Transcriptomics-Aided Dissection of the Intracellular and Extracellular Roles of Microcystin in Microcystis aeruginosa PCC 7806

Abstract

e Recent studies have provided evidence for both intracellular and extracellular roles of the potent hepatotoxin microcystin (MC) in the bloom-forming cyanobacterium Microcystis. Here, we surveyed transcriptomes of the wild-type strain M. aeruginosa PCC 7806 and the microcystin-deficient ⌬mcyB mutant under low light conditions with and without the addition of external MC of the LR variant (MC-LR). Transcriptomic data acquired by microarray and quantitative PCR revealed substantial differences in the relative expression of genes of the central intermediary metabolism, photosynthesis, and energy metabolism. In particular, the data provide evidence for a lower photosystem I (PSI)-to-photosystem II (PSII) ratio and a more pronounced carbon limitation in the microcystin-deficient mutant. Interestingly, only 6% of the transcriptional differences could be complemented by external microcystin-LR addition. This MC signaling effect was seen exclusively for genes of the secondary metabolism category. The orphan polyketide synthase gene cluster IPF38-51 was specifically downregulated in response to external MC-LR under low light. Our data suggest a hierarchical and light-dependent cross talk of secondary metabolites and support both an intracellular and an extracellular role of MC in Microcystis.C yanobacteria of the genus Microcystis frequently occur as thick surface scums in freshwater lakes during summer (1). While these blooms are unpleasant, both visually and due to the presence of odors, a more serious problem is caused by their regular production of the potent hepatotoxin microcystin (MC) (2). Increasing eutrophication caused by urban and industrial developments, as well as global warming, is expected to amplify the severity of the problem (3). Microcystis cells are organized into colonies of diverse shapes (4) and possess constitutively present gas vesicles (5). Both features enable vertical migration in the water column, a phenomenon widely discussed as a competitive advantage over other phytoplankton species (6). Toxic genotypes commonly constitute only a subfraction within Microcystis communities present in blooms. The proportion of toxic and nontoxic genotypes, however, is dynamically changing, and the factors underlying these variations are not well understood (7).In this respect, much research has been focused on deciphering the function and physiological role of microcystin in the MCproducing cyanobacteria (8). Microcystin is known to irreversibly inhibit eukaryotic protein phosphatases of types 1 and 2A (9). Indeed, some grazers and parasites have been shown to be sensitive to the toxin (10, 11). Nevertheless, a primary defense function of microcystin is increasingly questioned. One of the strongest arguments against this comes from an evolutionary analysis of the microcystin biosynthesis (mcy) genes that unambiguously showed that the corresponding genes already were present in the last common ancestor of all present cyanobacteria, long before the appearance of the first eukaryotic grazer (12). Numerous alte...

Influence of temperature, mixing, and addition of microcystin-LR on microcystin gene expression inMicrocystis aeruginosa

“…These findings are in agreement with results from Makower et al. (), where the authors found a nonsignificant upregulation of mcyA gene when adding 50 μg L −1 microcystin‐LR.…”

Contribution of the A. baumannii A1S_0114 Gene to the Interaction with Eukaryotic Cells and Virulence

“…Glutathione conjugation most commonly occurs via a nucleophilic attack by the glutathione cysteinyl thiol on an electrophilic carbon such as a lactone or epoxide (Wang and Ballatori, 1998). The γ-glutamyl residue can then be cleaved by a γ-glutamyl transpeptidase localized outside the plasma membrane, leaving the conjugated Cys-Gly, as occurs in the case of the glutathione-modified microcystin (Schmidt et al, 2014), a cyanobacteria toxin and intra- and extra-cellular signaling molecule (Makower et al, 2015). …”

Growth, toxin production, active oxygen species and catalase activity of Microcystis aeruginosa (Cyanophyceae) exposed to temperature stress

“…As more evidence supporting the role of MC related to oxidative stress, several studies showed an increased sensitivity of MC-deficient mutants under high light and oxidative stress conditions (Zilliges et al, 2011;Meissner et al, 2015;Makower et al, 2015). In addition, Briand et al (2008) observed a decrease in MC cell quota in the late exponential growth phase.…”