Episodic Decrease in Temperature Increases mcy Gene Transcription and Cellular Microcystin in Continuous Cultures of Microcystis aeruginosa PCC 7806.

Robbie M Martin,Ameet Pinto,Bofan Wei,Gwendolyn F Stark,Ferdi L Hellweger,Steven W Wilhelm,Eric R Gann,Dominique S Derminio,Gregory L Boyer,Mohammad Moniruzzaman

doi:10.3389/fmicb.2020.601864

Abstract

Microcystins produced during harmful cyanobacterial blooms are a public health concern. Although patterns are emerging, the environmental cues that stimulate production of microcystin remain confusing, hindering our ability to predict fluctuations in bloom toxicity. In earlier work, growth at cool temperatures relative to optimum (18°C vs. 26°C) was confirmed to increase microcystin quota in batch cultures of Microcystis aeruginosa NIES-843. Here, we tested this response in M. aeruginosa PCC 7806 using continuous cultures to examine temporal dynamics and using RNA-sequencing to investigate the physiological nature of the response. A temperature reduction from 26 to 19°C increased microcystin quota ∼2-fold, from an average of ∼464 ag μm–3 cell volume to ∼891 ag μm–3 over a 7–9 d period. Reverting the temperature to 26°C returned the cellular microcystin quota to ∼489 ag μm–3. Long periods (31–42 d) at 19°C did not increase or decrease microcystin quota beyond that observed at 7–9 d. Nitrogen concentration had little effect on the overall response. RNA sequencing indicated that the decrease in temperature to 19°C induced a classic cold-stress response in M. aeruginosa PCC 7806, but this operated on a different timescale than the increased microcystin production. Microcystin quota showed a strong 48- to 72-h time-lag correlation to mcy gene expression, but no correlation to concurrent mcy expression. This work confirms an effect of temperature on microcystin quota and extends our understanding of the physiological nature of the response.

Highlights

Cyanobacterial blooms plague fresh waters across the globe
We demonstrate, using continuous cultures, that an episodic decrease in temperature increases microcystin production in M. aeruginosa PCC 7806 and that this production reverts to previous rates with a return of temperature
With this long-term goal in mind, our objective here was to extend our understanding of how changes in the fundamental parameter of temperature affect the production of microcystin and the resulting quota

Summary

Introduction

Cyanobacterial blooms plague fresh waters across the globe. A recent study confirmed that bloom frequency and duration have increased over the past three decades, a pattern long suspected (Ho et al, 2019). While the physiological function of microcystin continues to be debated (Omidi et al, 2018), there is growing evidence that microcystin plays a role in moderating damage from oxidative stress by protecting key proteins involved in photosynthesis and carbon fixation (Zilliges et al, 2011; Wei et al, 2016). This picture is complicated by reports that microcystins can interfere with the ability of Microcystis to cope with externally induced oxidative stress (Schuurmans et al, 2018). These seemingly inconsistent results suggest a complexity in the function of microcystin that is yet to be fully revealed (Barchewitz et al, 2019)

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Results

Conclusion