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The Ecology and Evolution of Microbial Defense Systems in

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  • Authors: Margaret A. Riley1, John E. Wertz2, and Carla Goldstone3
  • Editor: David A. Rasko4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511; 2: Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511; 3: Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511; 4: University of Maryland, School of Medicine, Baltimore, MD
  • Received 23 July 2003 Accepted 10 October 2003 Published 27 February 2004
  • Address correspondence to Margaret A. Riley mmargaret.riley@yale.edu
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  • Abstract:

    Microbes produce an extraordinary array of microbial defense systems. These include broad-spectrum classical antibiotics critical to human health concerns; metabolic by-products, such as the lactic acids produced by lactobacilli; lytic agents, such as lysozymes found in many foods; and numerous types of protein exotoxins and bacteriocins. The abundance and diversity of this biological arsenal are clear. Lactic acid production is a defining trait of lactic acid bacteria. Bacteriocins are found in almost every bacterial species examined to date, and within a species, tens or even hundreds of different kinds of bacteriocins are produced. Halobacteria universally produce their own version of bacteriocins, the halocins. Streptomycetes commonly produce broad-spectrum antibiotics. It is clear that microbes invest considerable energy in the production and elaboration of antimicrobial mechanisms. What is less clear is how such diversity arose and what roles these biological weapons play in microbial communities. One family of microbial defense systems, the bacteriocins, has served as a model for exploring evolutionary and ecological questions. In this review, current knowledge of how the extraordinary range of bacteriocin diversity arose and is maintained in one species of bacteria, , is assessed and the role these toxins play in mediating microbial dynamics is discussed.

  • Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8

Key Concept Ranking

Amino Acids
0.46222213
Lactic Acid Bacteria
0.4361796
Microbial Ecology
0.41844305
Klebsiella pneumoniae
0.3548387
0.46222213

