Coordinated Diel Gene Expression of Cyanobacteria and Their Microbiome.

Kai Wang,Xiaozhen Mou

doi:10.3390/microorganisms9081670

Abstract

Diel rhythms have been well recognized in cyanobacterial metabolisms. However, whether this programmed activity of cyanobacteria could elicit coordinated diel gene expressions in microorganisms (microbiome) that co-occur with cyanobacteria and how such responses in turn impact cyanobacterial metabolism are unknown. To address these questions, a microcosm experiment was set up using Lake Erie water to compare the metatranscriptomic variations of Microcystis cells alone, the microbiome alone, and these two together (whole water) over two day-night cycles. A total of 1205 Microcystis genes and 4779 microbiome genes exhibited significant diel expression patterns in the whole-water microcosm. However, when Microcystis and the microbiome were separated, only 515 Microcystis genes showed diel expression patterns. A significant structural change was not observed for the microbiome communities between the whole-water and microbiome microcosms. Correlation analyses further showed that diel expressions of carbon, nitrogen, phosphorous, and micronutrient (iron and vitamin B12) metabolizing genes were significantly coordinated between Microcystis and the microbiome in the whole-water microcosm. Our results suggest that diel fluxes of organic carbon and vitamin B12 (cobalamin) in Microcystis could cause the diel expression of microbiome genes. Meanwhile, the microbiome communities may support the growth of Microcystis by supplying them with recycled nutrients, but compete with Microcystis for iron.

Highlights

Cyanobacteria are a group of oxygenic photosynthetic prokaryotes; they possess many adaptive strategies, which give them competitive advantages over other primary producers in aquatic environments [1]
Our results suggest that diel fluxes of organic carbon and vitamin B12 in Microcystis could cause the diel expression of microbiome genes
This work provides one of the first empirical studies to support the hypothesis that the diel metabolic activities in Microcystis could elicit a coordinated diel expression in its microbiome [35]

Summary

Introduction

Cyanobacteria are a group of oxygenic photosynthetic prokaryotes; they possess many adaptive strategies, which give them competitive advantages over other primary producers in aquatic environments [1] One of such critical adaptations is their temporal partitioning of cellular metabolisms according to daily fluctuations of light [2], i.e., performing lightdependent and energy-consuming biosynthesis (anabolism) mainly during the daytime and generating energy by breaking down synthesized organic molecules (catabolism) mainly at night [3]. Some co-occurring bacteria are attached to cyanobacterial cells [8,9], whereas others are free-living [10] The activities of these cyanobacterial microbiome species can impact the function and structures of cyanobacterial communities [11]. While the diel expression of genes is well recognized for cyanobacteria [2,5], the role of the cyanobacterial microbiome in this process remains largely unknown

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