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Ecology and exploration of the rare biosphere

This article has been updated

Key Points

  • Microbial-community abundance distributions have a long 'tail' of low-abundance organisms, referred to as the rare biosphere, which often comprises the large majority of species.

  • Rare-biosphere microorganisms display specific and sometimes unique ecology and biogeography that can differ substantially from that of more abundant representatives.

  • The rare biosphere contributes to a persistent microbial seed bank, contrasting the influence of local microbial extinction and immigration.

  • Recruitment from the rare biosphere provides a broad reservoir of ecological function and resiliency (redundancy and flexibility).

  • Broad time-series studies with rich metadata will improve the study of rare-biosphere dynamics and conditionally rare taxa.

  • Study of the rare biosphere is prone to experimental artefacts (sequencing noise) and biological artefacts (dormancy and taphonomic gradients).

  • The majority of microbial diversity exists, at least transiently, in the rare biosphere.

  • Novel rare-biosphere members can be studied through cultivation, targeted phylogenetic mining and single-cell genomics.

Abstract

The profound influence of microorganisms on human life and global biogeochemical cycles underlines the value of studying the biogeography of microorganisms, exploring microbial genomes and expanding our understanding of most microbial species on Earth: that is, those present at low relative abundance. The detection and subsequent analysis of low-abundance microbial populations — the 'rare biosphere' — have demonstrated the persistence, population dynamics, dispersion and predation of these microbial species. We discuss the ecology of rare microbial populations, and highlight molecular and computational methods for targeting taxonomic 'blind spots' within the rare biosphere of complex microbial communities.

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Figure 1: Rank–abundance curves.
Figure 2: Hypothetical temporal abundance profiles for rare-biosphere microorganisms.

Change history

  • 06 March 2015

    On page 6 the paper by Doxey, A. C. et al. entitled 'Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production'. ISME J. 9, 461–471 (2015) should have been cited at the end of the sentence ‘The recent discovery of thaumarchaeotal vitamin B12 production in aquatic environments also demonstrated winter archaeal abundance at station L4, in contrast to the low relative abundance of related genes at other sampled time points’ instead of reference 75. We have added this new reference as Ref 181 in the reference list.

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Acknowledgements

The authors appreciate comments provided by M. L. Sogin and B. J. Butler during the preparation of this manuscript. They acknowledge support from an Early Researcher Award (Government of Ontario), the Canadian Institutes of Health Research (CIHR) and the Natural Sciences and Engineering Research Council of Canada (NSERC).

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Glossary

Rare biosphere

Although this has been an arbitrarily defined term, subject to variable abundance thresholds (for example, <0.1% of total community relative abundance), the rare biosphere may be considered as the collective of rare viable or dormant microbial taxa that are found in a given environmental sample at a specific time point.

Bioprospecting

The screening of biological systems (for example, genomes or ecosystems) for novel components of industrial, commercial or scientific value.

Conditionally rare taxa

Species that are rare under some conditions but can become abundant when provided with optimal growth conditions.

Resilience

The ability of a community to regain functionality following a disturbance event. This ability is linked to role redundancy conferred through species diversity.

Operational taxonomic units

(OTUs). Commonly used theoretical framework for relating sequence differences to discrete taxonomic entities. The OTU remains a surrogate for a taxonomic rank (for example, species) and is typically based on a specified nucleotide identity (for example, 97% for small subunit ribosomal RNA marker-gene studies).

Biogeography

The study of species distribution through geographic space and time.

Copiotrophic

Microorganisms that grow optimally in nutrient-rich environments and are generally adapted to rapidly exploit available resources.

Killing-the-winner hypothesis

A negative frequency-dependent selection, in which abundant or active bacterial types are affected by viral pressure. This mechanism would promote the survival and viability of rare types of microorganisms, maintaining high diversity.

Taphonomic gradient

A temporal gradient involving decay and fossilization of cells. In the context of studying the rare biosphere, the term refers to the detection of nucleic acids from deceased organisms.

Microbial seed bank

A collection of dormant microorganisms that can respond to favourable environmental conditions.

r-selected growth

Growth strategy favouring rapid reproduction and exponential population size increase. It is common in organisms such as bacteria, insects and weeds.

K-selected growth

Growth strategy in which abundance tends to be stable and close to the maximum capacity in an environment. Populations undergoing K-selected growth often have larger body sizes, slower growth rates and longer life cycles.

Epilimnion

Top layer in a thermally stratified lake, typically with increased dissolved oxygen concentrations.

Hypolimnion

Dense bottom layer of a thermally stratified lake (below the epilimnion).

Black Queen hypothesis

A theory explaining reductive evolution in free-living organisms and dependence on co-occurring microorganisms. Natural selection favours the loss of costly biological functions ('leaky' functions) as long as the function is retained by a subset of the community and provides an indispensable public good.

Synapomorphic

A derived characteristic shared by two or more taxa and their most recent common ancestor.

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Lynch, M., Neufeld, J. Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13, 217–229 (2015). https://doi.org/10.1038/nrmicro3400

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