Awakening of a Dormant Cyanobacterium from Nitrogen Chlorosis Reveals a Genetically Determined Program

The molecular and physiological mechanisms involved in the transition of microbial cells from a resting state to the active vegetative state are critically relevant for solving problems in fields ranging from microbial ecology to infection microbiology. Cyanobacteria that cannot fix nitrogen are abl...

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Published in:Current biology 2016-11, Vol.26 (21), p.2862-2872
Main Authors: Klotz, Alexander, Georg, Jens, Bučinská, Lenka, Watanabe, Satoru, Reimann, Viktoria, Januszewski, Witold, Sobotka, Roman, Jendrossek, Dieter, Hess, Wolfgang R., Forchhammer, Karl
Format: Article
Language:English
Subjects:
chlorophyll biosynthesis
dormancy
Gene Expression Regulation, Bacterial
glycogen
nitrate assimilation
Nitrogen - metabolism
non-coding RNA
polyhydroxybutyrate
polyploidy
RNA, Bacterial - metabolism
RNA, Untranslated - metabolism
RuBisCO
starvation
synechocystis
Synechocystis - genetics
Synechocystis - physiology
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Summary:The molecular and physiological mechanisms involved in the transition of microbial cells from a resting state to the active vegetative state are critically relevant for solving problems in fields ranging from microbial ecology to infection microbiology. Cyanobacteria that cannot fix nitrogen are able to survive prolonged periods of nitrogen starvation as chlorotic cells in a dormant state. When provided with a usable nitrogen source, these cells re-green within 48 hr and return to vegetative growth. Here we investigated the resuscitation of chlorotic Synechocystis sp. PCC 6803 cells at the physiological and molecular levels with the aim of understanding the awakening process of a dormant bacterium. Almost immediately upon nitrate addition, the cells initiated a highly organized resuscitation program. In the first phase, they suppressed any residual photosynthetic activity and activated respiration to gain energy from glycogen catabolism. Concomitantly, they restored the entire translational apparatus, ATP synthesis, and nitrate assimilation. After only 12–16 hr, the cells re-activated the synthesis of the photosynthetic apparatus and prepared for metabolic re-wiring toward photosynthesis. When the cells reached full photosynthetic capacity after ∼48 hr, they resumed cell division and entered the vegetative cell cycle. An analysis of the transcriptional dynamics during the resuscitation process revealed a perfect match to the observed physiological processes, and it suggested that non-coding RNAs play a major regulatory role during the lifestyle switch in awakening cells. This genetically encoded program ensures rapid colonization of habitats in which nitrogen starvation imposes a recurring growth limitation. [Display omitted] •Awakening from nitrogen chlorosis is induced immediately upon the addition of nitrate•Cells activate respiration/restore translational apparatus before photosynthesis begins•Genes for major cellular processes are regulated in a highly orchestrated manner•Microarray analysis reveals a major impact of regulatory RNAs Klotz et al. present a detailed analysis of the cellular events during the awakening of a dormant bacterium. Resuscitation of a cyanobacterium from nitrogen chlorosis back to photosynthetically active life reveals a highly orchestrated program, with wide-ranging implications for our understanding of bacterial persistence and cellular aging.
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2016.08.054