References

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19. Ferrer S, Viejo MB, Guasch JF, Enfedaque J, Regue M. 1996. Genetic evidence for an activator required for induction of colicin-like bacteriocin 28b production in Serratia marcescens by DNA-damaging agents. J Bacteriol 178:951–960.
20. Guasch J, Enfedaque J, Ferrer S, Gargallo D, Regue M. 1995. Bacteriocin 28b, a chromosomally encoded bacteriocin produced by most Serratia marcesens biotypes. Res Microbiol 146:477–483. [CrossRef]
21. Lau PCK, Parsons M, Uchimura T. 1992. Molecular evolution of E colicin plasmids with emphasis on the endonuclease types, p 353–378. In James R, Lazdunski C, and Pattus F (ed), Bacteriocins, Microcins and Lantibiotics, vol. H65. Springer-Verlag, Berlin, Germany.
22. Riley MA. 1993. Molecular mechanisms of colicin evolution. Mol Biol Evol 10:1380–1395.
23. Roos U, Harkness RE, Braun V. 1989. Assembly of colicin genes from a few DNA fragments. Nucleotide sequence of colicin D. Mol Microbiol 3:891–902. [PubMed][CrossRef]
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26. Riley MA, Tan Y, Wang J. 1994. Nucleotide polymorphism in colicin E1 and Ia plasmids from natural isolates of Escherichia coli. Proc Natl Acad Sci USA 91:11276–11280. [PubMed][CrossRef]
27. Tan Y, Riley MA. 1997. Nucleotide polymorphism in colicin E2 gene clusters: evidence for nonneutral evolution. Mol Biol Evol 14:666–673.[PubMed]
28. Gordon D, Riley MA. 1999. A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology 145:655–661. [PubMed][CrossRef]
29. Tan Y, Riley MA. 1996. Rapid invasion by colicinogenic Escherichia coli with novel immunity functions. Microbiology 142:2175–2180. [PubMed][CrossRef]
30. Tan Y, Riley MA. 1997. Positive selection and recombination: major molecular mechanisms in colicin diversification. Trends Ecol Evol 12:348–351. [CrossRef]
31. Riley MA, Pinou T, Wertz JE, Tan Y, Valletta CM. 2001. Molecular characterization of the klebicin B plasmid of Klebsiella pneumoniae. Plasmid 45:209–221. [PubMed][CrossRef]
32. Pilsl H, Braun V. 1995. Strong function-related homology between the pore-forming colicins K and 5. J Bacteriol 177:6973–6977.[PubMed]
33. Sano Y, Matsui H, Kobayashi M, Kageyama M. 1993. Molecular structures and functions of pyocins S1 and S2 in Pseudomonas aeruginosa. J Bacteriol 175:2907–2916.[PubMed]
34. Riley MA, Wertz JE. 2002. Bacteriocins: evolution, ecology and application. Annu Rev Microbiol 56:117–137. [PubMed][CrossRef]
35. Riley MA. 1993. Positive selection for colicin diversity in bacteria. Mol Biol Evol 10:1048–1059.[PubMed]
36. Riley MA, Cadavid L, Collett MS, Neely MN, Adams MD, Phillips CM, Neel JV, Friedman JD. 2000. The newly characterized colicin Y provides evidence of positive selection in pore-former colicin diversification. Microbiology 146:1671–1677.[PubMed]
37. Smajs D, Pilsl H, Braun V. 1997. Colicin U, a novel colicin produced by Shigella boydii. J Bacteriol 179:4919–4928.[PubMed]
38. Smajs D, Weinstock G. 2001. Genetic organization of plasmid ColJs, encoding colicin Js activity, immunity, and release genes. J Bacteriol 183:3949–3957. [PubMed][CrossRef]
39. Wu S, Dornbusch K, Kronvall G, Norgren M. 1999. Characterization and nucleotide sequence of a Klebsiella oxytoca cryptic plasmid encoding a CMY-type β-lactamase: confirmation that the plasmid-mediated cephamycinase originated from the Citrobacter freundii Amp C β-lactamase. Antimicrob Agents Chemother 43:1350–1357.[PubMed]
40. Dery KJ, Chavideh R, Waters V, Chamorro R, Tolmasky L, Tolmasky M. 1997. Characterization of the replication and mobilization regions of the multiresistance Klebsiella pneumoniae plasmid pJHCMW1. Plasmid 38:97–105. [PubMed][CrossRef]
41. Hu P, Elliott J, McCready P, Skowronski E, Garnes J, Kobayashi A, Brubaker RR, Garcia E. 1998. Structural organization of virulence-associated plasmids of Yersinia pestis. J Bacteriol 180:5192–5202.[PubMed]
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43. Craven JA, Miniats OP, Barnum DA. 1971. Role of colicins in antagonism between strains of Escherichia coli in dual-infected gnotobiotic pigs. Am J Vet Res 32:1775–1779.[PubMed]
44. Feldgarden M, Golden S, Wilson H, Riley MA. 1995. Can phage defense maintain colicin plasmids in Escherichia coli? J Microbiol 141:2977–2984. [CrossRef]
45. Freter R. 1983. Mechanisms that control the microflora in the large intestine, p 33–55. In Hentges DJ (ed), Human Intestinal Microflora in Health and Disease. Academic Press, New York, N.Y.
46. Hardy KG. 1975. Colicinogeny and related phenomena. Bacteriol Rev 39:464–515.[PubMed]
47. Ikari NS, Kenta DM, Young VM. 1969. Interaction in the germfree mouse intestine of colicinogenic and colicin-sensitive microorganisms. Proc Soc Exp Med 130:1280–1284.
48. Kelstrup J, Gibbons RJ. 1969. Inactivation of bacteriocins in the intestinal and oral cavity. J Bacteriol 99:888–890.[PubMed]
49. Wilson KH. 1997. Biota of the Human Gastrointestinal Tract, vol. 2. Chapman and Hall, New York, N.Y.
50. Chao L, Levin BR. 1981. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci USA 78:6324–6328. [PubMed][CrossRef]
51. Czárán TL, Hoekstra RF, Pagie L. 2002. Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci USA 99:786–790. [PubMed][CrossRef]
52. Kerr B, Riley MA, Feldman M, Bohannan B. 2002. Local dispersal and interaction promote coexistence in a real life game of rock-paper-scissors. Nature 418:171–174. [PubMed][CrossRef]
53. Feldgarden M, Riley MA. 1998. The phenotypic and fitness effects of colicin resistance in Escherichia coli K-12. Evolution 53:1019–1027. [CrossRef]
54. Lenski RR, Riley MA. 2002. Chemical warfare from an ecological perspective. Proc Natl Acad Sci USA 99:556–558. [PubMed][CrossRef]
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57. Riley MA, Goldstone CM, Wertz JE. 2003. A phylogenetic approach to assessing the targets of microbial warfare. J Evol Biol 16:690–697. [CrossRef]
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2004-02-27
2017-08-21

