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Evolutionary microbial genomics: insights into bacterial host adaptation

Key Points

  • The wealth of genome data for host-adapted bacteria have made it possible to re-examine and quantify the level of integration between bacteria and their hosts.

  • For genera with multiple hosts there seems to be a correlation between host range, host population size and the repertoire of bacterial outer surface proteins.

  • Shifts in bacterial lifestyle towards greater interaction with the host are mediated by mechanisms such as gain of new functions through horizontal gene transfer and duplication and functional divergence of existing genes.

  • Bacteria from many different phyla have established relationships with animals, plants and invertebrates. Mutualistic relationships are mostly seen in invertebrates, suggesting that plants and animals present barriers to obligate mutualism that are difficult to overcome.

  • Secretion systems in bacteria are essential for the interaction with their eukaryotic hosts. Horizontal gene transfer events, functional diversification and innovation through gene duplication of these systems have made it possible for bacteria to adapt to their host in various ways, giving rise to pathogenic or mutualistic relationships.

  • Obligate mutualistic bacteria with highly eroded genomes have survived owing to selective pressure on the essential function they contribute to eukaryotic fitness. This contribution has resulted in intimate relationships, in which some bacteria have transferred their genes to the host nuclear genome or established consortia with other co-habiting symbionts for the benefit of the host.

Abstract

Host-adapted bacteria include mutualists and pathogens of animals, plants and insects. Their study is therefore important for biotechnology, biodiversity and human health. The recent rapid expansion in bacterial genome data has provided insights into the adaptive, diversifying and reductive evolutionary processes that occur during host adaptation. The results have challenged many pre-existing concepts built from studies of laboratory bacterial strains. Furthermore, recent studies have revealed genetic changes associated with transitions from parasitism to mutualism and opened new research avenues to understand the functional reshaping of bacteria as they adapt to growth in the cytoplasm of a eukaryotic host.

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Figure 1: Global phylogeny of host-associated bacteria.
Figure 2: Stages of host adaptation.
Figure 3: Genome size in bacteria correlates with the intracellular stage.

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Acknowledgements

This work was supported by grants to S.G.E.A. from the Swedish Research Council, the Göran Gustafsson Foundation, the Swedish Foundation for Strategic Research and the Knut and Alice Wallenberg Foundation.

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Supplementary information

Supplementary Figure 1 (PDF 161 kb)

Supplementary Table 2

List of some of the main sequenced intracellular genomes (as of January 2010) indicating the genome size, GC contents, number of protein coding genes, RNAs, number of plasmids and the year of publishing as well as lifestyle. (PDF 265 kb)

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Glossary

Mutualistic relationship

A symbiosis in which both species increase their fitness.

Pathogenic relationship

A symbiosis in which one species increases its fitness while the fitness of the other species is adversely affected.

Commensal relationship

A symbiosis in which one partner increases its fitness without affecting the other species.

Endosymbiont

An intracellular organism that contributes to the survival of the host cell and depends on the host for its own persistence. The relationship can be either mutualistic or commensalistic.

Protozoan

A single-celled (usually microscopic) eukaryotic organism. The name originates from the Greek words 'proton' and 'zoa', meaning first and animals, respectively.

Horizontal gene transfer

The transfer of genetic material between the genomes of two organisms not through the normal parent–progeny transmission during cell division.

Pseudogenization

The process whereby changes in the coding region of a gene that disrupt the function of the gene lead to its inactivation.

Endosymbiotic bacterium

A non-pathogenic bacterium that lives inside host cells.

Bacteriocyte

A specialised host cell that houses obligate mutualistic bacteria.

Conjugation

The physical joining of two bacterial cells to transfer genetic material from the donor cell to the recipient cell through a pilus.

Coefficient of variation

A normalized measure of dispersion of a probability distribution.

Genomic island

A region of the genome that has been acquired through a horizontal event.

Bacteriophage

A virus that infects bacteria and can serve as a vector of novel genetic material.

Prophage

The genome of a bacteriophage when it is integrated into the chromosome of the host bacterium.

Secondary symbiont

A facultative bacterial symbiont that is not essential for host survival and reproduction.

tRNA isoacceptor

One of a group of tRNA species that can bind to different codons for the same amino acid residue.

Rhizobium

One of a group of nitrogen-fixing bacteria that have symbiotic associations with plants.

Virulence

The ability to cause disease by breaking down the protective mechanisms of the host.

Primary endosymbiont

An obligate mutualistic endosymbiont that is essential for host survival and reproduction. Primary endosymbionts are often located in bacteriocytes and are maternally transmitted between host generations.

Psyllids

Small sap-sucking insects, also known as 'jumping plant lice'.

Metagenomics

The functional and sequence-based analysis of the collective microbial genomes contained in an environmental sample.

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Toft, C., Andersson, S. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet 11, 465–475 (2010). https://doi.org/10.1038/nrg2798

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