scholarly journals Increased abundance of secreted hydrolytic enzymes and secondary metabolite gene clusters define the genomes of latent plant pathogens in the Botryosphaeriaceae

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Jan H. Nagel ◽  
Michael J. Wingfield ◽  
Bernard Slippers
Keyword(s):  
Secondary Metabolite ◽  
Plant Pathogens ◽  
Plant Cell Wall ◽  
Hydrolytic Enzymes ◽  
Gene Clusters ◽  
Comparative Genomic ◽  
Biosynthetic Gene ◽  
Plant Interactions ◽  
Biosynthetic Gene Clusters ◽  
Genome Analyses

Abstract Background The Botryosphaeriaceae are important plant pathogens, but also have the ability to establish asymptomatic infections that persist for extended periods in a latent state. In this study, we used comparative genome analyses to shed light on the genetic basis of the interactions of these fungi with their plant hosts. For this purpose, we characterised secreted hydrolytic enzymes, secondary metabolite biosynthetic gene clusters and general trends in genomic architecture using all available Botryosphaeriaceae genomes, and selected Dothideomycetes genomes. Results The Botryosphaeriaceae genomes were rich in carbohydrate-active enzymes (CAZymes), proteases, lipases and secondary metabolic biosynthetic gene clusters (BGCs) compared to other Dothideomycete genomes. The genomes of Botryosphaeria, Macrophomina, Lasiodiplodia and Neofusicoccum, in particular, had gene expansions of the major constituents of the secretome, notably CAZymes involved in plant cell wall degradation. The Botryosphaeriaceae genomes were shown to have moderate to high GC contents and most had low levels of repetitive DNA. The genomes were not compartmentalized based on gene and repeat densities, but genes of secreted enzymes were slightly more abundant in gene-sparse regions. Conclusion The abundance of secreted hydrolytic enzymes and secondary metabolite BGCs in the genomes of Botryosphaeria, Macrophomina, Lasiodiplodia, and Neofusicoccum were similar to those in necrotrophic plant pathogens and some endophytes of woody plants. The results provide a foundation for comparative genomic analyses and hypotheses to explore the mechanisms underlying Botryosphaeriaceae host-plant interactions.

scholarly journals Abundant secreted hydrolytic enzymes and secondary metabolite gene clusters in genomes of the Botryosphaeriaceae reflect their role as important plant pathogens

2021 ◽  
Author(s):  
JH Nagel ◽  
MJ Wingfield ◽  
B Slippers
Keyword(s):  
Secondary Metabolite ◽  
Plant Pathogens ◽  
Plant Cell Wall ◽  
Hydrolytic Enzymes ◽  
Gene Clusters ◽  
Comparative Genomic ◽  
Biosynthetic Gene ◽  
Plant Interactions ◽  
Biosynthetic Gene Clusters ◽  
Plant Cell Wall Degradation

AbstractThe Botryosphaeriaceae are important plant pathogens, but unique in their ability to establish asymptomatic infections that persist for extended periods in a latent state. In this study, we used comparative analyses to consider elements that might shed light on the genetic basis of the interactions of these fungi with their plant hosts. For this purpose, we characterised secreted hydrolytic enzymes, secondary metabolite biosynthetic gene clusters and considered general trends in genomic architecture using all available Botryosphaeriaceae genomes, and selected Dothideomycetes genomes. The Botryosphaeriaceae genomes were rich in carbohydrate-active enzymes (CAZymes), proteases, lipases and secondary metabolic biosynthetic gene clusters (BGCs) compared to other Dothideomycete genomes. The genomes of Botryosphaeria, Macrophomina, Lasiodiplodia and Neofusicoccum, in particular, had gene expansions of the major constituents of the secretome, notably CAZymes involved in plant cell wall degradation. The Botryosphaeriaceae genomes were shown to have moderate to high GC contents and most had low levels of repetitive DNA. The genomes were not compartmentalized based on gene and repeat densities, but genes of secreted enzymes were slightly more abundant in gene-sparse regions. The abundance of secreted hydrolytic enzymes and secondary metabolite BGCs in the genomes of Botryosphaeria, Macrophomina, Lasiodiplodia, and Neofusicoccum were similar to those in necrotrophic plant pathogens, but also endophytes of woody plants. The results provide a foundation for future comparative genomic analyses and hypothesis to explore the mechanisms underlying Botryosphaeriaceae host-plant interactions.

scholarly journals Elucidating the diversity and potential function of nonribosomal peptide and polyketide biosynthetic gene clusters in the root microbiome

2020 ◽  
Author(s):  
Barak Dror ◽  
Zongqiang Wang ◽  
Sean F. Brady ◽  
Edouard Jurkevitch ◽  
Eddie Cytryn
Keyword(s):  
Secondary Metabolite ◽  
Gene Clusters ◽  
Bulk Soil ◽  
Large Set ◽  
Biosynthetic Gene ◽  
Plant Interactions ◽  
Biosynthetic Gene Clusters ◽  
Shotgun Metagenomics ◽  
Nonribosomal Peptide ◽  
Encoding Genes