Abstract:

Microbes produce an extraordinary array of microbial defense systems. These include broad-spectrum classical antibiotics critical to human health concerns; metabolic by-products, such as the lactic acids produced by lactobacilli; lytic agents, such as lysozymes found in many foods; and numerous types of protein exotoxins and bacteriocins. The abundance and diversity of this biological arsenal are clear. Lactic acid production is a defining trait of lactic acid bacteria. Bacteriocins are found in almost every bacterial species examined to date, and within a species, tens or even hundreds of different kinds of bacteriocins are produced. Halobacteria universally produce their own version of bacteriocins, the halocins. Streptomycetes commonly produce broad-spectrum antibiotics. It is clear that microbes invest considerable energy in the production and elaboration of antimicrobial mechanisms. What is less clear is how such diversity arose and what roles these biological weapons play in microbial communities. One family of microbial defense systems, the bacteriocins, has served as a model for exploring evolutionary and ecological questions. In this review, current knowledge of how the extraordinary range of bacteriocin diversity arose and is maintained in one species of bacteria, , is assessed and the role these toxins play in mediating microbial dynamics is discussed.

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Figures

Image of Figure 1
Figure 1

The values below each comparison indicate the sequence identity for the region indicated. The colicin proteins are not drawn to scale.

Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8
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Image of Figure 2
Figure 2

The chimeric nature of the pKlebB plasmid sequence is indicated by different shading patterns. The key shows regions of sequence similarity to other bacteriocin gene clusters and plasmids. pKlebB illustrates a pattern typical of other bacteriocin-encoding plasmids in which sequences encoding plasmid functions are similar to sequences found in other plasmids segregating in the host species, whereas those sequences composing and flanking the bacteriocin gene cluster show similarity to bacteriocin sequences from other species.

Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8
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Image of Figure 3
Figure 3

Most of the divergence between colicins occurs in the immunity region of the gene cluster (composed of the immunity gene and the immunity binding region of the colicin gene).

Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8
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Image of Figure 4
Figure 4

Calculations were performed on pairs of aligned nucleotide sequences using a sliding window of 40 bp and a step size of 1 base. Gaps in aligned sequences were deleted from both sequences; there were no ambiguous bases. % Identity, percentage of nucleotide matches per total number of sites compared; ds, percentage of synonymous substitutions per synonymous sites; dn, percentage of nonsynonymous substitutions per nonsynonymous sites. The values are not corrected for multiple substitutions per site. The axis is the number of the first nucleotide in the comparison window.

Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8
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Image of Figure 5
Figure 5

Over 400 strains were isolated from two populations of feral mice in Australia over a period of 7 months. The isolates were scored for colicin production and resistance. (a) Colicin production is abundant, with just under 50% of the strains producing eight distinct colicin types. Col , nonproducer strains. (b) The majority of isolates are resistant to most co-occurring colicins. (c) A small proportion of the population is sensitive to co-occurring colicins.

Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8
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Image of Figure 6
Figure 6

The killing spectrum of each class of bacteriocins was cross-referenced with a phylogenetic tree of the enteric species they were screened against. The heights of the solid boxes are proportional to the percentage of strains sensitive to each class of bacteriocin. Bacteriocins were screened against 40 natural isolates from each enteric species. The molecular phylogeny of a subset of enteric bacteria is based on a composite of five housekeeping genes (, , , , and ) and 16S ribosomal sequences. The tree is rooted using as an outgroup. Abbreviations: KO, ; KP, ; EB, ; CF, ; EC, ; SM, ; HA, , VC, .

Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8
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Tables

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Table 1

Chemical warfare among microbes as a nontransitive three-way game similar to the RPS game

Citation: Riley M, Wertz J, Goldstone C. 2004. The Ecology and Evolution of Microbial Defense Systems in , EcoSal Plus 2004; doi:10.1128/ecosalplus.6.4.8

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