Dataset Information

Suberin Regulates the Production of Cellulolytic Enzymes in Streptomyces scabiei, the Causal Agent of Potato Common Scab.

ABSTRACT: Suberin, a major constituent of the potato periderm, is known to promote the production of thaxtomins, the key virulence factors of the common scab-causing agent Streptomyces scabiei. In the present study, we speculated that suberin affected the production of glycosyl hydrolases, such as cellulases, by S. scabiei, and demonstrated that suberin promoted glycosyl hydrolase activity when added to cellulose-, xylan-, or lichenin-containing media. Furthermore, secretome analyses revealed that the addition of suberin to a cellulose-containing medium increased the production of glycosyl hydrolases. For example, the production of 13 out of the 14 cellulases produced by S. scabiei in cellulose-containing medium was stimulated by the presence of suberin. In most cases, the transcription of the corresponding cellulase-encoding genes was also markedly increased when the bacterium was grown in the presence of suberin and cellulose. The level of a subtilase-like protease inhibitor was markedly decreased by the presence of suberin. We proposed a model for the onset of S. scabiei virulence mechanisms by both cellulose and suberin, the main degradation product of cellulose that acts as an inducer of thaxtomin biosynthetic genes, and suberin promoting the biosynthesis of secondary metabolites including thaxtomins.

SUBMITTER: Padilla-Reynaud R

PROVIDER: S-EPMC4567563 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Suberin Regulates the Production of Cellulolytic Enzymes in Streptomyces scabiei, the Causal Agent of Potato Common Scab.

Padilla-Reynaud Rebeca R Simao-Beaunoir Anne-Marie AM Lerat Sylvain S Bernards Mark A MA Beaulieu Carole C

Microbes and environments 20150901 3

Suberin, a major constituent of the potato periderm, is known to promote the production of thaxtomins, the key virulence factors of the common scab-causing agent Streptomyces scabiei. In the present study, we speculated that suberin affected the production of glycosyl hydrolases, such as cellulases, by S. scabiei, and demonstrated that suberin promoted glycosyl hydrolase activity when added to cellulose-, xylan-, or lichenin-containing media. Furthermore, secretome analyses revealed that the add ...[more]

PMID: 26330095

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Project description:Thaxtomin A is a potent phytotoxin that serves as the principle pathogenicity determinant of the common scab pathogen, Streptomyces scabiei, and is also a promising natural herbicide for agricultural applications. The biosynthesis of thaxtomin A involves the non-ribosomal peptide synthetases (NRPSs) TxtA and TxtB, and an MbtH-like protein (MLP), TxtH, which may function as a chaperone by promoting the proper folding of the two NRPS enzymes in S. scabiei. MLPs are required for the proper function of many NRPS enzymes in bacteria, and they are often capable of interacting with NRPSs from different biosynthetic pathways, though the mechanism by which this occurs is still poorly understood. To gain additional insights into MLP functional cross-talk, we conducted a broad survey of MLPs from diverse phylogenetic lineages to determine if they could functionally replace TxtH. The MLPs were assessed using a protein solubility assay to determine whether they could promote the soluble expression of the TxtA and TxtB adenylation domains. In addition, the MLPs were tested for their ability to restore thaxtomin production in a S. scabiei mutant that lacked TxtH and other endogenous MLPs. Our results showed that the MLPs investigated vary in their ability to exhibit functional cross-talk with TxtH, with two of the MLPs being unable to compensate for the loss of TxtH in the assays performed. The ability of an MLP to serve as a functional partner for the thaxtomin NRPS was not correlated with its overall amino acid similarity with TxtH, but instead with the presence of highly conserved residues. In silico structural analysis of TxtH in association with the TxtA and TxtB adenylation domains revealed that several such residues are situated at the predicted interaction interface, suggesting that they might be critical for promoting functional interactions between MLPs and the thaxtomin NRPS enzymes. Overall, our study provides additional insights into the mechanism of MLP cross-talk, and it enhances our understanding of the thaxtomin biosynthetic machinery. It is anticipated that our findings will have useful applications for both the control of common scab disease and the commercial production of thaxtomin A for agricultural use.