AbstractPolyketides (PKs) and nonribosomal peptides (NRPs) are two microbial secondary metabolite (SM) families known for their variety of functions, including antimicrobials, siderophores and others. Despite their involvement in bacteria-bacteria and bacteria-plant interactions, root-associated SMs are largely unexplored due to the limited cultivability of bacteria. Here, we analyzed the diversity and expression of SM-encoding biosynthetic gene clusters (BGCs) in root microbiomes by culture-independent amplicon sequencing, shotgun metagenomics and metatranscriptomics. Roots (tomato and lettuce) harbored distinct compositions of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs) relative to the adjacent bulk soil, and specific BGC markers were both enriched and highly expressed in the root microbiomes. While several of the highly abundant and expressed sequences were remotely associated with known BGCs, the low similarity to characterized genes suggests their potential novelty. Low similarity genes were screened against a large set of soil-derived cosmid libraries, from which five whole BGCs of unknown function were retrieved. Three clusters were taxonomically affiliated with Actinobacteria, while the remaining were not associated with known bacteria. One Streptomyces-derived BGC was predicted to encode for a polyene with potential antifungal activity, while the others were too novel to predict chemical structure. Screening against a suite of metagenomic datasets revealed a higher abundance of retrieved clusters in roots and soil samples. In contrast, they were almost completely absent in aquatic and gut environments, supporting the notion that they might play an important role in root ecosystems. Overall, our results indicate that root microbiomes harbor a specific assemblage of undiscovered SMs.ImportanceWe identified distinct secondary metabolite (polyketide and nonribosomal peptide) encoding genes that are enriched (relative to adjacent bulk soil) and expressed in root ecosystems, yet almost completely absent in human gut and aquatic environments. Several of the genes were distantly related to genes encoding for antimicrobials and siderophores, and their high sequence variability relative to known sequences suggests that they may encode for novel metabolites and may have unique ecological functions. This study demonstrates that plant roots harbor a diverse array of unique secondary metabolite encoding genes that are highly enriched and expressed in the root ecosystem. The secondary metabolites encoded by these genes might assist the bacteria that produce them in colonization and persistence in the root environment. To explore this hypothesis, future investigations should assess their potential role in inter-bacterial and bacterial-plant interactions.

scholarly journals Elucidating the Diversity and Potential Function of Nonribosomal Peptide and Polyketide Biosynthetic Gene Clusters in the Root Microbiome

mSystems ◽  
2020 ◽  
Vol 5 (6) ◽  
pp. e00866-20
Author(s):  
Barak Dror ◽  
Zongqiang Wang ◽  
Sean F. Brady ◽  
Edouard Jurkevitch ◽  
Eddie Cytryn
Keyword(s):  
Secondary Metabolite ◽  
Gene Clusters ◽  
Bulk Soil ◽  
Metagenomic Data ◽  
Large Set ◽  
Biosynthetic Gene ◽  
Plant Interactions ◽  
Biosynthetic Gene Clusters ◽  
Nonribosomal Peptide ◽  
Encoding Genes

ABSTRACTPolyketides (PKs) and nonribosomal peptides (NRPs) are two microbial secondary metabolite (SM) families known for their variety of functions, including antimicrobials, siderophores, and others. Despite their involvement in bacterium-bacterium and bacterium-plant interactions, root-associated SMs are largely unexplored due to the limited cultivability of bacteria. Here, we analyzed the diversity and expression of SM-encoding biosynthetic gene clusters (BGCs) in root microbiomes by culture-independent amplicon sequencing, shotgun metagenomics, and metatranscriptomics. Roots (tomato and lettuce) harbored distinct compositions of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs) relative to the adjacent bulk soil, and specific BGC markers were both enriched and highly expressed in the root microbiomes. While several of the highly abundant and expressed sequences were remotely associated with known BGCs, the low similarity to characterized genes suggests their potential novelty. Low-similarity genes were screened against a large set of soil-derived cosmid libraries, from which five whole BGCs of unknown function were retrieved. Three clusters were taxonomically affiliated with Actinobacteria, while the remaining were not associated with known bacteria. One Streptomyces-derived BGC was predicted to encode a polyene with potential antifungal activity, while the others were too novel to predict chemical structure. Screening against a suite of metagenomic data sets revealed higher abundances of retrieved clusters in roots and soil samples. In contrast, they were almost completely absent in aquatic and gut environments, supporting the notion that they might play an important role in root ecosystems. Overall, our results indicate that root microbiomes harbor a specific assemblage of undiscovered SMs.IMPORTANCE We identified distinct secondary-metabolite-encoding genes that are enriched (relative to adjacent bulk soil) and expressed in root ecosystems yet almost completely absent in human gut and aquatic environments. Several of the genes were distantly related to genes encoding antimicrobials and siderophores, and their high sequence variability relative to known sequences suggests that they may encode novel metabolites and may have unique ecological functions. This study demonstrates that plant roots harbor a diverse array of unique secondary-metabolite-encoding genes that are highly enriched and expressed in the root ecosystem. The secondary metabolites encoded by these genes might assist the bacteria that produce them in colonization and persistence in the root environment. To explore this hypothesis, future investigations should assess their potential role in interbacterial and bacterium-plant interactions.

