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Putative antiparasite defensive system involving ribosomal and nonribosomal oligopeptides in cyanobacteria of the genus Planktothrix.

ABSTRACT: Parasitic chytrid fungi can inflict significant mortality on cyanobacteria but frequently fail to keep cyanobacterial dominance and bloom formation in check. Our study tested whether oligopeptide production, a common feature in many cyanobacteria, can be a defensive mechanism against chytrid parasitism. The study employed the cyanobacterial strain Planktothrix NIVA-CYA126/8 and its mutants with knockout mutations for microcystins, anabaenopeptins, and microviridins, major oligopeptide classes to be found in NIVA-CYA126/8. Four chytrid strains were used as parasite models. They are obligate parasites of Planktothrix and are unable to exploit alternative food sources. All chytrid strains were less virulent to the NIVA-CYA126/8 wild type than to at least one of its oligopeptide knockout mutants. One chytrid strain even failed to infect the wild type, while exhibiting considerable virulence to all mutants. It is therefore evident that producing microcystins, microviridins, and/or anabaenopeptins can reduce the virulence of chytrids to Planktothrix, thereby increasing the host's chance of survival. Microcystins and anabaenopeptins are nonribosomal oligopeptides, while microviridins are produced ribosomally, suggesting that Planktothrix resists chytrids by relying on metabolites that are produced via distinct biosynthetic pathways. Chytrids, on the other hand, can adapt to the oligopeptides produced by Planktothrix in different ways. This setting most likely results in an evolutionary arms race, which would probably lead to Planktothrix and chytrid population structures that closely resemble those actually found in nature. In summary, the findings of the present study suggest oligopeptide production in Planktothrix to be part of a defensive mechanism against chytrid parasitism.

SUBMITTER: Rohrlack T

PROVIDER: S-EPMC3623205 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Putative antiparasite defensive system involving ribosomal and nonribosomal oligopeptides in cyanobacteria of the genus Planktothrix.

Rohrlack Thomas T Christiansen Guntram G Kurmayer Rainer R

Applied and environmental microbiology 20130208 8

Parasitic chytrid fungi can inflict significant mortality on cyanobacteria but frequently fail to keep cyanobacterial dominance and bloom formation in check. Our study tested whether oligopeptide production, a common feature in many cyanobacteria, can be a defensive mechanism against chytrid parasitism. The study employed the cyanobacterial strain Planktothrix NIVA-CYA126/8 and its mutants with knockout mutations for microcystins, anabaenopeptins, and microviridins, major oligopeptide classes to ...[more]

PMID: 23396340

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Project description:BackgroundBloom-forming cyanobacteria cause toxic algae outbreaks in lakes and reservoirs. We aimed to explore and quantify mutation events occurring within the large mcy gene cluster (55 kbp) encoding microcystin (MC) biosynthesis that inactivate MC net production. For this purpose we developed a workflow to detect mutations in situ occurring anywhere within the large mcy gene cluster as amplified from one single filament of the red-pigmented cyanobacterium Planktothrix rubescens. From five lakes of the Alps eight hundred Planktothrix filaments were isolated and each individual filament was analyzed for mutations affecting the mcy genes.ResultsMutations inactivating MC synthesis were either through an insertion element ISPlr1 or the partial deletion of mcy genes. Neutral mutations not affecting MC biosynthesis occurred within two intergenic spacer regions, either through the insertion of a Holliday-junction resolvase RusA or ISPlr1. Altogether, the insertions affected a few mcy genes only and their location was correlated with regions similar to repetitive extragenic palindromic DNA sequences (REPs). Taking all of the filaments together, the mutations leading to the inactivation of MC synthesis were more rare (0.5-6.9%), when compared with the neutral mutations (7.5-20.6%). On a spatial-temporal scale the ratio of MC synthesis-inactivating vs. neutral mutations was variable, e.g., the filament abundance carrying partial deletion of mcyD (5.2-19.4%) and/or mcyHA (0-7.3%) exceeded the abundance of neutral mutations.ConclusionsIt is concluded that insertion events occurring within the Planktothrix mcy gene cluster are predictable due to their correlation with REPs. The frequency of occurrence of the REPs within the mcy gene cluster of Planktothrix relates to the rather common mutation of mcy genes in Planktothrix. Spatial-temporal variable conditions may favor the emergence of partial mcy deletion mutants in Planktothrix, in particular a higher proportion of genotypes resulting in inactivation of MC synthesis might be caused by increased ISPlr1 activity.

Project description:BACKGROUND: Cyanobacteria often produce several different oligopeptides, with unknown biological functions, by nonribosomal peptide synthetases (NRPS). Although some cyanobacterial NRPS gene cluster types are well described, the entire NRPS genomic content within a single cyanobacterial strain has never been investigated. Here we have combined a genome-wide analysis using massive parallel pyrosequencing ("454") and mass spectrometry screening of oligopeptides produced in the strain Planktothrix rubescens NIVA CYA 98 in order to identify all putative gene clusters for oligopeptides. RESULTS: Thirteen types of oligopeptides were uncovered by mass spectrometry (MS) analyses. Microcystin, cyanopeptolin and aeruginosin synthetases, highly similar to already characterized NRPS, were present in the genome. Two novel NRPS gene clusters were associated with production of anabaenopeptins and microginins, respectively. Sequence-depth of the genome and real-time PCR data revealed three copies of the microginin gene cluster. Since NRPS gene cluster candidates for microviridin and oscillatorin synthesis could not be found, putative (gene encoded) precursor peptide sequences to microviridin and oscillatorin were found in the genes mdnA and oscA, respectively. The genes flanking the microviridin and oscillatorin precursor genes encode putative modifying enzymes of the precursor oligopeptides. We therefore propose ribosomal pathways involving modifications and cyclisation for microviridin and oscillatorin. The microviridin, anabaenopeptin and cyanopeptolin gene clusters are situated in close proximity to each other, constituting an oligopeptide island. CONCLUSION: Altogether seven nonribosomal peptide synthetase (NRPS) gene clusters and two gene clusters putatively encoding ribosomal oligopeptide biosynthetic pathways were revealed. Our results demonstrate that whole genome shotgun sequencing combined with MS-directed determination of oligopeptides successfully can identify NRPS gene clusters and the corresponding oligopeptides. The analyses suggest independent evolution of all NRPS gene clusters as functional units. Our data indicate that the Planktothrix genome displays evolution of dual pathways (NRPS and ribosomal) for production of oligopeptides in order to maximize the diversity of oligopeptides with similar but functional discrete bioactivities.

Dataset Information

Putative antiparasite defensive system involving ribosomal and nonribosomal oligopeptides in cyanobacteria of the genus Planktothrix.

Publications

Putative antiparasite defensive system involving ribosomal and nonribosomal oligopeptides in cyanobacteria of the genus Planktothrix.

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