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Bacterial transformation: distribution, shared mechanisms and divergent control

Nature Reviews Microbiology volume 12, pages 181–196 (2014)Cite this article

Subjects

Key Points

  • This Review discusses natural bacterial transformation, highlighting the common and divergent features that exist in a phylogenetically diverse range of naturally transformable species.

  • Transformation is defined as the uptake of foreign DNA as single strands and its subsequent integration into the bacterial chromosome by homologous recombination. The mechanisms of uptake and integration, which are largely conserved among species, are highlighted and their conservation is explored.

  • In contrast to DNA-uptake mechanisms, the regulation of the ability to transform (which is known as competence) and the signals that induce competence vary widely between species; the range of mechanisms that are involved are discussed.

  • The roles of competence and imported DNA are also considered, and we argue that evidence so far generally points towards a role for transformation in the generation of genetic diversity or in chromosomal repair, rather than a nutritional role.

  • Finally, we explore the future prospects in this field of research, detailing several case studies of species that have recently been shown to be transformable and the potential difficulties in demonstrating transformability in a new species.

Abstract

Natural bacterial transformation involves the internalization and chromosomal integration of DNA and has now been documented in ∼80 species. Recent advances have established that phylogenetically distant species share conserved uptake and processing proteins but differ in the inducing cues and regulatory mechanisms that are involved. In this Review, we highlight divergent and common principles that govern the transformation process in different bacteria. We discuss how this cumulative knowledge enables the prediction of new transformable species and supports the idea that the main role of internalized DNA is in the generation of genetic diversity or in chromosome repair rather than in nutrition.

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Figure 1: Phylogenetic distribution of naturally transformable species, the DNA-uptake protein ComEC and the DNA-processing protein DprA.
Figure 2: An overview of the transformation process.
Figure 3: Divergent competence regulatory cascades.

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Acknowledgements

The authors thank Y. Quentin for his help with phylogenetic analysis and the construction of the species tree. The authors apologize to researchers whose work could not be specifically cited owing to space limitations.

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Authors and Affiliations

  1. Centre National de la Recherche Scientifique, LMGM-UMR5100, Toulouse, F-31000, France

    Calum Johnston, Bernard Martin, Gwennaele Fichant, Patrice Polard & Jean-Pierre Claverys

  2. Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, Toulouse, F-31000, France

    Calum Johnston, Bernard Martin, Gwennaele Fichant, Patrice Polard & Jean-Pierre Claverys

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FURTHER INFORMATION

Sun, D. Thesis (reference 153)

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Supplementary information S1 (table)

Naturally transformable bacterial species (XLSX 25 kb)

Glossary

Parasexual

A term used to describe a form of reproduction in which genetic recombination occurs in the absence of meiosis, wherein one 'partner' is DNA.

Homologous recombination

The exchange of DNA sequences between identical or similar molecules. In the case of transformation, this involves the host chromosome and internalized single-stranded DNA (ssDNA).

Transduction

A mechanism of horizontal gene transfer, in which DNA is accidentally transferred to a new host by a bacteriophage vector.

Conjugation

A mechanism of horizontal gene transfer by cell-to-cell contact that is primarily used for plasmid transfer but occasionally leads to chromosomal transfer.

Regulons

Sets of genes that are under coordinated control by dedicated regulatory circuits.

Transformation heteroduplex

A DNA duplex that is comprised of one strand of host chromosomal DNA and a complementary strand of internalized DNA.

Pili

Filamentous extracellular appendages that are present in some bacteria and that participate in different processes. Transformation pili promote the capture of exogenous DNA for uptake.

Alternative sigma factors

(alternative σ factors). Alternative RNA polymerase cofactors that direct the RNA polymerase to specific promoters.

Transcription co-regulators

Proteins that lack DNA-binding activity but can interact with and stimulate the activity of a transcription activator, thus indirectly promoting transcription.

SOS response

A global response to DNA damage that enables DNA repair in bacteria.

Orthologue

A homologous gene that is derived by a speciation event from a single ancestral sequence. Orthologues typically carry out equivalent functions in closely related species.

Two-component signal-transduction system

(TCS). A system that comprises a histidine kinase and a response regulator; TCSs enable bacteria to sense signals (including those in the extracellular environment) and to regulate genes accordingly.

Bacteriocins

Small peptides that are produced by bacteria to inhibit the growth of other species (sometimes closely related species) to which the producer possesses an immunity mechanism.

Non-coding small RNA

A functional RNA molecule that is not translated into a protein.

CAI-1

(Cholerae autoinducer 1).The main quorum-sensing signalling molecule of the human pathogen Vibrio cholerae; it has been identified as (S)-3-hydroxytridecan-4-one.

AI-2

(Autoinducer 2). An inter-genera signalling molecule that is involved in quorum-sensing; it has been identified as the furanyl borate diester (2S,4S)-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran borate.

CSF

(Competence and sporulation factor). A signalling molecule that contributes to quorum-sensing in Bacillus subtilis. CSF is a pentapeptide that is produced from Phr precursor peptide, which is re-imported by the oligopeptide permease Opp.

Pherotypes

Streptococci that produce the same competence-stimulating peptide (CSP) belong to the same pherotype.

Quorum-sensing

The regulation of gene expression in response to cell density; secreted inducing molecules are sensed and induction occurs only when a critical cell density is reached.

Cell–cell signalling

A mechanism of cell–cell communication in which an inducing molecule is produced and can be sensed by neighbouring cells, resulting in coordinated gene expression. This mechanism is not necessarily dependent on cell density owing to the fact that inducer expression can be regulated by external signals.

Alarmone

A signalling molecule that is produced by bacteria in response to stress, which stimulates the expression of proteins involved in cellular processes that counteract the stress.

Autoinducers

Non-proteinaceous chemical signalling molecules that are involved in cell–cell signalling and quorum-sensing.

Carbon catabolite repression

(CCR). A regulatory mechanism in which the regulation of phosphotransferase systems enables the sequential utilization of carbon sources.

Mitomycin C

A DNA-damaging agent that crosslinks target DNA and is toxic to bacterial cells.

Hydroxyurea

A synthetic compound that promotes the stalling of bacterial replication forks by depleting nucleotide pools.

Fratricide

The ability of competent pneumococcal cells to promote lysis of non-competent neighbouring pneumococci and closely related streptococci, liberating DNA for transformation and virulence factors.

Paralogue

One of a pair of homologous genes that are derived by a duplication event from a single sequence. Paralogous relationships occur both within and between genomes, and paralogues can evolve to have novel functions.

Restriction–modification system

(R–M system). A bacterial immune system that protects cells from invading foreign DNA, such as that injected by bacteriophages. Most of these systems encode a restriction enzyme that cleaves specific sequences in unmethylated DNA and a methylase that methylates the host genome, thereby protecting it from restriction.

K-state

An alternative for competence in ComK-possessing bacteria (Bacilli), representing induction of the ComK regulon.

X-state

An alternative for competence in σX-possessing bacteria (Streptococci), representing induction of the σX regulon.

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Johnston, C., Martin, B., Fichant, G. et al. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol 12, 181–196 (2014). https://doi.org/10.1038/nrmicro3199

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