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Comparative Genomics Reveals Insights into Induction of Violacein Biosynthesis and Adaptive Evolution in Janthinobacterium.

ABSTRACT: Violacein has different bioactive properties conferring distinct selective advantages, such as defense from predation and interspecific competition. Adaptation of Janthinobacterium to diverse habitats likely leads to variation in violacein production among phylogenetically closely related species inhabiting different environments, yet genomic mechanisms and the influence of adaptive evolution underpinning violacein biosynthesis in Janthinobacterium are not clear. In this study, we performed genome sequencing, comparative genomic analysis, and phenotypic characterization to investigate genomic factors regulating violacein production in nine Janthinobacterium strains, including a type strain from soil and eight strains we isolated from terrestrial subsurface sediment and groundwater. Results show that although all nine Janthinobacterium strains are phylogenetically closely related and contain genes essential for violacein biosynthesis, they vary in carbon usage and violacein production. Sediment and groundwater strains are weak violacein producers and possess far fewer secondary metabolite biosynthesis genes, indicating genome adaptation compared to soil strains. Further examination suggests that quorum sensing (QS) may play an important role in regulating violacein in Janthinobacterium: the strains exhibiting strong potential in violacein production possess both N-acyl-homoserine lactone (AHL) QS and Janthinobacterium QS (JQS) systems in their genomes, while weaker violacein-producing strains harbor only the JQS system. Preliminary tests of spent media of two Janthinobacterium strains possessing both AHL QS and JQS systems support the potential role of AHLs in inducing violacein production in Janthinobacterium. Overall, results from this study reveal potential genomic mechanisms involved in violacein biosynthesis in Janthinobacterium and provide insights into evolution of Janthinobacterium for adaptation to oligotrophic terrestrial subsurface environment. IMPORTANCE Phylogenetically closely related bacteria can thrive in diverse environmental habitats due to adaptive evolution. Genomic changes resulting from adaptive evolution lead to variations in cellular function, metabolism, and secondary metabolite biosynthesis. The most well-known secondary metabolite produced by Janthinobacterium is the purple-violet pigment violacein. To date, the mechanisms of induction of violacein biosynthesis in Janthinobacterium is not clear. Comparative genome analysis of closely related Janthinobacterium strains isolated from different environmental habitats not only reveals potential mechanisms involved in induction of violacein production by Janthinobacterium but also provides insights into the survival strategy of Janthinobacterium for adaptation to oligotrophic terrestrial subsurface environment.

SUBMITTER: Wu X

PROVIDER: S-EPMC8672880 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe Begonia species are common shade plants that are mostly found in southwest China. They have not been well studied despite their medicinal and decorative uses because gene penetration, decreased adaptability, and restricted availability are all caused by frequent interspecific hybridization.ResultTo understand the patterns of mutation in the chloroplast genomes of different species of Begonia, as well as their evolutionary relationships, we collected seven Begonia species in China and sequenced their chloroplast genomes. Begonia species exhibit a quadripartite structure of chloroplast genomes (157,634 - 169,694 bp), consisting of two pairs of inverted repeats (IR: 26,529 - 37,674 bp), a large single copy (LSC: 75,477 - 86,500 bp), and a small single copy (SSC: 17,861 - 18,367 bp). 128-143 genes (comprising 82-93 protein-coding genes, 8 ribosomal RNAs, and 36-43 transfer RNAs) are found in the chloroplast genomes. Based on comparative analyses, this taxon has a relatively similar genome structure. A total of six substantially divergent DNA regions (trnT-UGU-trnL-UAA, atpF-atpH, ycf4-cemA, psbC-trnS-UGA, rpl32-trnL-UAG, and ccsA-ndhD) are found in the seventeen chloroplast genomes. These regions are suitable for species identification and phylogeographic analysis. Phylogenetic analysis shows that Begonia species that were suited to comparable environments grouped in a small clade and that all Begonia species formed one big clade in the phylogenetic tree, supporting the genus' monophyly. In addition, positive selection sites were discovered in eight genes (rpoC1, rpoB, psbE, psbK, petA, rps12, rpl2, and rpl22), the majority of which are involved in protein production and photosynthesis.ConclusionUsing these genome resources, we can resolve deep-level phylogenetic relationships between Begonia species and their families, leading to a better understanding of evolutionary processes. In addition to enhancing species identification and phylogenetic resolution, these results demonstrate the utility of complete chloroplast genomes in phylogenetically and taxonomically challenging plant groupings.

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Comparative Genomics Reveals Insights into Induction of Violacein Biosynthesis and Adaptive Evolution in Janthinobacterium.

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