Ancient, recurrent phage attacks and recombination events shaped dynamic sequence-variable mosaic structures at the root of phytoplasma genome evolution

Authors: WEI, WEI - LIAONING CHINA; Davis, Robert; JOMANTIENE, RASA - VILNIUS LITHUANIA; Zhao, Yan

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/11/2008
Publication Date: 6/6/2008
Citation: Wei, W., Davis, R.E., Jomantiene, R., Zhao, Y. 2008. Ancient, recurrent phage attacks and recombination events shaped dynamic sequence-variable mosaic structures at the root of phytoplasma genome evolution. Proceedings of the National Academy of Sciences. 105:11827-11832.

Interpretive Summary: Phytoplasmas are small bacteria that infect several hundred plant species, responsible for numerous diseases in economically important crops worldwide. In recent years, new phytoplasmas and emerging phytoplasmal diseases have been identified in an ever increasingly rapid pace, but scientists still do not know how phytoplasmas cause diseases. In previous studies we discovered that genomes (complete sets of genetic materials) of phytoplasmas contain certain diverse genes that are occur in repeated clusters, forming unique mosaic structures. We hypothesized that these composite structures were formed through repeated attacks by mobile genetic entities. In the present study, we discovered that the unique mosaic structures were generated through repeated attacks by phages (bacterial viruses) whose genes had became part of the phytoplasma genome. Differences in sizes among different phytoplasma genomes were explained by the numbers of phage-derived genes that were “absorbed” by the phytoplasma over evolutionary time. Each phytoplasma’s phage-derived genes possess unique physical properties distinct from those of their host genes, marking them as forming functionally important structures called “genomic islands”. In other plant-, animal-, and human-infecting bacteria such genomic islands often carry genes that cause diseases. Since the phage-derived mosaic genome structure is present only in phytoplasmas but not in closely-related bacteria or their common ancestors, we envision that repeated ancient phage attacks and subsequent genetic recombination events launched phytoplasma genome evolution, shaped phytoplasma genome architecture, and introduced novel genes enabling phytoplasmal pathogenicity. This work will interest scientists and students studying the evolution of bacteria and molecular basis of disease mechanisms, as well as to plant doctors involved in pathogen detection.

Technical Abstract: Mobile genetic elements have impacted biological evolution across all studied organisms, but evidence for a role in launching evolutionary emergence of an entire phylogenetic clade has not been forthcoming. Here we suggest that mobile element predation played a formative role in the emergence of the phytoplasma clade. Phytoplasmas are cell wall-less bacteria that cause numerous diseases in plants and are transmitted by insects. Phylogenetic analyses indicate that these transkingdom parasites descended from Gram-positive walled bacteria, but events giving rise to the origin of the first phytoplasma have remained unknown. Previously we discovered a unique feature of phytoplasmal genome architecture, genes clustered in sequence variable mosaics (SVMs), and suggested that such structure formed through recurrent, targeted attacks by mobile elements. In the present study, we discovered that cryptic prophage remnants, originating from phages in Class Caudovirales, formed the SVMs and comprised exceptionally large percentages of the chromosomes of ‘Candidatus Phytoplasma asteris’-related strains OYM and AYWB, occupying nearly all major non-syntenic sections, and accounting for most of the overall size difference between the two genomes. The clustered phage remnants formed genomic islands exhibiting distinct DNA physical signatures, such as dinucleotide relative abundance and codon position GC values. Numerous phytoplasma strain-specific genes were identified as phage morons, some of which were located in hyper-variable regions within individual SVMs, indicating that prophage remnants played important roles in generating phytoplasma genetic diversity. Since no SVM-like structures could be identified in genomes of ancestral relatives including Acholeplasma spp., we hypothesize that ancient phage attacks leading to SVMs formation occurred after divergence of phytoplasmas from acholeplasmas, triggering evolution of the phytoplasma clade.