Distribution and Evolution of Nonribosomal Peptide Synthetase Gene Clusters in the Ceratocystidaceae

Sayari, Mohammad; Nest, Magriet A. van der; Steenkamp, Emma Theodora; Soal, Nicole; Wilken, P. Markus; Wingfield, Brenda D.

doi:10.3390/genes10050328

Cited by 15 publications

(13 citation statements)

References 74 publications

(116 reference statements)

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“…The relative abundance of uncultured bacteria is not as high as that observed for KS domains. Additionally, in contrast with the KS domain dataset, several AD domain sequences were associated with Fungi and Planctomycetes, known to be rich in NRPS gene clusters [61,62] (Figure 4C).…”

Section: Taxonomic Identity Of Nrps Genesmentioning

confidence: 88%

Diversity of Bacterial Biosynthetic Genes in Maritime Antarctica

et al. 2020

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Bacterial natural products (NPs) are still a major source of new drug leads. Polyketides (PKs) and non-ribosomal peptides (NRP) are two pharmaceutically important families of NPs and recent studies have revealed Antarctica to harbor endemic polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS) genes, likely to be involved in the production of novel metabolites. Despite this, the diversity of secondary metabolites genes in Antarctica is still poorly explored. In this study, a computational bioprospection approach was employed to study the diversity and identity of PKS and NRPS genes to one of the most biodiverse areas in maritime Antarctica-Maxwell Bay. Amplicon sequencing of soil samples targeting ketosynthase (KS) and adenylation (AD) domains of PKS and NRPS genes, respectively, revealed abundant and unexplored chemical diversity in this peninsula. About 20% of AD domain sequences were only distantly related to characterized biosynthetic genes. Several PKS and NRPS genes were found to be closely associated to recently described metabolites including those from uncultured and candidate phyla. The combination of new approaches in computational biology and new culture-dependent and -independent strategies is thus critical for the recovery of the potential novel chemistry encoded in Antarctica microorganisms. target the highly conserved ketosynthase (KS) and adenylation (AD) domains of PKS and NRPS genes, respectively. A growing number of studies have employed the PCR-based sequence tag approach to uncover PKS and NRPS gene diversity across different environmental microbiomes [7][8][9].Extreme environments, such as Antarctica, have the potential to reveal novel molecules since they are still a poorly explored source of chemical scaffolds and novel chemical diversity [10,11]. As such, metabarcoding approaches to study PKS and NRPS diversity in Antarctic ecosystems represent a simple and effective strategy to understand the biosynthetic potential of a large number of sampling sites [7]. A couple of such studies have been carried out very recently in Antarctica [12,13] revealing that soils at different Antarctica locations harbor multiple endemic PKS and NRPS genes, likely to be involved in the synthesis of new chemical diversity. In Antarctic soils, the percentage of yet-uncultured genera is expected to be much higher [14] than the 82% described for general soils [15]. A considerable fraction of such uncultured bacteria corresponds to members of the NP-rich Actinobacteria [16,17] and Cyanobacteria [18,19] phyla.King George Island is one of the largest ice-free and biodiverse areas in maritime Antarctica [20]. It harbors a high density of scientific stations, particularly in Maxwell Bay [21], where most of terrestrial biology research takes place. Although bacterial diversity studies have been conducted in this area [22,23], the diversity of bacterial biosynthetic genes has not been a target of study. Here, we perform a detailed study on soil samples from Maxwell Bay, with the main goal of assessing the...

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Section: Taxonomic Identity Of Nrps Genesmentioning

confidence: 88%

Diversity of Bacterial Biosynthetic Genes in Maritime Antarctica

et al. 2020

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“…In all genomes, putative genes responsible for secondary metabolite production and gene clusters for type III PKS, NRPS and terpenes were found, with the last two being commonly observed in fungi. NRPS comprises a family of enzymes that assemble acyl substrates into compounds having functions in primary metabolism, cellular development and morphology, and stress responses, receiving attention due to their applications in medicine as antibiotics or immunosuppressive drugs ( Bloudoff and Schmeing, 2017 ; Sayari et al, 2019 ). Terpenoids are structurally the most diverse (over 70,000 different chemical structures) groups of natural compounds, widely distributed in nature, that play important physiological and metabolic functions and have significant medicinal value as antibacterial, antioxidant, and immune regulation ( Lyu et al, 2019 ; Moser and Pichler, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

