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Chapter 9 : Bacteriophage-Mediated Transduction: An Engine for Change and Evolution

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Abstract:

To understand transduction, one must first understand the biology of bacterial viruses called bacteriophages. This chapter explores the mechanisms of transduction and discusses some of the evidence that it is more than a simple laboratory phenomenon. It discusses the potential of transduction to affect bacterial evolution. Bacteriophages, like all viruses, are intracellular parasites. The life cycles of bacteriophages consist of both biotic and abiotic components. There are two types of life cycles for complex viruses: (i) the lytic cycle that leads to the lysis of the host cell and production of progeny virions and (ii) the temperate cycle in which a viral genome (prophage) becomes part of the genetic component of the host cell and is replicated and passed on to daughter cells. Transduction is a bacteriophage-mediated mechanism of horizontal gene transfer among bacteria. There are two types of transduction: (i) generalized and (ii) specialized. Bacteriophages are root regulators of natural ecosystems, affecting both the flow of energy and carbon. The validity of the model of environmental transduction can be demonstrated in continuous-culture experiments. Experiments described in the chapter show that transduction is a viable source of genetic diversity in a natural bacterial gene pool. In bacterial populations, transduction can act to overcome the negative fitness imposed by certain genes that would otherwise lead to extinction of the genotype.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9

Key Concept Ranking

Genetic Elements
0.5094006
Horizontal Gene Transfer
0.43562892
Generalized Transduction
0.41625392
Specialized Transduction
0.41407457
Chromosomal DNA
0.40634748
0.5094006
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Figures

Image of FIGURE 1
FIGURE 1

Electron micrographs of various bacteriophages. (A, B, D—F) Complex bacteriophages; (C) filamentous bacteriophage. (A, B, D) Bacteriophages isolated from sewage; (C, E, F) those isolated from a freshwater lake.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 2
FIGURE 2

A Buckminster Fuller-like home in Oklahoma. The rendering in panel ? emphasizes the geometry of the icosidodecahedron making up the building's roof.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 3
FIGURE 3

A complex bacteriophage. The various parts of the capsid arc identified. The nucleic acid (double-stranded DNA in all known cases) is contained in the head. Contact with the host bacterium is initially made with the tail fibers. Irreversible contact is made at the base plate and the DNA is “injected” into the cell through the tail that often contracts. Compare this diagram with the electron micrographs in Fig. 1 .

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 4
FIGURE 4

The life cycles of a complex bacteriophage. (A) Lytic life cycle that leads to the production of progeny phages; (B) temperate life cycle in which a prophage is established in the host cell producing a bacterium referred to as a lysogen. The prophage is not transcribed (indicated by the Xs) but replicates with the host cell's genome and is partitioned into its daughter cells. Some prophages are integrated into the host genome (see Fig. 6 ) while other types are carried as plasmids. Note: The host genome is not illustrated in this figure.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 5
FIGURE 5

Attachment of a bacteriophage particle to the host-cell receptor. (A) Diagram; (B) electron micrograph of phage UT1 infecting

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 6
FIGURE 6

Diagram of the “activation” of an integrated prophage into the host genome. When the prophage is “activated” to the lytic cycle by some environmental stressor (perhaps solar UV radiation), it disintegrates as the first step in producing progeny bacteriophages. Sometimes the disintegration is not precise and a “transducing sequence” containing part of the host genome is incorporated. This gene sequence (here “A”) is then found in all the progeny specialized transducing particles.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 7
FIGURE 7

Production of generalized transducing particles.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 8
FIGURE 8

A model of the consequences of transduction of genetic markers from a bacterium introduced into an environmental bacterial community. Here the transduction of plasmid DNA is illustrated for simplicity, but chromosomal genes could enter the community's gene pool in a like manner. The following sequence of events is envisioned. (A) Environmental stressors lead to the “activation” or “induction” of a prophage from an environmental lysogen ( ), resulting in the production and release of bacteriophage virions ( ). (B) One of these virions then infects an introduced bacterium containing a plasmid (P) and propagates lyrically in the cell (C) releasing virions and transducing particles ( ). (D) Transducing particles produced in this way are absorbed to members of the resident environmental bacterial community. Following absorption of the plasmid DNA from the transducing particle, the plasmid is established in the environmental lysogen (E) and enters the environmental gene pool that can be transferred by any of a number of horizontal gene-transfer mechanisms (see chapters 7 through 10). By virtue of being a lysogen, the transductant is immune to subsequent lytic infection by virions of the transducing virus. This helps to ensure the survival of the transductant in the environmental community.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 9
FIGURE 9

A chemostat used for continuous cultivation of bacteria allowing studies of long-term evolution of populations of bacteria. Chemostats are used for many experiments in microbiology and in industry to produce bacteria in quantity.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 10
FIGURE 10

(A) Results of a control chemostat experiment in which gene transfer by transduction was not allowed to take place. CFU, colony-forrning-units. (B) The mock transductant was lost for the community due to a slight negative fitness coefficient. The change in mock transductants as a function of generation is plotted (dMT/dg). (Adapted from with permission.)

