Phytoplasma genomes: Evolution through mutually complementary mechanisms, gene loss and horizontal acquisition

Abstract

Phytoplasmas are cell wall-less bacteria that inhabit phloem sieve cells of infected plants and are transmitted by phloem-feeding insect vectors. Having descended from a Gram-positive, low G+C walled bacterium and more recently from an Acholeplasma-like ancestor, the phytoplasma clade underwent substantial evolutionary genome shrinkage. Yet, phytoplasma genomes contain numerous repeated sequences that appear in genomic islands. These islands, first termed sequence-variable mosaics (SVMs), were formed by recurrent and targeted attacks by ancient phages. This chapter describes distinctive architecture of phytoplasma genomes, genes unique to phytoplasmas, and genes that underwent lineage-specific acquisition and loss. The chapter also discusses essential genes that are missing in phytoplasmas compared with those present in Mycoplasma genitalium, a model free-living bacterium thought to have the minimum gene complement among known cellular organisms. Available genome data indicate that a common genomic thread unites all phytoplasmas: Through the formation of phage-based genomic islands, SVMs, the phytoplasma progenitor acquired new capabilities. Repeated and targeted chromosomal integration of phage genomes, and further gene acquisition through targeted insertion of mobile gene cassette-like elements, shaped the phytoplasma genome. While the loss of genes encoding diverse metabolic pathways must have led to increased host dependence, new capabilities were acquired that enabled and enhanced phytoplasma-host interactions. Thus, two mutually complementary, genome-sculpting mechanisms acting in concert played key roles in phytoplasma evolution. The rapidly evolving nature and lineage-specific adaptation of vertically inherited as well as horizontally acquired phytoplasmal genes are evident and deserve attention in future studies.