With Other Replicons and Evolutionary Significance

Keith F. Chater1 (K) • Haruyasu Kinashi2

:John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, UK [email protected]

2Department of Molecular Biotechnology, Hiroshima University, 739-8530 Higashi-Hiroshima, Japan

1 Introduction: Early Studies of Plasmids 2

2 Exploring the Genetics of Other Bacteria:

The Dawn of Streptomyces Genetics 3

3 Streptomyces coelicolor A3(2) Has a Plasmid Fertility Factor, SCP1, Capable of Integration into the Chromosome to Give High-Fertility Variants 5

4 SCP1 is a Very Large Linear Molecule, and Linear Plasmids are Widespread Among Streptomycetes 7

5 Interactions of Linear Plasmids with the Chromosome: Physical Analysis 12

5.1 Integration of SCP1 Within the Chromosome 12

5.2 Single Crossover Recombination Between a Linear Plasmid and the Chromosome to Generate Molecules with Heterologous Ends ... 14

6 Linear Plasmids and Antibiotic Production 16

6.1 Genes for Methylenomycin Production 18

6.2 pSLA2-L of Streptomyces rochei:

A Plasmid Densely Packed with Genes for Secondary Metabolism 19

7 Linear Plasmids and Evolution 20

7.1 Evolutionarily and Adaptively Significant Genes

Carried by Linear Plasmids 21

7.2 Possible Role of Linear Plasmids in the Dissemination of TTA-Containing Genes Subject to the Influence of the Developmental Gene bldA 23

7.3 Co-evolution of Streptomycetes and Their Linear Replicons 23

References 25

Abstract Unusually among bacteria, streptomycetes possess linear chromosomes, and many of them also carry linear plasmids (circular plasmids are also found). The linear plasmids range in size from tens to hundreds of kilobases. The most studied is SCP1, discovered as a sex factor in the model organism Streptomyces coelicolor A3(2). A variety of co-integrates and hybrids have been found between SCP1 and the host chromosome, which can greatly increase the likelihood of chromosomal transfer. Several examples of the exchange of ends between linear plasmids and linear chromosomes have been documented. These can sometimes bring about the mobilisation of chromosomal genes for antibiotic biosynthesis. Some very large linear plasmids themselves carry genes for the biosynthesis of bioactive small molecules, including antibiotics. For example, such genes occupy about two thirds of the plasmid pSLA2-L. In another case, almost identical gene sets for methylenomycin biosynthesis are present both on the linear plasmid, SCP1, and on a quite different circular plasmid, pSV1, in a related streptomycete. It appears that linear plasmids have played key roles in the architecture, accessory gene content and rapid evolution of Streptomyces chromosomes. They may have permitted the diversification and spread of pathways for secondary metabolism, and the evolution of some Streptomyces-specific families of paralogous genes. They may also have been the source of most of the genes that, because of their possession of the rare TTA codon, are dependent for expression on the cognate tRNA specified by bldA, a gene whose deletion has wide-ranging effects on morphological differentiation and secondary metabolism.

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