Evolutionary history of synthesis pathway genes for phloroglucinol and cyanide antimicrobials in plant-associated fluorescent pseudomonads

• Published in: Molecular phylogenetics and evolution 2012-06, Vol.63 (3), p.877-890
• Main Authors: Frapolli, Michele, Pothier, Joël F., Défago, Geneviève, Moënne-Loccoz, Yvan
• Format: Article
• Language: English
• Subjects: 2,4-Diacetylphloroglucinol; Anti-Infective Agents - metabolism; Antibiosis - genetics; Bacterial Typing Techniques; Base Composition; Bayes Theorem; Biochemistry, Molecular Biology; Biocontrol; Biosynthetic Pathways - genetics; Codon - genetics; Cyanides - metabolism; Evolution, Molecular; Evolutionary; Genes; Genes, Bacterial; Genes, Essential; Human health and pathology; Hydrogen cyanide; Life Sciences; Likelihood Functions; Linkage Disequilibrium; Loci; Metabolites; Models, Genetic; Multilocus analysis; Multilocus Sequence Typing; Phloroglucinol - metabolism; Phylogeny; Plants - microbiology; Pseudomonas; Pseudomonas fluorescens - genetics; Pseudomonas fluorescens - metabolism; Synthesis; Trees
• ISSN: 1055-7903; 1095-9513
• DOI: 10.1016/j.ympev.2012.02.030

[Display omitted] ► We studied genes involved in secondary metabolism of biocontrol pseudomonads. ► Pseudomonas genes for synthesis of antimicrobials displayed purifying selection. ► The evolutionary history of these genes was similar to that of housekeeping genes. ► Biocontrol-relevant genes are ancestral and inherited vertically in these bacteria. Plant-beneficial fluorescent Pseudomonas spp. play important ecological roles. Here, their evolutionary history was investigated by a multilocus approach targeting genes involved in synthesis of secondary antimicrobial metabolites implicated in biocontrol of phytopathogens. Some of these genes were proposed to be ancestral, and this was investigated using a worldwide collection of 30 plant-colonizing fluorescent pseudomonads, based on phylogenetic analysis of 14 loci involved in production of 2,4-diacetylphloroglucinol (phlACBDE, phlF, intergenic locus phlA/phlF), hydrogen cyanide (hcnABC, anr) or global regulation of secondary metabolism (gacA, gacS, rsmZ). The 10 housekeeping loci rrs, dsbA, gyrB, rpoD, fdxA, recA, rpoB, rpsL, rpsG, and fusA served as controls. Each strain was readily distinguished from the others when considering allelic combinations for these 14 biocontrol-relevant loci. Topology comparisons based on Shimodaira-Hasegawa tests showed extensive incongruence when comparing single-locus phylogenetic trees with one another, but less when comparing (after sequence concatenation) trees inferred for genes involved in 2,4-diacetylphloroglucinol synthesis, hydrogen cyanide synthesis, or secondary metabolism global regulation with trees for housekeeping genes. The 14 loci displayed linkage disequilibrium, as housekeeping loci did, and all 12 protein-coding loci were subjected to purifying selection except for one positively-selected site in HcnA. Overall, the evolutionary history of Pseudomonas genes involved in synthesis of secondary antimicrobial metabolites important for biocontrol functions is in fact similar to that of housekeeping genes, and results suggest that they are ancestral in pseudomonads producing hydrogen cyanide and 2,4-diacetylphloroglucinol.