nine different ecosystems (air; marine; lake; stream; adult human skin, tongue, and gut; infant gut; and brewery wastewater treatment), we introduce a new method to detect typically rare microbial taxa that occasionally become very abundant (conditionally rare taxa [CRT]) and then quantify their contributions to temporal shifts in community structure. We discovered that CRT made up 1.5 to 28% of the community membership, represented a broad diversity of bacterial and archaeal lineages, and explained large amounts of temporal community dissimilarity (i.e., up to 97% of Bray-Curtis dissimilarity). Most of the CRT were detected at multiple time points, though we also identified “one-hit wonder” CRT that were observed at only one time point. Using a case study from a temperate lake, we gained additional insights into the ecology of CRT by comparing routine community time series to large disturbance events. Our results reveal that many rare taxa contribute a greater amount to microbial community dynamics thanmore » is apparent from their low proportional abundances. In conclusion, this observation was true across a wide range of ecosystems, indicating that these rare taxa are essential for understanding community changes over time.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7]
  1. Michigan State Univ., East Lansing, MI (United States)
  2. Univ. of Notre Dame, Notre Dame, IN (United States)
  3. Argonne National Lab. (ANL), Argonne, IL (United States); Northern Arizona Univ., Flagstaff, AZ (United States)
  4. Yale Univ., New Haven, CT (United States)
  5. Howard Hughes Medical Institute, Boulder, CO (United States); Univ. of Colorado, Boulder, CO (United States)
  6. Univ. of Colorado, Boulder, CO (United States)
  7. Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Chicago, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE; Argonne National Laboratory
OSTI Identifier:
1392633
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 5; Journal Issue: 4; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Shade, Ashley, Jones, Stuart E., Caporaso, J. Gregory, Handelsman, Jo, Knight, Rob, Fierer, Noah, and Gilbert, Jack A. Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity. United States: N. p., 2014. Web. doi:10.1128/mBio.01371-14.
Shade, Ashley, Jones, Stuart E., Caporaso, J. Gregory, Handelsman, Jo, Knight, Rob, Fierer, Noah, & Gilbert, Jack A. Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity. United States. https://doi.org/10.1128/mBio.01371-14
Shade, Ashley, Jones, Stuart E., Caporaso, J. Gregory, Handelsman, Jo, Knight, Rob, Fierer, Noah, and Gilbert, Jack A. Tue . "Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity". United States. https://doi.org/10.1128/mBio.01371-14. https://www.osti.gov/servlets/purl/1392633.
@article{osti_1392633,
title = {Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity},
author = {Shade, Ashley and Jones, Stuart E. and Caporaso, J. Gregory and Handelsman, Jo and Knight, Rob and Fierer, Noah and Gilbert, Jack A.},
abstractNote = {Microbial communities typically contain many rare taxa that make up the majority of the observed membership, yet the contribution of this microbial “rare biosphere” to community dynamics is unclear. Using 16S rRNA amplicon sequencing of 3,237 samples from 42 time series of microbial communities from nine different ecosystems (air; marine; lake; stream; adult human skin, tongue, and gut; infant gut; and brewery wastewater treatment), we introduce a new method to detect typically rare microbial taxa that occasionally become very abundant (conditionally rare taxa [CRT]) and then quantify their contributions to temporal shifts in community structure. We discovered that CRT made up 1.5 to 28% of the community membership, represented a broad diversity of bacterial and archaeal lineages, and explained large amounts of temporal community dissimilarity (i.e., up to 97% of Bray-Curtis dissimilarity). Most of the CRT were detected at multiple time points, though we also identified “one-hit wonder” CRT that were observed at only one time point. Using a case study from a temperate lake, we gained additional insights into the ecology of CRT by comparing routine community time series to large disturbance events. Our results reveal that many rare taxa contribute a greater amount to microbial community dynamics than is apparent from their low proportional abundances. In conclusion, this observation was true across a wide range of ecosystems, indicating that these rare taxa are essential for understanding community changes over time.},
doi = {10.1128/mBio.01371-14},
journal = {mBio (Online)},
number = 4,
volume = 5,
place = {United States},
year = {Tue Jul 15 00:00:00 EDT 2014},
month = {Tue Jul 15 00:00:00 EDT 2014}
}

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Sustaining Rare Marine Microorganisms: Macroorganisms As Repositories and Dispersal Agents of Microbial Diversity
journal, May 2017


Core versus diet-associated and postprandial bacterial communities of the rainbow trout ( Oncorhynchus mykiss ) midgut and faeces
journal, May 2018

  • Mente, Eleni; Nikouli, Eleni; Antonopoulou, Efthimia
  • Biology Open, Vol. 7, Issue 6
  • DOI: 10.1242/bio.034397

Thermal disruption of soil bacterial assemblages decreases diversity and assemblage similarity
journal, February 2019

  • Weiser, Michael D.; Ning, Daliang; Buzzard, Vanessa
  • Ecosphere, Vol. 10, Issue 2
  • DOI: 10.1002/ecs2.2598

Effects of Salinity and Inundation on Microbial Community Structure and Function in a Mangrove Peat Soil
journal, February 2016


Dynamics of herbicide transport and partitioning under event flow conditions in the lower Burdekin region, Australia
journal, January 2012


Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops
journal, September 2019


Inter-personal diversity and temporal dynamics of dental, tongue, and salivary microbiota in the healthy oral cavity
journal, January 2017

  • Hall, Michael W.; Singh, Natasha; Ng, Kester F.
  • npj Biofilms and Microbiomes, Vol. 3, Issue 1
  • DOI: 10.1038/s41522-016-0011-0

Gut microbiota features of the geographically diverse Indian population
posted_content, November 2018


Biogeography and ecological diversity patterns of rare and abundant bacteria in oil-contaminated soils
journal, September 2017

  • Jiao, Shuo; Chen, Weimin; Wei, Gehong
  • Molecular Ecology, Vol. 26, Issue 19
  • DOI: 10.1111/mec.14218

Quantifying long‐term recurrence in planktonic microbial eukaryotes
journal, February 2019

  • Giner, Caterina R.; Balagué, Vanessa; Krabberød, Anders K.
  • Molecular Ecology, Vol. 28, Issue 5
  • DOI: 10.1111/mec.14929

Pipeline for amplifying and analyzing amplicons of the V1–V3 region of the 16S rRNA gene
journal, August 2016


Dynamic linear models guide design and analysis of microbiota studies within artificial human guts
journal, November 2018


Dormancy dynamics and dispersal contribute to soil microbiome resilience
journal, March 2020

  • Sorensen, Jackson W.; Shade, Ashley
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798
  • DOI: 10.1098/rstb.2019.0255

The Microbiomes of Seven Lichen Genera Reveal Host Specificity, a Reduced Core Community and Potential as Source of Antimicrobials
journal, March 2020


Antibiotics-induced monodominance of a novel gut bacterial order
text, January 2019


Where less may be more: how the rare biosphere pulls ecosystems strings
text, January 2017

  • Jousset, Alexandre; Rillig, Matthias C.; Bienhold, Christina
  • Freie Universität Berlin
  • DOI: 10.17169/refubium-25396

Think global, act local: The small-scale environment mainly influences microbial community development and function in lake sediment
text, January 2020

  • Orland, C.; Yakimovich, Km; Mykytczuk, Ncs
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.44763

Multiple Comparative Metagenomics using Multiset k-mer Counting
preprint, January 2016