Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity

By A. Shade, Stuart E. Jones, J. Gregory Caporaso, Jo Handelsman, Rob Knight, Noah Fierer, Jack A. Gilbert. mBio, 2014

637 citations recorded by the source corpus.

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. 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.

Subfields: Ecology, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/a6f62dd5bd9a59b1f22922fe9978800d8e878af1

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Citations in the corpus

Direct and indirect effects of climate change on soil microbial and soil microbial‐plant interactions: What lies ahead? (2015, methodology): “Although this method yields data relevant to potential function, it lacks the depth associated with amplicon sequencing, so rare taxa may be overlooked (Shade et al. 2014, Lynch and Neufeld 2015, Zhou et al. 2015).”
Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils (2020, background): “5–28% of all microbes are ‘conditionally rare taxa’, which are rare in most conditions but may become dominant occasionally (Shade et al., 2014).”
What drives study‐dependent differences in distance–decay relationships of microbial communities? (2021, background): “However, rare microorganisms are well known to be of crucial importance in the context of environmental perturbations (Low- Décarie et al., 2016; Shade et al., 2014) and in providing ecosystem processes (e.g., sulfate reduction in peat soils, Hausmann et al., 2016; and anaerobic ammonia oxidation…”
Where less may be more: how the rare biosphere pulls ecosystems strings (2017, background): “Species that are considered functionally non-relevant under a given environmental condition may become important under changing conditions by providing necessary traits or acting as partners in new interspecific interactions (Shade et al., 2014; Fetzer et al., 2015).”
Ecology and exploration of the rare biosphere (2015, background): “Shade et al. 25 analysed 3,237 samples across 42 timeseries data sets, identifying conditionally rare taxa.”
Microbiome definition re-visited: old concepts and new challenges (2020, background): “For example, as a result of data evaluation methods allowing investigation of taxa with a representation of more than 1% only, rare taxa are often neglected [166].”