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Diversity within species: interpreting strains in microbiomes

Abstract

Studying within-species variation has traditionally been limited to culturable bacterial isolates and low-resolution microbial community fingerprinting. Metagenomic sequencing and technical advances have enabled culture-free, high-resolution strain and subspecies analyses at high throughput and in complex environments. This holds great scientific promise but has also led to an overwhelming number of methods and terms to describe infraspecific variation. This Review aims to clarify these advances by focusing on the diversity within bacterial and archaeal species in the context of microbiomics. We cover foundational microevolutionary concepts relevant to population genetics and summarize how within-species variation can be studied and stratified directly within microbial communities with a focus on metagenomics. Finally, we describe how common applications of within-species variation can be achieved using metagenomic data. We aim to guide the selection of appropriate terms and analytical approaches to facilitate researchers in benefiting from the increasing availability of large, high-resolution microbiome genetic sequencing data.

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Fig. 1: Drivers of variability within bacterial species.
Fig. 2: Within-species stratification.
Fig. 3: Applications of within-species variation.

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Acknowledgements

Funding for research in the authors’ laboratories was provided by the European Research Council (ERC) (grant ERC-AdG-669830 MicrobioS), the European Union’s Horizon 2020 Research and Innovation Programme (grant 825694 MICROB-PREDICT), the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung, BMBF) (grant 01GL1746B PRIMAL) and the European Molecular Biology Laboratory (EMBL).

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Glossary

Conspecific

Belonging to the same species; for example, conspecific strains are strains that belong to the same species.

Metagenomics

The study of all genomes present in a sample from a microbial community. Often performed as shotgun metagenomics, in which extracted DNA is fragmented before sequencing.

Population

A set of individuals who occupy a particular spatial area.

Mutator allele

Genetic variation (allele) that results in an increased mutation rate.

Genetic drift

Change of allele frequencies in a population caused by stochastic factors.

Horizontal gene transfer

(HGT). The movement of genetic information between organisms, in contrast to vertical gene transfer from parent to offspring.

Homologous recombination

(HR). Type of genetic recombination in which genetic material is exchanged between two similar or identical regions of DNA.

Marker genes

In microbiome context: genes or genetic segments, the presence or specific DNA sequence of which is distinctive of a category of interest such as a species or clade.

Selective sweep

A reduction of the genetic variation in a population owing to selection acting on novel mutations or existing alleles.

Hard selective sweep

One beneficial allele at a locus replaces most other alleles in the population.

Soft selective sweeps

Multiple beneficial alleles at a locus gain prevalence, replacing standing genetic variation in the population.

Infraspecific

Below species level, that is, at a higher resolution than species.

Metagenome-assembled genomes

(MAGs). Genome sequences recovered from metagenomic data, usually fragmented, and potentially incomplete or contaminated. Typically, shotgun metagenomic sequencing produces short DNA sequences that are then assembled and binned into ‘genomes’ using k-mer frequencies and abundance information.

Type strains

Living cultures that serve as a fixed reference point for the assignment of bacterial and archaeal names. They are descended from the original isolate used in a species’ description and share all of its relevant phenotypic and genotypic properties.

Microbiomics

The study of microbial communities (microbiomes) using one or more -omic approaches; for example, genomics, transcriptomics and proteomics.

Polyphyletic

Describes a group of organisms that do not share an immediate common ancestor; not a clade.

Guilds

A guild is a group of species that use the same type of resources in a similar way; although originally defined as a group of species (Root, 1967), the concept could be applied to strains or subspecies.

Genome-wide sweep

Alleles at the locus under selection cause other linked loci (for example, genome and plasmid) to gain or lose abundance across the population; also known as a broad sweep.

Gene-specific sweep

Only alleles at the locus under selection gain or lose abundance across the population; also known as a narrow or locus-specific sweep.

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Van Rossum, T., Ferretti, P., Maistrenko, O.M. et al. Diversity within species: interpreting strains in microbiomes. Nat Rev Microbiol 18, 491–506 (2020). https://doi.org/10.1038/s41579-020-0368-1

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