Linear Plasmids and Evolution

It is likely that the linearity of Streptomyces chromosomes originally resulted from Campbell-type recombination between a circular genome and a linear plasmid (Volff and Altenbuchner 2000; Chen et al. 2002). Although it has been suggested that this occurred many times independently within the Streptomyces lineage (Chen et al. 2002), it is also attractive to consider the case for a unitary linearisation event at the birth of the genus. On the assumption that diverse linear plasmids continued to arise, their ends would have readily been moved into and between the linear chromosomes of streptomycetes, both early and more recently in their evolution, as illustrated by the phenomenology described in this chapter (see also Hopwood 2006). This would have accelerated the rate of diversification of Streptomyces genomes at a critical point in their early evolution which, it has been argued, took place when a vast new ecological niche first became available on the earth through colonisation of the land by green plants about half a billion years ago (Chater and Chandra 2006). In this final section, we consider linear plasmids in the context of the evolution of their hosts.

Evolutionarily and Adaptively Significant Genes Carried by Linear Plasmids

As is often the case for large plasmids, both circular and linear, a relatively high proportion of SCP1 genes (57%) show no significant database matches, and a further 20% resemble database entries of unknown function. The equivalent numbers for the host chromosome are 23 and 30%. This reinforces the idea that plasmids are an important route by which new genes enter their hosts, though it has been argued elsewhere that fundamentally novel genes probably arise more often in bacteriophages (Chater and Chandra 2006). It is interesting to note that one of the linear plasmids, SCP1, is a vehicle for members of several families of regulatory genes that are particularly important in streptomycetes. One such family is the arpA-like genes referred to above, representatives of which (mmfR and mmyR) function in methylenomycin production. Another comprises genes for ECF (extracytoplasmic function) sigma factors, which are particularly abundant in streptomycetes (e.g. nearly 50 each in S. coelicolor and S. avermitilis, compared to one in E. coli K-12; Bentley et al. 2002; Ikeda et al. 2003): three of these are present on SCP1. The plasmid also carries three genes belonging to the whiB-like family (wbl genes; Soliveri et al. 2000). Such wbl genes are confined to actinomycetes, where they are abundant and play important roles in cell division/development and antibiotic resistance (Chater and Chandra 2006). (Remarkably, one of the wbl genes (wblP; SCP1.161c) encodes a Wbl-ECF sigma factor fusion protein, reinforcing evidence that Wbl proteins directly interact with sigma factors (Steyn et al. 2002).) SCP1 also contains a representative of the family of abaA-like clusters found only in streptomycetes, in which there are many such gene sets. In S. coelicolor, the prototype of these clusters, abaA, is involved in the regulation of antibiotic production (Fernandez-Moreno et al. 1992), while another includes the developmental gene whiJ (Gehring et al. 2000). The SCP1 abaA-related par-alogues (SCP1.58c-60 and 295-293c: the cluster is present in both TIRs) are co-transcribed with the sapCDE genes for spore-associated proteins. Thus, SCP1 may be representative of the mechanism of expansion and spread of these regulatory gene families, so important in the contexts of secondary metabolism, differentiation and cellular homeostasis/stress responses. Frequent lateral transfer of such genes among streptomycetes is also indicated by the fact that, in each species, a set of universally conserved versions of all these families is augmented by species-specific chromosomal versions, often located in the poorly conserved TIR regions.

Other large linear plasmids are much less rich in such families of regulatory genes, but may help to bring about other aspects of genome evolution. As discussed in the preceding section, pSLA2-L illustrates the possibility that linear plasmids help to bring sets of antibiotic production genes together as a prelude to the selection of synergistic cooperations, while the movement of genes for oxytetracycline biosynthesis between the S. rimosus chromosome and linear plasmid pPZG101 illustrates how readily such chromosomal gene sets might be mobilised to other streptomycetes. Such recombinational exchanges are likely to be helped by the frequent occurrence of transposable DNA in some (but not all) linear plasmids (Fig. 8) and chromosome ends. The occurrence of transposable elements near chromosome ends may well reflect exchanges with the ends of linear plasmids.

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