scholarly journals Phylogenetic Distribution of Secondary Metabolites in the Bacillus subtilis Species Complex

mSystems ◽  
2021 ◽  
Vol 6 (2) ◽  
Author(s):  
Kat Steinke ◽  
Omkar S. Mohite ◽  
Tilmann Weber ◽  
Ákos T. Kovács
Keyword(s):  
Bacillus Subtilis ◽  
Secondary Metabolites ◽  
Secondary Metabolite ◽  
Species Complex ◽  
Gene Clusters ◽  
Biosynthetic Gene ◽  
Biosynthetic Gene Clusters ◽  
Content Type ◽  
Frameshift Mutations ◽  
Metabolite Production

ABSTRACT Microbes produce a plethora of secondary (or specialized) metabolites that, although not essential for primary metabolism, benefit them to survive in the environment, communicate, and influence cell differentiation. Biosynthetic gene clusters (BGCs), responsible for the production of these secondary metabolites, are readily identifiable on bacterial genome sequences. Understanding the phylogeny and distribution of BGCs helps us to predict the natural product synthesis ability of new isolates. Here, we examined 310 genomes from the Bacillus subtilis group, determined the inter- and intraspecies patterns of absence/presence for all BGCs, and assigned them to defined gene cluster families (GCFs). This allowed us to establish patterns in the distribution of both known and unknown products. Further, we analyzed variations in the BGC structures of particular families encoding natural products, such as plipastatin, fengycin, iturin, mycosubtilin, and bacillomycin. Our detailed analysis revealed multiple GCFs that are species or clade specific and a few others that are scattered within or between species, which will guide exploration of the chemodiversity within the B. subtilis group. Surprisingly, we discovered that partial deletion of BGCs and frameshift mutations in selected biosynthetic genes are conserved within phylogenetically related isolates, although isolated from around the globe. Our results highlight the importance of detailed genomic analysis of BGCs and the remarkable phylogenetically conserved erosion of secondary metabolite biosynthetic potential in the B. subtilis group. IMPORTANCE Members of the B. subtilis species complex are commonly recognized producers of secondary metabolites, among those, the production of antifungals, which makes them promising biocontrol strains. While there are studies examining the distribution of well-known secondary metabolites in Bacilli, intraspecies clade-specific distribution has not been systematically reported for the B. subtilis group. Here, we report the complete biosynthetic potential within the B. subtilis group to explore the distribution of the biosynthetic gene clusters and to reveal an exhaustive phylogenetic conservation of secondary metabolite production within Bacillus that supports the chemodiversity within this species complex. We identify that certain gene clusters acquired deletions of genes and particular frameshift mutations, rendering them inactive for secondary metabolite biosynthesis, a conserved genetic trait within phylogenetically conserved clades of certain species. The overview guides the assignment of the secondary metabolite production potential of newly isolated Bacillus strains based on genome sequence and phylogenetic relatedness.

scholarly journals The antiSMASH database, a comprehensive database of microbial secondary metabolite biosynthetic gene clusters

2016 ◽  
Vol 45 (D1) ◽  
pp. D555-D559 ◽  
Author(s):  
Kai Blin ◽  
Marnix H. Medema ◽  
Renzo Kottmann ◽  
Sang Yup Lee ◽  
Tilmann Weber
Keyword(s):  
Secondary Metabolite ◽  
Gene Clusters ◽  
Biosynthetic Gene ◽  
Biosynthetic Gene Clusters ◽  
Comprehensive Database

scholarly journals DoBISCUIT: a database of secondary metabolite biosynthetic gene clusters

2012 ◽  
Vol 41 (D1) ◽  
pp. D408-D414 ◽  
Author(s):  
Natsuko Ichikawa ◽  
Machi Sasagawa ◽  
Mika Yamamoto ◽  
Hisayuki Komaki ◽  
Yumi Yoshida ◽  
...  
Keyword(s):  
Secondary Metabolite ◽  
Gene Clusters ◽  
Biosynthetic Gene ◽  
Biosynthetic Gene Clusters

scholarly journals A Community Effort: Combining Functional Amplicon Sequencing and Metagenomics Reveals Potential Biosynthetic Gene Clusters Associated with Protective Phenotypes in Rhizosphere Microbiomes

mSystems ◽  
2021 ◽  
Author(s):  
Jaclyn M. Winter
Keyword(s):  
Plant Growth ◽  
Plant Pathogens ◽  
Gene Clusters ◽  
Amplicon Sequencing ◽  
Plant Roots ◽  
Biosynthetic Gene ◽  
Biosynthetic Gene Clusters ◽  
First Line ◽  
Community Effort ◽  
Promote Plant Growth

Soil-dwelling microorganisms associated with plant roots carry out essential processes that promote plant growth and productivity. In addition to these beneficial functions, the rhizosphere microbiome also serves as the first line of defense against many plant pathogens.

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