Conservation of Gene Order and Content in the Circular Chromosomes of ‘Candidatus Liberibacter asiaticus’ and Other Rhizobiales

PLOS ONE, Dec 2019

‘Ca. Liberibacter asiaticus,’ an insect-vectored, obligate intracellular bacterium associated with citrus-greening disease, also called “HLB," is a member of the Rhizobiales along with nitrogen-fixing microsymbionts Sinorhizobium meliloti and Bradyrhizobium japonicum, plant pathogen Agrobacterium tumefaciens and facultative intracellular mammalian pathogen Bartonella henselae. Comparative analyses of their circular chromosomes identified 514 orthologous genes shared among all five species. Shared among all five species are 50 identical blocks of microsyntenous orthologous genes (MOGs), containing a total of 283 genes. While retaining highly conserved genomic blocks of microsynteny, divergent evolution, horizontal gene transfer and niche specialization have disrupted macrosynteny among the five circular chromosomes compared. Highly conserved microsyntenous gene clusters help define the Rhizobiales, an order previously defined by 16S RNA gene similarity and herein represented by the three families: Bartonellaceae, Bradyrhizobiaceae and Rhizobiaceae. Genes without orthologs in the other four species help define individual species. The circular chromosomes of each of the five Rhizobiales species examined had genes lacking orthologs in the other four species. For example, 63 proteins are encoded by genes of ‘Ca. Liberibacter asiaticus’ not shared with other members of the Rhizobiales. Of these 63 proteins, 17 have predicted functions related to DNA replication or RNA transcription, and some of these may have roles related to low genomic GC content. An additional 17 proteins have predicted functions relevant to cellular processes, particularly modifications of the cell surface. Seventeen unshared proteins have specific metabolic functions including a pathway to synthesize cholesterol encoded by a seven-gene operon. The remaining 12 proteins encoded by ‘Ca. Liberibacter asiaticus’ genes not shared with other Rhizobiales are of bacteriophage origin. ‘Ca. Liberibacter asiaticus’ shares 11 genes with only Sinorhizobium meliloti and 12 genes are shared with only Bartonella henselae.

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Conservation of Gene Order and Content in the Circular Chromosomes of ‘Candidatus Liberibacter asiaticus’ and Other Rhizobiales

Hartung JS (2012) Conservation of Gene Order and Content in the Circular Chromosomes of 'Candidatus Liberibacter asiaticus' and Other Rhizobiales. PLoS ONE 7(4): e34673. doi:10.1371/journal.pone.0034673 Conservation of Gene Order and Content in the Circular Chromosomes of 'Candidatus Liberibacter asiaticus' and Other Rhizobiales L. David Kuykendall 0 Jonathan Y. Shao 0 John S. Hartung 0 John Parkinson, Hospital for Sick Children, Canada 0 Molecular Plant Pathology Laboratory, Agricultural Research Service, United States Department of Agriculture , Beltsville, Maryland , United States of America 'Ca. Liberibacter asiaticus,' an insect-vectored, obligate intracellular bacterium associated with citrus-greening disease, also called ''HLB,'' is a member of the Rhizobiales along with nitrogen-fixing microsymbionts Sinorhizobium meliloti and Bradyrhizobium japonicum, plant pathogen Agrobacterium tumefaciens and facultative intracellular mammalian pathogen Bartonella henselae. Comparative analyses of their circular chromosomes identified 514 orthologous genes shared among all five species. Shared among all five species are 50 identical blocks of microsyntenous orthologous genes (MOGs), containing a total of 283 genes. While retaining highly conserved genomic blocks of microsynteny, divergent evolution, horizontal gene transfer and niche specialization have disrupted macrosynteny among the five circular chromosomes compared. Highly conserved microsyntenous gene clusters help define the Rhizobiales, an order previously defined by 16S RNA gene similarity and herein represented by the three families: Bartonellaceae, Bradyrhizobiaceae and Rhizobiaceae. Genes without orthologs in the other four species help define individual species. The circular chromosomes of each of the five Rhizobiales species examined had genes lacking orthologs in the other four species. For example, 63 proteins are encoded by genes of 'Ca. Liberibacter asiaticus' not shared with other members of the Rhizobiales. Of these 63 proteins, 17 have predicted functions related to DNA replication or RNA transcription, and some of these may have roles related to low genomic GC content. An additional 17 proteins have predicted functions relevant to cellular processes, particularly modifications of the cell surface. Seventeen unshared proteins have specific metabolic functions including a pathway to synthesize cholesterol encoded by a seven-gene operon. The remaining 12 proteins encoded by 'Ca. Liberibacter asiaticus' genes not shared with other Rhizobiales are of bacteriophage origin. 'Ca. Liberibacter asiaticus' shares 11 genes with only Sinorhizobium meliloti and 12 genes are shared with only Bartonella henselae. - Funding: This research was supported by intramural United States Department of Agriculture Funds funds. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Related bacteria share orthologous proteins and genes. When chromosomes are compared, phylogenetically-related bacteria typically share regions of conserved gene order or microsynteny, formerly called clusters of orthologous genes (COGs). We propose the term MOG for Microsyntenous Orthologous Gene clusters to avoid confusion with clusters of orthologous groups of proteins described in the COG database which is now very widely used to identify and classify proteins and thus to identify and classify orthologous genes by their predicted products. Computational algorithms are available that allow identification of regions containing microsyntenous orthologous genes [1]. The arrangement of MOGs relative to that found in other genomes is revealed by mapping the order of blocks of microsyntenous orthologous genes in two or more genomes under comparison. Blocks of syntenous orthologous gene regions retain a phylogenetic signal over a broad range of bacteria [2]. This approach has been used to discover syntenous regions within the Rhizobiales, where large regions of conserved synteny were observed among free-living members of this order [34]. Huanglongbing (HLB), also called citrus greening, is the most serious disease of citrus worldwide [56]. This disease originated in south Asia [78] but has recently invaded both Brazil [9] and Florida [10], the sources of 90% of the worlds supply of orange juice. Candidatus Liberibacter asiaticus, a member of the a-2 subdivision of the Proteobacteria [11], is widely considered to be the causal agent of the disease, since it is consistently associated with the disease although Kochs postulates have not yet been demonstrated [12]. The pathogen is observed within sieve cells of phloem vessels of infected plant hosts [13] or in the salivary glands of citrus psyllids, the natural vector of the pathogen. Ca. Liberibacter asiaticus is also routinely detected by PCR assays, most based on the 16S rRNA gene [141 (...truncated)


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L. David Kuykendall, Jonathan Y. Shao, John S. Hartung. Conservation of Gene Order and Content in the Circular Chromosomes of ‘Candidatus Liberibacter asiaticus’ and Other Rhizobiales, PLOS ONE, 2012, 4, DOI: 10.1371/journal.pone.0034673