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Mobile DNA in obligate intracellular bacteria

Key Points

  • Mobile genetic elements are a common feature of most prokaryotes. Specific examples include plasmids, bacteriophages, DNA transposable elements and RNA transposable elements. Some prophages can occupy up to 20% of the host bacterial chromosome and comprise the majority of strain-specific DNA in genome comparisons.

  • Facultative intracellular bacteria have a four-fold higher genomic content of mobile DNA than obligate intracellular bacteria. This disparity is probably explained by accelerated deletion rates, intracellular confinement and the deleterious effects of mobile DNA in obligate intracellular species.

  • DNA transposable elements are the most abundant group of mobile elements in intracellular bacteria. They also preferentially suffer from inactivating mutations compared with other genetic parasites. Inserted plasmid genes are uncommon. Extrachromosomal plasmids might be more common in mutualistic endosymbionts and aid the primary functions of dietary endosymbionts in insects.

  • The 'intracellular arena' hypothesis posits that eukaryotic cells that are co-infected by multiple intracellular bacteria will elevate contact with novel gene pools and increase rates of mobile-DNA transfer between intracellular bacteria. Consistent with this hypothesis are the recent inferences of lateral phage transfer between co-infecting Wolbachia endosymbionts.

  • Increasing discoveries of mobile genetic elements in obligate intracellular species should motivate new insights and the development of tractable hypotheses, such as whether transmission differences among intracellular bacteria generally predict distinct outcomes for mobile-DNA content.

Abstract

The small genomes of obligate intracellular bacteria are often presumed to be impervious to mobile DNA and the fluid genetic processes that drive diversification in free-living bacteria. Categorized by reductive evolution and streamlining, the genomes of some obligate intracellular bacteria manifest striking degrees of stability and gene synteny. However, recent findings from complete genome sequences of obligate intracellular species and their mobile genetic associates favour the abandonment of these wholesale terms for a more complex and tantalizing picture.

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Figure 1: Examples of mobile genetic elements in prokaryotes.
Figure 2: Mobile-DNA composition in the genomes of intracellular bacteria.
Figure 3: Correlation of genome size and mobile-DNA composition.
Figure 4: Transposable genetic elements.

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Acknowledgements

Work for this article was supported by a NASA Astrobiology Institute grant and the Evelyn Mercer Professorship of Biochemistry and Molecular Biology, University of Wisconsin, USA. We thank M. Belfort, S. Biber, A. Lazarus, S. Roland and J. Wernegreen for their insightful comments.

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Correspondence to Seth R. Bordenstein.

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DATABASES

Entrez

φCPAR39

φX174

Buchnera aphidicola

Buchnera sp. APS

Chlamydia muridarum

Chlamydia trachomatis

Chlamydophila caviae

Chlamydophila pneumoniae

Chp1

Chp2

Coxiella burnetti

Listeria monocytogenes 4b

Mycobacterium smegmatis

Mycobacterium tuberculosis

Mycoplasma pneumoniae

Streptococcus pneumoniae

Wigglesworthia glossinidia

Wolbachia pipientis

FURTHER INFORMATION

Seth Bordenstein's laboratory

William Reznikoff's homepage

The Comprehensive Microbial Resource

The Institute for Genomic Research

International Symbiosis Society

Wolbachia FIBR Project

Wolbachia

Glossary

COSPECIATION PATTERNS

The speciation in parallel by closely associated species, such as a symbiont and host.

PARASITIC ASSOCIATION

A symbiotic relationship in which the bacteria benefits and the host is harmed.

MUTUALISTIC ASSOCIATION

A symbiotic relationship that benefits both the bacteria and its host.

COMMENSAL ASSOCIATION

A symbiotic relationship that benefits the bacteria but causes no important harm or benefit to the host.

REDUCTIVE EVOLUTION

The process by which genomes of obligate intracellular bacteria shrink and undergo extreme levels of gene degradation and loss.

DELETION BIASES

The mutational bias by which DNA deletions outnumber DNA insertions.

TROPHALLAXIS

The regurgitation of food from one adult or larvae to another that is most common in social insects such as termites, bees and wasps.

GENETIC DRIFT

An evolutionary process that is characterized by random variation in gene frequencies over time owing to random sampling in finite populations. Genetic drift is often seen in small populations owing to the increased effect of random occurrences in these communities.

FILARIAL DISEASE

Diseases such as human river blindness and elephantiasis that are caused by filarial nematodes and their Wolbachia endosymbionts.

CLADE

A group of genetically related organisms that includes an ancestor and all of its descendants.

TRANSPOSASE GENE

A gene that encodes an enzyme that mediates movement of one segment of genomic DNA into another location.

INSERTION SEQUENCE

A small segment of mobile DNA flanked by inverted repeat sequences that encodes a protein that catalyses transposition.

MATURASE DOMAIN

A region of the reverse-transcriptase gene that ensures proper RNA folding for intron excision from the RNA.

MOBILE GROUP II INTRON

A catalytic RNA molecule that acts as a mobile genetic element as it encodes a reverse transcriptase and can insert site-specifically into target DNA.

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Bordenstein, S., Reznikoff, W. Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3, 688–699 (2005). https://doi.org/10.1038/nrmicro1233

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