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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 Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE; Argonne National Laboratory
OSTI Identifier:
1392633
Grant/Contract Number:
AC02-06CH11357
Resource Type:
Journal Article: 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. doi: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. doi: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}
}

Journal Article:
Free Publicly Available Full Text
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Citation Metrics:
Cited by: 93works
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  • Understanding the spatial patterns of organisms and the underlying mechanisms shaping biotic communities is a central goal in community ecology. One of the most well documented spatial patterns in plant and animal communities is the positive-power law relationship between species (or taxa) richness and area. Such a taxa-area relationships (TARs) are one of the principal generalizations in ecology, and are fundamental to our understanding of the distribution of global biodiversity. However, TARs remain elusive and controversial in microbial communities, especially in soil habitats, due to inadequate sampling methodologies. Here, we describe TARs, at a whole-community level, across various microbial functionalmore » and phylogenetic groups in a forest soil using a comprehensive functional gene array (FGA) with > 24,000 probes. Our analysis indicated that the forest soil microbial community exhibited a relatively flat taxa-area relationship (slope z = 0.0624), but the z values varied considerably across different functional and phylogenetic groups (z = 0.0475-0.0959), which are several times lower than those commonly observed in higher plants and animals. These results suggest that the turnover in space of microorganisms may be, in general, lower than that of plants and animals.« less
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