Abstract
Understanding how microorganisms adjust their metabolism to maintain their ability to cope with short-term environmental variations constitutes one of the major current challenges in microbial ecology. Here, the best physiologically characterized marine Synechococcus strain, WH7803, was exposed to modulated light/dark cycles or acclimated to continuous high-light (HL) or low-light (LL), then shifted to various stress conditions, including low (LT) or high temperature (HT), HL and ultraviolet (UV) radiations. Physiological responses were analyzed by measuring time courses of photosystem (PS) II quantum yield, PSII repair rate, pigment ratios and global changes in gene expression. Previously published membrane lipid composition were also used for correlation analyses. These data revealed that cells previously acclimated to HL are better prepared than LL-acclimated cells to sustain an additional light or UV stress, but not a LT stress. Indeed, LT seems to induce a synergic effect with the HL treatment, as previously observed with oxidative stress. While all tested shift conditions induced the downregulation of many photosynthetic genes, notably those encoding PSI, cytochrome b6/f and phycobilisomes, UV stress proved to be more deleterious for PSII than the other treatments, and full recovery of damaged PSII from UV stress seemed to involve the neo-synthesis of a fairly large number of PSII subunits and not just the reassembly of pre-existing subunits after D1 replacement. In contrast, genes involved in glycogen degradation and carotenoid biosynthesis pathways were more particularly upregulated in response to LT. Altogether, these experiments allowed us to identify responses common to all stresses and those more specific to a given stress, thus highlighting genes potentially involved in niche acclimation of a key member of marine ecosystems. Our data also revealed important specific features of the stress responses compared to model freshwater cyanobacteria.
Highlights
All microorganisms are constrained to adjust their metabolism in order to maintain their ability to survive in constantly changing environments
Most genes were found to respond to a subset of the tested conditions (Supplementary Figure S5), with the most stressful treatments (LLHL, LLUV, LLLT, and HLLT) notably triggering a strong induction of numerous chaperone- and protease-encoding genes and of the psbA gene copies encoding the D1:2 isoform of the D1 protein, while most genes involved in the neosynthesis of PSII were in contrast downregulated
This includes genes coding for NADH dehydrogenase subunits involved in CO2 fixation and cyclic electron transport around PSI, some genes of the glycogen degradation pathway, as well as betP encoding a component of the glycine betaine uptake system
Summary
All microorganisms are constrained to adjust their metabolism in order to maintain their ability to survive in constantly changing environments. Bacteria possess numerous mechanisms that enable acclimation to the variety of possible external stresses (Schimel et al, 2007) These range from up or downregulation of a single metabolic process to the activation of complex gene expression networks, e.g., through regulation by two-component sensory systems that translate extracellular signals into intracellular responses (Suzuki et al, 2001; Los et al, 2010). In this context, comparing global gene expression profiles on laboratory strains submitted to different individual stresses and for which conditions can be perfectly controlled, allows to uncover stress-specific global transcriptional responses and to shed light on novel or unsuspected cellular stress responses
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