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Abstract Planthoppers in the family Cixiidae (Hemiptera: Auchenorrhyncha: Fulgoromorpha) harbor a diverse set of obligate bacterial endosymbionts that provision essential amino acids and vitamins that are missing from their plant-sap diet. “Candidatus Sulcia muelleri” and “Ca. Vidania fulgoroidea” have been associated with cixiid planthoppers since their origin within the Auchenorrhyncha, whereas “Ca. Purcelliella pentastirinorum” is a more recent endosymbiotic acquisition. Hawaiian cixiid planthoppers occupy diverse habitats including lava tube caves and shrubby surface landscapes, which offer different nutritional resources and environmental constraints. Genomic studies have focused on understanding the nutritional provisioning roles of cixiid endosymbionts more broadly, yet it is still unclear how selection pressures on endosymbiont genes might differ between cixiid host species inhabiting such diverse landscapes, or how variation in selection might impact symbiont evolution. In this study, we sequenced the genomes of Sulcia, Vidania, and Purcelliella isolated from both surface and cave-adapted planthopper hosts from the genus Oliarus. We found that nutritional biosynthesis genes were conserved in Sulcia and Vidania genomes in inter- and intra-host species comparisons. In contrast, Purcelliella genomes retain different essential nutritional biosynthesis genes between surface- and cave-adapted planthopper species. Finally, we see the variation in selection pressures on symbiont genes both within and between host species, suggesting that strong coevolution between host and endosymbiont is associated with different patterns of molecular evolution on a fine scale that may be associated with the host diet. 

Abstract Methylobacterium is a group of methylotrophic microbes associated with soil, fresh water, and particularly the phyllosphere, the aerial part of plants that has been well studied in terms of physiology but whose evolutionary history and taxonomy are unclear. Recent work has suggested that Methylobacterium is much more diverse than thought previously, questioning its status as an ecologically and phylogenetically coherent taxonomic genus. However, taxonomic and evolutionary studies of Methylobacterium have mostly been restricted to model species, often isolated from habitats other than the phyllosphere and have yet to utilize comprehensive phylogenomic methods to examine gene trees, gene content, or synteny. By analyzing 189 Methylobacterium genomes from a wide range of habitats, including the phyllosphere, we inferred a robust phylogenetic tree while explicitly accounting for the impact of horizontal gene transfer (HGT). We showed that Methylobacterium contains four evolutionarily distinct groups of bacteria (namely A, B, C, D), characterized by different genome size, GC content, gene content, and genome architecture, revealing the dynamic nature of Methylobacterium genomes. In addition to recovering 59 described species, we identified 45 candidate species, mostly phyllosphere-associated, stressing the significance of plants as a reservoir of Methylobacterium diversity. We inferred an ancient transition from a free-living lifestyle to association with plant roots in Methylobacteriaceae ancestor, followed by phyllosphere association of three of the major groups (A, B, D), whose early branching in Methylobacterium history has been heavily obscured by HGT. Together, our work lays the foundations for a thorough redefinition of Methylobacterium taxonomy, beginning with the abandonment of Methylorubrum. 

Abstract Synechococcus cyanobacteria are ubiquitous and abundant in the marine environment and contribute to an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core, from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus cells to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examine the variability of gene content and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements for DNA integration and site-specific recombination, suggesting that their genomic variability relies in part on a “tycheposon”-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the core genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of incomplete lineage sorting in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events.