Project description:Coronafacoyl phytotoxins are an important family of plant toxins that are produced by several different phytopathogenic bacteria, including the gammaproteobacterium Pseudomonas syringae and the actinobacterium Streptomyces scabiei (formerly Streptomyces scabies). The phytotoxins consist of coronafacic acid (CFA) linked via an amide bond to different amino acids or amino acid derivatives. Previous work suggested that S. scabiei and P. syringae use distinct biosynthetic pathways for producing CFA, which is subsequently linked to its amino acid partner to form the complete phytotoxin. Here, we provide further evidence that the S. scabiei CFA biosynthetic pathway is novel by characterizing the role of CYP107AK1, a predicted cytochrome P450 that has no homologue in P. syringae Deletion of the CYP107AK1 gene abolished production of coronafacoyl-isoleucine (CFA-Ile), the primary coronafacoyl phytotoxin produced by S. scabiei Structural elucidation of accumulated biosynthetic intermediates in the ΔCYP107AK1 mutant indicated that CYP107AK1 is required for introducing the oxygen atom that ultimately forms the carbonyl group in the CFA backbone. The CYP107AK1 gene along with two additional genes involved in CFA-Ile biosynthesis in S. scabiei were found to be associated with putative CFA biosynthetic genes in other actinobacteria but not in other organisms. Analysis of the overall genetic content and organization of known and putative CFA biosynthetic gene clusters, together with phylogenetic analysis of the core biosynthetic genes, indicates that horizontal gene transfer has played an important role in the dissemination of the gene cluster and that rearrangement, insertion, and/or deletion events have likely contributed to the divergent biosynthetic evolution of coronafacoyl phytotoxins in bacteria.IMPORTANCE The ability of plants to defend themselves against invading pathogens relies on complex signaling pathways that are controlled by key phytohormones such as jasmonic acid (JA). Some phytopathogenic bacteria have evolved the ability to manipulate JA signaling in order to overcome host defenses by producing coronatine (COR), which functions as a potent JA mimic. COR and COR-like molecules, collectively referred to as coronafacoyl phytotoxins, are produced by several different plant-pathogenic bacteria, and this study provides supporting evidence that different biosynthetic pathways are utilized by different bacteria for production of these phytotoxins. In addition, our study provides a greater understanding of how coronafacoyl phytotoxin biosynthesis may have evolved in phylogenetically distinct bacteria, and we demonstrate that production of these compounds may be more widespread than previously recognized and that their role for the producing organism may not be limited to host-pathogen interactions.

Project description:BACKGROUND:Suberin is a recalcitrant plant biopolymer composed of a polyphenolic and a polyaliphatic domain. Although suberin contributes to a significant portion of soil organic matter, the biological process of suberin degradation is poorly characterized. It has been suggested that Streptomyces scabiei, a plant pathogenic bacterium, can produce suberin-degrading enzymes. In this study, a comparative analysis of the S. scabiei secretome from culture media supplemented or not with potato suberin was carried out to identify enzymes that could be involved in suberin degradation. METHODS:S. scabiei was grown in the presence of casein only or in the presence of both casein and suberin. Extracellular proteins from 1-, 3- and 5-day-old supernatants were analyzed by LC-MS/MS to determine their putative functions. Real-time RT-PCR was performed to monitor the expression level of genes encoding several proteins potentially involved in suberin degradation. RESULTS:The effect of suberin on the extracellular protein profile of S. scabiei strain has been analyzed. A total of 246 proteins were found to be common in the data sets from both casein medium (CM) and casein-suberin medium (CSM), whereas 124 and 139 proteins were detected only in CM or CSM, respectively. The identified proteins could be divided into 19 functional groups. Two functional groups of proteins (degradation of aromatic compounds and secondary metabolism) were only associated with the CSM. A high proportion of the proteins found to be either exclusively produced, or overproduced, in presence of suberin were involved in carbohydrate metabolism. Most of the proteins included in the lipid metabolism class have been detected in CSM. Apart from lipid metabolism proteins, other identified proteins, particularly two feruloyl esterases, may also actively participate in the breakdown of suberin architecture. Both feruloyl esterase genes were overexpressed between 30 to 340 times in the presence of suberin. CONCLUSION:This study demonstrated that the presence of suberin in S. scabiei growth medium induced the production of a wide variety of glycosyl hydrolases. Furthermore, this study has allowed the identification of extracellular enzymes that could be involved in the degradation of suberin, including enzymes of the lipid metabolism and feruloyl esterases.

Dataset Information

Suberin Regulates the Production of Cellulolytic Enzymes in Streptomyces scabiei, the Causal Agent of Potato Common Scab.

Publications

Suberin Regulates the Production of Cellulolytic Enzymes in Streptomyces scabiei, the Causal Agent of Potato Common Scab.

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