Dataset Information

In Silico Analysis of P450s and Their Role in Secondary Metabolism in the Bacterial Class Gammaproteobacteria.

ABSTRACT: The impact of lifestyle on shaping the genome content of an organism is a well-known phenomenon and cytochrome P450 enzymes (CYPs/P450s), heme-thiolate proteins that are ubiquitously present in organisms, are no exception. Recent studies focusing on a few bacterial species such as Streptomyces, Mycobacterium, Cyanobacteria and Firmicutes revealed that the impact of lifestyle affected the P450 repertoire in these species. However, this phenomenon needs to be understood in other bacterial species. We therefore performed genome data mining, annotation, phylogenetic analysis of P450s and their role in secondary metabolism in the bacterial class Gammaproteobacteria. Genome-wide data mining for P450s in 1261 Gammaproteobacterial species belonging to 161 genera revealed that only 169 species belonging to 41 genera have P450s. A total of 277 P450s found in 169 species grouped into 84 P450 families and 105 P450 subfamilies, where 38 new P450 families were found. Only 18% of P450s were found to be involved in secondary metabolism in Gammaproteobacterial species, as observed in Firmicutes as well. The pathogenic or commensal lifestyle of Gammaproteobacterial species influences them to such an extent that they have the lowest number of P450s compared to other bacterial species, indicating the impact of lifestyle on shaping the P450 repertoire. This study is the first report on comprehensive analysis of P450s in Gammaproteobacteria.

SUBMITTER: Msomi NN

PROVIDER: S-EPMC7998510 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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Publications

In Silico Analysis of P450s and Their Role in Secondary Metabolism in the Bacterial Class Gammaproteobacteria.

Msomi Ntombizethu Nokuphiwa NN Padayachee Tiara T Nzuza Nomfundo N Syed Puleng Rosinah PR Kryś Justyna Dorota JD Chen Wanping W Gront Dominik D Nelson David R DR Syed Khajamohiddin K

Molecules (Basel, Switzerland) 20210311 6

The impact of lifestyle on shaping the genome content of an organism is a well-known phenomenon and cytochrome P450 enzymes (CYPs/P450s), heme-thiolate proteins that are ubiquitously present in organisms, are no exception. Recent studies focusing on a few bacterial species such as Streptomyces, Mycobacterium, Cyanobacteria and Firmicutes revealed that the impact of lifestyle affected the P450 repertoire in these species. However, this phenomenon needs to be understood ...[more]

PMID: 33799696

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Project description:BackgroundMicrobes, plants, and fungi synthesize an enormous number of metabolites exhibiting rich chemical diversity. For a high-level classification, metabolism is subdivided into primary (PM) and secondary (SM) metabolism. SM products are often not essential for survival of the organism and it is generally assumed that SM enzymes stem from PM homologs.ResultsWe wanted to assess evolutionary relationships and function of bona fide bacterial PM and SM enzymes. Thus, we analyzed the content of 1010 biosynthetic gene clusters (BGCs) from the MIBiG dataset; the encoded bacterial enzymes served as representatives of SM. The content of 15 bacterial genomes known not to harbor BGCs served as a representation of PM. Enzymes were categorized on their EC number and for these enzyme functions, frequencies were determined. The comparison of PM/SM frequencies indicates a certain preference for hydrolases (EC class 3) and ligases (EC class 6) in PM and of oxidoreductases (EC class 1) and lyases (EC class 4) in SM. Based on BLAST searches, we determined pairs of PM/SM homologs and their functional diversity. Oxidoreductases, transferases (EC class 2), lyases and isomerases (EC class 5) form a tightly interlinked network indicating that many protein folds can accommodate different functions in PM and SM. In contrast, the functional diversity of hydrolases and especially ligases is significantly limited in PM and SM. For the most direct comparison of PM/SM homologs, we restricted for each BGC the search to the content of the genome it comes from. For each homologous hit, the contribution of the genomic neighborhood to metabolic pathways was summarized in BGC-specific html-pages that are interlinked with KEGG; this dataset can be downloaded from https://www.bioinf.ur.de .ConclusionsOnly few reaction chemistries are overrepresented in bacterial SM and at least 55% of the enzymatic functions present in BGCs possess PM homologs. Many SM enzymes arose in PM and Nature utilized the evolvability of enzymes similarly to establish novel functions both in PM and SM. Future work aimed at the elucidation of evolutionary routes that have interconverted a PM enzyme into an SM homolog can profit from our BGC-specific annotations.

Project description:Orders Oceanospirillales and Pseudomonadales play important roles in various ecosystems as the keystone taxa of microbiomes. However, the two orders present a close evolutionary relationship, which might have caused taxonomic misinterpretation and resulted in an incorrect understanding of their evolutionary history. In this study, first, we used the 16S rRNA gene sequences of 2,049 species of Gammaproteobacteria to build a phylogenetic tree, which demonstrated that reports regarding the evolutionary relationship of orders Cellvibrionales, Oceanospirillales, and Pseudomonadales based on a single conserved gene with a poor resolution have been conflicting; in particular, the major families Moraxellaceae and Pseudomonadaceae of order Pseudomonadales were separated from orders Cellvibrionales and Oceanospirillales Subsequently, we constructed the bac120 trees of all representative reference genomes of class Gammaproteobacteria based on 120 ubiquitous single-copy proteins from bacteria and a phylogenomic tree based on the 119 core genes of 257 reference genomes obtained from orders Cellvibrionales, Oceanospirillales, and Pseudomonadales to cross validate and infer their intrinsic evolutionary relationships. These results indicated that two novel orders, Moraxellales ord. nov. and Kangiellales ord. nov., and three novel families, Marinobacteraceae fam. nov., Perlucidibacaceae fam. nov., and Zooshikellaceae fam. nov., should be proposed. Additionally, orders Cellvibrionales and Oceanospirillales were merged into the order Pseudomonadales except for families Moraxellaceae and Kangiellaceae in class Gammaproteobacteria, which currently includes 18 families. Our work sheds some light on the evolutionary history of class Gammaproteobacteria, which could facilitate the detection and taxonomic analysis of natural communities.IMPORTANCE The orders Cellvibrionales, Oceanospirillales, and Pseudomonadales, as three major orders of the largest bacterial class, Gammaproteobacteria, play important roles in various ecosystems as the keystone taxa of microbiomes, but their evolutionary relationship is currently polyphyletic and chaotic. Here, we constructed a bac120 tree and core-genome tree and calculated the amino acid identity (AAI) value to explore their intrinsic evolutionary history. In this study, we proposed two novel orders and three novel families. This evolution study vastly reconstructed the taxonomic framework of class Gammaproteobacteria and could provide a more distinct perspective on global distribution and evolutionary patterns of these environmental microorganisms.

Dataset Information

In Silico Analysis of P450s and Their Role in Secondary Metabolism in the Bacterial Class Gammaproteobacteria.

Publications

In Silico Analysis of P450s and Their Role in Secondary Metabolism in the Bacterial Class <i>Gammaproteobacteria</i>.

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