Nutrients drive transcriptional changes that maintain metabolic homeostasis but alter genome architecture in Microcystis

Abstract

The cyanobacterium Microcystis aeruginosa is a globally distributed bloom-forming organism that degrades freshwater systems around the world. Factors that drive its dispersion, diversification and success remain, however, poorly understood. To develop insight into cellular-level responses to nutrient drivers of eutrophication, RNA sequencing was coupled to a comprehensive metabolomics survey of M. aeruginosa sp. NIES 843 grown in various nutrient-reduced conditions. Transcriptomes were generated for cultures grown in nutrient-replete (with nitrate as the nitrogen (N) source), nitrogen-reduced (with nitrate, urea or ammonium acting as the N sources) and phosphate-reduced conditions. Extensive expression differences (up to 696 genes for urea-grown cells) relative to the control treatment were observed, demonstrating that the chemical variant of nitrogen available to cells affected transcriptional activity. Of particular note, a high number of transposase genes (up to 81) were significantly and reproducibly up-regulated relative to the control when grown on urea. Conversely, phosphorus (P) reduction resulted in a significant cessation in transcription of transposase genes, indicating that variation in nutrient chemistry may influence transcription of transposases and may impact the highly mosaic genomic architecture of M. aeruginosa. Corresponding metabolomes showed comparably few differences between treatments, suggesting broad changes to gene transcription are required to maintain metabolic homeostasis under nutrient reduction. The combined observations provide novel and extensive insight into the complex cellular interactions that take place in this important bloom-forming organism during variable nutrient conditions and highlight a potential unknown molecular mechanism that may drive Microcystis blooms and evolution.

Chemically mediated interactions between Microcystis and Planktothrix: impact on their growth, morphology and metabolic profiles

“…Simultaneously, transcriptome‐based characterization of interactions between co‐occurring organisms would contribute to the current knowledge about the molecular mechanisms involved in the intraspecies and interspecies cyanobacterial interactions. Regulatory molecular mechanisms, such as activity of transposable elements, enabling cells to face various environmental conditions, like N availability (Steffen et al ., ) and grazing (Harke et al ., ), may facilitate adaptability through the regulation of the production of metabolites.…”

Microbial metaproteomics for characterizing the range of metabolic functions and activities of human gut microbiota

“…Collectively, they comprise the central foundation of the current molecular biology paradigm: genes (DNA) for genetic information storage, transcription (mRNA) for gene expression, proteins for structural and metabolic/enzymatic activities, and metabolites for the substrates/inhibitors/products of metabolism. Recent advances in ‐omics technologies have facilitated their application to microbial consortia/communities, which have been designated as metagenomics , metatranscriptomics , metaproteomics , and meta‐metabolomics . Even a brief inspection of scientific literature over the past 10 years will clearly reveal how these ‐omics technologies have revolutionized microbial ecology.…”

Advances in genomics, transcriptomics and proteomics of toxin‐producing cyanobacteria

“…In comparison, studies that have tried to pin down nutrient availabilities, such as for nitrogen and other distinct environmental conditions to the level of microcystin production, have resulted in controversial results. A steady expression independent of nitrate availability as seen by Sevilla and colleagues () was contradicted by the downregulation of mcy under nitrate limitation in other studies (Harke and Gobler, ; Steffen et al ., ). Apart from contradictory mcy expression patterns in these studies, the comprehensive transcriptomic investigations of Steffen and colleagues () were able to uncover unforeseen correlations between nitrogen availability and potential genomic reorganization via the activation of transposases and insertion sequences.…”

“…A steady expression independent of nitrate availability as seen by Sevilla and colleagues () was contradicted by the downregulation of mcy under nitrate limitation in other studies (Harke and Gobler, ; Steffen et al ., ). Apart from contradictory mcy expression patterns in these studies, the comprehensive transcriptomic investigations of Steffen and colleagues () were able to uncover unforeseen correlations between nitrogen availability and potential genomic reorganization via the activation of transposases and insertion sequences. Thus, they proposed the concept of nutrients as evolutionary drivers for the formation of subspecies, with the microcystin gene cluster as a top candidate for genomic mobilization under nitrogen‐reduced conditions.…”

“…This suggests a significant selective pressure to maintain a functional form of the cluster or to rapidly eject dysfunctional forms that arise, potentially through the action of co-localized transposases. Indeed, the alteration of nutrient concentrations that elicit transposase expression in Microcystis, also leads to an alternate genomic architecture (Steffen et al, 2014). This raises the question as to the extent to which re-arrangements can occur within the gene cluster before the organism deems these pathways redundant.…”