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 communi...

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Autores principales:	Ashley Shade, Stuart E. Jones, J. Gregory Caporaso, Jo Handelsman, Rob Knight, Noah Fierer, Jack A. Gilbert
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8eb6c7f2f3e64dc3a32d4afd838bb367
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spelling	oai:doaj.org-article:8eb6c7f2f3e64dc3a32d4afd838bb3672021-11-15T15:47:22ZConditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity10.1128/mBio.01371-142150-7511https://doaj.org/article/8eb6c7f2f3e64dc3a32d4afd838bb3672014-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01371-14https://doaj.org/toc/2150-7511ABSTRACT 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. This observation was true across a wide range of ecosystems, indicating that these rare taxa are essential for understanding community changes over time. IMPORTANCE Microbial communities and their processes are the foundations of ecosystems. The ecological roles of rare microorganisms are largely unknown, but it is thought that they contribute to community stability by acting as a reservoir that can rapidly respond to environmental changes. We investigated the occurrence of typically rare taxa that very occasionally become more prominent in their communities (“conditionally rare”). We quantified conditionally rare taxa in time series from a wide variety of ecosystems and discovered that not only were conditionally rare taxa present in all of the examples, but they also contributed disproportionately to temporal changes in diversity when they were most abundant. This result indicates an important and general role for rare microbial taxa within their communities.Ashley ShadeStuart E. JonesJ. Gregory CaporasoJo HandelsmanRob KnightNoah FiererJack A. GilbertAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 4 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Ashley Shade Stuart E. Jones J. Gregory Caporaso Jo Handelsman Rob Knight Noah Fierer Jack A. Gilbert Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity
description	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 than is apparent from their low proportional abundances. This observation was true across a wide range of ecosystems, indicating that these rare taxa are essential for understanding community changes over time. IMPORTANCE Microbial communities and their processes are the foundations of ecosystems. The ecological roles of rare microorganisms are largely unknown, but it is thought that they contribute to community stability by acting as a reservoir that can rapidly respond to environmental changes. We investigated the occurrence of typically rare taxa that very occasionally become more prominent in their communities (“conditionally rare”). We quantified conditionally rare taxa in time series from a wide variety of ecosystems and discovered that not only were conditionally rare taxa present in all of the examples, but they also contributed disproportionately to temporal changes in diversity when they were most abundant. This result indicates an important and general role for rare microbial taxa within their communities.
format	article
author	Ashley Shade Stuart E. Jones J. Gregory Caporaso Jo Handelsman Rob Knight Noah Fierer Jack A. Gilbert
author_facet	Ashley Shade Stuart E. Jones J. Gregory Caporaso Jo Handelsman Rob Knight Noah Fierer Jack A. Gilbert
author_sort	Ashley Shade
title	Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity
title_short	Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity
title_full	Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity
title_fullStr	Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity
title_full_unstemmed	Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity
title_sort	conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/8eb6c7f2f3e64dc3a32d4afd838bb367
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Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity

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