Identification of Stress-Related Genes and a Comparative Analysis of the Amino Acid Compositions of Translated Coding Sequences Based on Draft Genome Sequences of Antarctic Yeasts

et al. 2021

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Microorganisms inhabiting cold environments have evolved strategies to tolerate and thrive in those extreme conditions, mainly the low temperature that slow down reaction rates. Among described molecular and metabolic adaptations to enable functioning in the cold, there is the synthesis of cold-active proteins/enzymes. In bacterial cold-active proteins, reduced proline content and highly flexible and larger catalytic active sites than mesophylls counterparts have been described. However, beyond the low temperature, microorganisms’ physiological requirements may differ according to their growth velocities, influencing their global protein compositions. This hypothesis was tested in this work using eight cold-adapted yeasts isolated from Antarctica, for which their growth parameters were measured and their draft genomes determined and bioinformatically analyzed. The optimal temperature for yeasts’ growth ranged from 10 to 22°C, and yeasts having similar or same optimal temperature for growth displayed significative different growth rates. The sizes of the draft genomes ranged from 10.7 (Tetracladium sp.) to 30.7 Mb (Leucosporidium creatinivorum), and the GC contents from 37 (Candida sake) to 60% (L. creatinivorum). Putative genes related to various kinds of stress were identified and were especially numerous for oxidative and cold stress responses. The putative proteins were classified according to predicted cellular function and subcellular localization. The amino acid composition was compared among yeasts considering their optimal temperature for growth and growth rates. In several groups of predicted proteins, correlations were observed between their contents of flexible amino acids and both the yeasts’ optimal temperatures for growth and their growth rates. In general, the contents of flexible amino acids were higher in yeasts growing more rapidly as their optimal temperature for growth was lower. The contents of flexible amino acids became lower among yeasts with higher optimal temperatures for growth as their growth rates increased.

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“…basicola ). These genomes were previously shown to have high levels of completeness [ 16 , 17 ], suggesting that they would be useful for the identification of putative genes in involved in terpenoid biosynthesis.…”

Section: Methodsmentioning

confidence: 99%

Characterization of the Ergosterol Biosynthesis Pathway in Ceratocystidaceae

Sayari

Nest

Steenkamp

et al. 2021

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Terpenes represent the biggest group of natural compounds on earth. This large class of organic hydrocarbons is distributed among all cellular organisms, including fungi. The different classes of terpenes produced by fungi are mono, sesqui, di- and triterpenes, although triterpene ergosterol is the main sterol identified in cell membranes of these organisms. The availability of genomic data from members in the Ceratocystidaceae enabled the detection and characterization of the genes encoding the enzymes in the mevalonate and ergosterol biosynthetic pathways. Using a bioinformatics approach, fungal orthologs of sterol biosynthesis genes in nine different species of the Ceratocystidaceae were identified. Ergosterol and some of the intermediates in the pathway were also detected in seven species (Ceratocystis manginecans, C. adiposa, Huntiella moniliformis, Thielaviopsis punctulata, Bretziella fagacearum, Endoconidiophora polonica and Davidsoniella virescens), using gas chromatography-mass spectrometry analysis. The average ergosterol content differed among different genera of Ceratocystidaceae. We also identified all possible terpene related genes and possible biosynthetic clusters in the genomes used in this study. We found a highly conserved terpene biosynthesis gene cluster containing some genes encoding ergosterol biosynthesis enzymes in the analysed genomes. An additional possible terpene gene cluster was also identified in all of the Ceratocystidaceae. We also evaluated the sensitivity of the Ceratocystidaceae to a triazole fungicide that inhibits ergosterol synthesis. The results showed that different members of this family behave differently when exposed to different concentrations of triazole tebuconazole.

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Distribution and Evolution of Nonribosomal Peptide Synthetase Gene Clusters in the Ceratocystidaceae

Cited by 15 publications

References 74 publications

Diversity of Bacterial Biosynthetic Genes in Maritime Antarctica

Diversity of Bacterial Biosynthetic Genes in Maritime Antarctica

Identification of Stress-Related Genes and a Comparative Analysis of the Amino Acid Compositions of Translated Coding Sequences Based on Draft Genome Sequences of Antarctic Yeasts

Characterization of the Ergosterol Biosynthesis Pathway in Ceratocystidaceae

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