Structure and evolution of NGRRS-1, a complex, repeated element in the genome of Rhizobium sp. strain NGR234

Abstract

Much of the remarkable ability of Rhizobium sp. strain NGR234 to nodulate at least 110 genera of legumes, as well as the nonlegume Parasponia andersonii, stems from the more than 80 different Nod factors it secretes. Except for nodE, nodG, and nodPQ, which are on the chromosome, most Nod factor biosynthesis genes are dispersed over the 536,165-bp symbiotic plasmid, pNGR234a. Mosaic sequences and insertion sequences (ISs) comprise 18% of pNGR234a. Many of them are clustered, and these IS islands divide the replicon into large blocks of functionally related genes. At 6 kb, NGRRS-1 is a striking example: there is one copy on pNGR234a and three others on the chromosome. DNA sequence comparisons of two NGRRS-1 elements identified three types of IS, NGRIS-2, NGRIS-4, and NGRIS-10. Here we show that all four copies of NGRRS-1 probably originated from transposition of NGRIS-4 into a more ancient IS-like sequence, NGRIS-10. Remarkably, all nine copies of NGRIS-4 have transposed into other ISs. It is unclear whether the accumulation of potentially mutagenic sequences in large clusters is due to the nature of the IS involved or to some selection process. Nevertheless, a direct consequence of the preferential targeting of transposons into such IS islands is to minimize the likelihood of disrupting vital functions.

The complete genome sequence ofMycobacterium aviumsubspeciesparatuberculosis

“…2); this is a Ϸ1,400-bp repeated insertion sequence that was first described in the Mtb genome (24,25). It is believed that insertion sequences preferentially integrate within intergenic regions so as to avoid the disruption of essential genes (26). Consistent with this hypothesis, the majority of the IS elements found in K-10 appear to be clustered within intergenic regions.…”

“…A total of 52.5% of the genes are transcribed with the same polarity as that of DNA replication, a fraction that is slightly lower than the 59% observed in Mtb. Interestingly, there appears to be a higher bias toward transcription in the same polarity as replication in some other organisms (for e.g., 75% in Bacillus subtilis) (26,27). Although it is tempting to speculate that this bias may, in part, contribute to the slow growth in Mtb and the even slower growth in Map, it is important to note that only 55% of Escherichia coli genes are transcribed in the same polarity as replication, suggesting that gene location in relation to the origin of replication cannot fully explain Map's slow growth in laboratory culture (28).…”

Dynamics of Genome Architecture in Rhizobium sp. Strain NGR234

“…One of them consists of a complex repeated element, NGRRS-1 of 6 kb (16). Initially, the presence of one copy of NGRRS-1 in pNGR234a and three copies in the chromosome was reported (16). However, after the identification of the pNGR234b replicon (2), it is now known that the latter contains two NGRRS-1 copies, whereas the chromosome bears one.…”

“…Some of them participate in intragenomic rearrangements such as DNA amplifications or deletions (3). Reiterated sequences are also present in the chromosome and in pNGR234b (16,24), suggesting that the three replicons may participate in the plasticity of the NGR234 genome. This makes strain NGR234 a convenient model to analyze genome dynamics and its biological consequences.…”

Rhizobium sp. Strain NGR234 Possesses a Remarkable Number of Secretion Systems

“…Unlike the NGR234 chromosome, both plasmids seem prone to DNA rearrangements and include segments of up to 12 kb exclusively constituted of several layers of ISs that transposed into one another, however. ISs that range in size from 623 to 3,316 bp, were grouped into 36 families, the largest of which includes 10 copies of the NGRIS-4 transposable element (67). Of these 36 types of ISs, five families are chromosome specific, six are pNGR234a specific, and seven are pNGR234b specific.…”