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Studying plasmid horizontal transfer in situ: a critical review

  • Review Article
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From Nature Reviews Microbiology

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Key Points

  • This review focuses on the techniques used to analyse plasmid transfer and to study the extent of horizontal gene transfer (HGT) in the environment.

  • Typically, direct evidence of in situ plasmid transfer in natural environments was obtained using plasmid-encoded phenotypes such as antibiotic resistance. As yet, there is no agreed consensus on the best system to report the extent of plasmid transfer and so it is difficult to compare results from different studies; in this review, the transconjugant to donor ratio (T/D) is used.

  • The main problems associated with traditional methods of analysis are identified: culture-based techniques cannot distinguish between an increased number of transfer events and post-transfer selection, and these methods produce a population-averaged measure of gene transfer and therefore cannot provide an insight into the spatial extent of HGT, especially within microcolonies and biofilms. The extent of gene transfer in the environment might therefore have been underestimated.

  • New methods for in situ analysis include the use of reporter genes — such as gfp (green fluorescent protein), either in a single or dual labelling assay in conjunction with fluorescence analysis — which can be used to assess both the extent of HGT and plasmid host range. Although this technique has been used successfully, it should be noted that not all transconjugant bacteria can be detected using reported genes, as some transconjugants might not efficiently transcribe the reporter gene, and codon usage can hinder translation of reporter-gene mRNA in certain bacteria.

  • To date, studies of the extent of plasmid transfer in situ have not only been able to identify environmental factors that influence the frequency of conjugal gene transfer, they have also identified certain environmental hot spots for gene transfer, such as biofilms, and additional studies have shown that the spatial structure or architecture of the biofilm has a decisive role in gene transfer.

  • Mathematical models are also used to analyse the frequency of plasmid transfer. Although many of the currently available models are of limited value as they are based on an assumption of a completely mixed, homogeneous environment with population-averaged behaviour, recent useful developments include individual-based models, which model a population or community by describing the actions and properties of the individuals comprising this population or community. If IbMs can be developed into individual-based conjugal models, this could facilitate the interpretation of experimental observations on the role of plasmid transfer by providing a quantitative and predictive framework for understanding bacterial-community response and adaptation.

Abstract

This review deals with the prospective, experimental documentation of horizontal gene transfer (HGT) and its role in real-time, local adaptation. We have focused on plasmids and their function as an accessory and/or adaptive gene pool. Studies of the extent of HGT in natural environments have identified certain hot spots, and many of these involve biofilms. Biofilms are uniquely suited for HGT, as they sustain high bacterial density and metabolic activity, even in the harshest environments. Single-cell detection of donor, recipient and transconjugant bacteria in various natural environments, combined with individual-based mathematical models, has provided a new platform for HGT studies.

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Figure 1: A schematic outline of the transfer reporter-gene approach.
Figure 2: Detection of the host range of horizontal gene transfer (HGT) without cultivation.
Figure 3: Horizontal gene transfer (HGT) in the phyllosphere.
Figure 4: Horizontal gene transfer in biofilms.

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Acknowledgements

This research was partly supported by funding of Dr S.J. Sørensen and Dr N. Kroer by the Natural and Accelerated Bioremediation Research (NABIR) programme, Biological and Environmental Research (BER), US Department of Energy.

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Authors and Affiliations

  1. Department of Microbiology, Institute of Biology, University of Copenhagen, Sølvgade 83H, Copenhagen K, 1307, Denmark

    Søren J. Sørensen & Lars H. Hansen

  2. Natural Environment Research Council,Centre for Ecology and Hydrology, Mansfield Road, Oxford, OX1 3SR, UK

    Mark Bailey

  3. Department of Environmental Chemistry and Microbiology, National Environmental Research Institute, Frederiksborgvej 399, Roskilde, DK-4000, Denmark

    Niels Kroer

  4. Department of Civil and Environmental Engineering, One Shields Avenue, University of California, Davis, 95616, California, USA

    Stefan Wuertz

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Correspondence to Søren J. Sørensen.

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Glossary

PATHOGENICITY ISLANDS

A contiguous block of genes acquired by horizontal transfer in which at least a subset of the genes code for virulence factors.

TRANSFORMATION

The uptake and incorporation of exogenous, 'naked' DNA directly from the environment.

TRANSDUCTION

The horizontal transfer of DNA mediated by bacteriophage.

CONJUGATION

The transfer of DNA between bacterial cells after cell–cell contact. Conjugation is mediated by mobile genetic elements (usually plasmids or transposons) and is unidirectional and conservative (a copy of the DNA remains in the donor strain)

TYPE IV SECRETION SYSTEM

A syringe-like proteinaceous machinery that can transport bacterial protein or DNA effector molecules directly into a eukaryotic cell.

TYPE II PROTEIN-EXPORT SYSTEMS

The type II protein-export system or secreton allows the energy-dependent secretion of specific proteins from the periplasm of Gram-negative bacteria.

TRANSCONJUGANTS

Bacterial recipient cells that have recieved a plasmid by the process of conjugation as indicated by molecular, phenotypic or microscopic analysis.

RHIZOSPHERE

The zone directly surrounding the roots of plants.

PHYLLOPLANE

The micro-environment on the leaf surface of plants.

VIABLE BUT NON-CULTURABLE

A hypothesis that assumes a physiological state of normally culturable bacteria in which they no longer grow on conventional media but remain intact and retain viability.

EPIFLUORESCENCE MICROSCOPY

A form of light microscopy that involves the detection of primary fluorescence or of specimens stained with fluorescent dyes.

MICROCOSM EXPERIMENTS

Experiments in scaled-down replicas of natural environments.

PHYTOSPHERE

All plant-associated environments, for example, rhizosphere or phylloplane.

HYPOCOTYL

The area of the plant-embryo axis below the area where cotyledons are attached that forms the primary root of a seedling.

EPILITHON

Biofilms attached to rocks in rivers and streams.

STOMATA

Pores on the underside of leaves, which enable gas exchanges. They can be either opened or closed.

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Sørensen, S., Bailey, M., Hansen, L. et al. Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3, 700–710 (2005). https://doi.org/10.1038/nrmicro1232

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  • DOI: https://doi.org/10.1038/nrmicro1232

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