Genome Sequences of ThreeAgrobacteriumBiovars Help Elucidate the Evolution of Multichromosome Genomes in Bacteria

Abstract

The family Rhizobiaceae contains plant-associated bacteria with critical roles in ecology and agriculture. Within this family, many Rhizobium and Sinorhizobium strains are nitrogen-fixing plant mutualists, while many strains designated as Agrobacterium are plant pathogens. These contrasting lifestyles are primarily dependent on the transmissible plasmids each strain harbors. Members of the Rhizobiaceae also have diverse genome architectures that include single chromosomes, multiple chromosomes, and plasmids of various sizes. Agrobacterium strains have been divided into three biovars, based on physiological and biochemical properties. The genome of a biovar I strain, A. tumefaciens C58, has been previously sequenced. In this study, the genomes of the biovar II strain A. radiobacter K84, a commercially available biological control strain that inhibits certain pathogenic agrobacteria, and the biovar III strain A. vitis S4, a narrow-host-range strain that infects grapes and invokes a hypersensitive response on nonhost plants, were fully sequenced and annotated. Comparison with other sequenced members of the Alphaproteobacteria provides new data on the evolution of multipartite bacterial genomes. Primary chromosomes show extensive conservation of both gene content and order. In contrast, secondary chromosomes share smaller percentages of genes, and conserved gene order is restricted to short blocks. We propose that secondary chromosomes originated from an ancestral plasmid to which genes have been transferred from a progenitor primary chromosome. Similar patterns are observed in select Beta-and Gammaproteobacteria species. Together, these results define the evolution of chromosome architecture and gene content among the Rhizobiaceae and support a generalized mechanism for second-chromosome formation among bacteria.The family Rhizobiaceae (order Rhizobiales) of the Alphaproteobacteria includes the plant pathogens of the genus Agrobacterium and the nitrogen-fixing plant mutualists of the genera Rhizobium and Sinorhizobium. Members house single and multiple chromosome arrangements, linear replicons, and plasmids of various sizes. Genes of pathogenicity, mutualism, and other symbiotic properties are primarily encoded on large transmissible plasmids. Given the promiscuous nature of these elements, different genomic lineages within the Rhizobiaceae exhibit a variety of symbiotic phenotypes that range from pathogenesis to nitrogen-fixing mutualism.Agrobacterium taxonomy and phylogeny display a marked disparity. Empirically, organisms of the genus Agrobacterium are grouped into five species based on the disease phenotype associated with the resident disease-inducing plasmid: A. tumefaciens causes crown gall on dicotyledonous plants, including stone fruit and nut trees; A. rubi causes crown gall on raspberries; A. vitis causes gall formation that is limited to grapes; A. rhizogenes causes hairy root disease; and A. radiobacter is avirulent. An alternative classification scheme

What traits are carried on mobile genetic elements, and why?

“…In fact, reduced costs of plasmid carriage may have been the driving force for the creation of secondary chromosomes in many bacteria. Such chromosomes often have plasmid-like features and are ubiquitous in some bacterial clades (Egan and Waldor, 2003;Slater et al, 2009). Accordingly, recent work shows that the very largest plasmids have lost mobility and acquired essential genes (Smillie et al, in preparation).…”

Evolutionary origins and diversification of proteobacterial mutualists

“…P reversals are well supported in the consensus ASR (see the electronic supplementary material, S1) and appear to be driven by HGT events; the plant pathogen taxa Pseudomonas syringae and Agrobacterium spp. have probably evolved from mutualists via HGT of Type-III secretion systems and other key virulence loci [33,34]. By contrast, M !…”

Neo-formation of chromosomes in bacteria

“…Only the largest, primary, ER is expected to be a bona fide chromosome, i.e., homologous to the single chromosome constituting the stable genome of most bacteria. The additional, secondary, ERs (SERs) are proposed to derive from accessory replicons (plasmids 5,6 ) that were acquired by a mono-chromosome progenitor bacterium and stabilized through the transfer from the chromosome of genes essential to the cell viability 7,8 . The existence of plasmid-like replication and partition systems in SERs 7,9-14 as well as experimental results 15 support this view.…”