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 11
FIGURE 11

Electron micrograph of bacteriophage F116 of . F116 is a generalized transducing phage with a genome of 85.5 kbp with a G + C content of 61 %. This is approximately 2.5% of the genome and almost exactly the same size as the Tra, Mob plasmid Rms l49. Its head is 65 nm in diameter, and its tail has a 12-nm diameter and is 80 nm long.

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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Image of FIGURE 12
FIGURE 12

(A) Results of a chemostat experiment in which transduction was allowed to occur. CFU, colony-forming units. (B) T h e transductants increased in frequency in the populations even though they have a slight negative fitness coefficient. T h e change in transductants as a function of generation is plotted (dT/dg). (Adapted from with permission.)

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9
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References

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1. Bratbak, G.,, M. Heldal,, S. Norland,, and T. F. Thingstad. 1990. Viruses as partners in spring bloom microbial trophodynamics. Appl. Environ. Microbiol. 56:14001405.
2. Miller, R. V. 2001. Environmental bacteriophage-host interactions: factors contribution to natural transduction. Antonie van Leeuwenhoek 79:141147.
3. Miller, R. V.,, and S. A. Ripp,. 2002. Pseudo-lysogeny: a bacteriophage strategy for increasing longevity in situ, p. 8194. In M. Syvanen, and C. Kado (ed.), Horizontal Gene Transfer, 2nd ed. Academic Press, San Diego, Calif.
4. Miller, R. V.,, S. Ripp,, J. Replicon,, O. A. Ogunseitan,, and T. A. Kokjohn,. 1992. Virus-mediated gene transfer in freshwater environments, p. 5062. In M. J. Gauthier (ed.), Gene Transfers and Environment. Springer-Verlag, Berlin, Germany.
5. Proctor, L. M.,, A. Okubo,, and J. A. Fuhrman. 1993. Calibrating estimates of phage-induced mortality in marine bacteria: ultrastructural studies of marine bacteriophage development from one-step growth experiments. Microb. Ecol. 25:161182.
6. Replicon, J.,, A. Frankfater,, and R. V. Miller. 1995. A continuous culture model to examine factors that affect transduction among Pseudomonas aeruginosa strains in freshwater environments. Appl. Environ. Microbiol. 61:33593366.
7. Ripp, S.,, and R. V. Miller. 1997. The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment. Microbiology 143:20652070.
8. Ripp, S.,, O. A. Ogunseitan,, and R. V. Miller. 1994. Transduction of a freshwater microbial community by a new Pseudomonas aeruginosa generalized transducing phage, UT1. Mol. Ecol. 3:121126.
9. Saye, D. J.,, O. A. Ogunseitan,, G. S. Sayler,, and R. V. Miller. 1990. Transduction of linked chromosomal genes between Pseudomonas aeruginosa during incubation in situ in a freshwater habitat. Appl. Environ. Microbiol. 56:140145.
10. Saye, D. J.,, O. Ogunseitan,, G. S. Sayler,, and R. V. Miller. 1987. Potential for transduction of plasmids in a natural freshwater environment: effect of plasmid donor concentration and a natural microbial community on transduction in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 53: 987995.
11. Schicklmaier, P.,, and H. Schmieger. 1995. Frequency of generalized transducing phages in natural isolates of the Salmonella typhimurium complex. Appl. Environ. Microbiol. 61:16371640.
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13. Waldor, M. K.,, and J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:19101914.
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18. Kokjohn, T. A., 1989. Transduction; mechanism and potential for gene transfer in the environment, p. 7398. In S. B. Levy, and R. V. Miller (ed.), Gene Transfer in the Environment. McGraw-Hill Publishing Co., New York, N.Y.
19. Masters, M., 1996. Generalized transduction, p. 24212441. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella Cellular and Molecular Biology. American Society for Microbiology, Washington, D.C.
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23. Saye, D.J.,, and R. V. Miller,. 1989. The aquatic environment: Consideration of horizontal gene transmission in a diversified habitat, p. 223259. In S. B. Levy, and R. V. Miller (ed.), Gene Transfer in the Environment. McGraw-Hill, New York, N.Y.
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Tables

Generic image for table
TABLE 1

Strains used in continuous-culture experiments

Citation: Miller R. 2004. Bacteriophage-Mediated Transduction: An Engine for Change and Evolution, p 144-157. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch9

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