Freshwater Cyanobacterium Synechococcus elongatus PCC 7942 Adapts to an Environment with Salt Stress via Ion-Induced Enzymatic Balance of Compatible Solutes

Abstract

Salinity is one of the most important abiotic factors in various natural habitats of microbes. Cyanobacteria are the most widely distributed family of photosynthetic microorganisms in environments with fluctuating salinity. In response to salt stress, many cyanobacteria de novo synthesize compatible solutes to maintain osmotic balance in the cell. However, the regulation of intracellular accumulation of these compounds is still not well understood. The freshwater cyanobacterium Synechococcus elongatus PCC 7942 (Syn7942) exclusively accumulates sucrose as a compatible solute upon salt stress and is thus an ideal model microorganism for studying the metabolism of compatible solute dynamics. Here, we focused on elucidating the regulatory mechanisms involved in salt-induced sucrose accumulation in Syn7942. Using a series of physiological and biochemical experiments, we showed that the ionic effect of salt stress plays an important role in inducing sucrose synthesis, whereby elevated ion concentration directly activates the sucrose-synthesizing enzyme sucrose-phosphate synthase and simultaneously inhibits the sucrose-degrading enzyme invertase, resulting in a rapid sucrose accumulation. Thus, we propose a novel mechanism for cyanobacterial adaption to salt stress and fluctuating salinity, i.e., the ion-induced synergistic modulation of the enzymes synthesizing and degrading compatible solutes. These findings greatly enhance our current understanding of microbial adaptation to salt. IMPORTANCE Most microbes de novo synthesize compatible solutes for adaptation to salt stress or fluctuating salinity environments. However, to date, one of the core questions involved in these physiological processes, i.e., the regulation of salt-induced compatible solute biosynthesis, is still not well understood. Here, this issue was systematically investigated by employing the model freshwater cyanobacterium Synechococcus elongatus PCC 7942. A novel mechanism for cyanobacterial adaption to salt stress and fluctuating salinity, i.e., the ion-induced synergistic modulation of key synthesizing and degrading enzymes of compatible solutes, is proposed. Because the ion-induced activation/inhibition of enzymes is a fast and efficient process, it may represent a common strategy of microbes for adaptation to environments with fluctuating salinity.

Genome Streamlining, Plasticity, and Metabolic Versatility Distinguish Co-occurring Toxic and Nontoxic Cyanobacterial Strains of Microcoleus

“…7 ). Sucrose serves as one of the major compatible solutes among cyanobacteria in freshwater habitats, and the intracellular accumulation of sucrose helps cyanobacteria cope with salt stress ( 76 – 78 ). Missing genes related to sucrose synthesis suggest that toxic strains may be less tolerant to salt stress, possibly due to expendable gene loss, as they exclusively inhabit freshwater environments ( 12 ) and thus encounter minimum fluctuations in salinity.…”

Manipulating the Expression of Glycogen Phosphorylase in Synechococcus elongatus PCC 7942 to Mobilize Glycogen Storage for Sucrose Synthesis

“…Based on the effects of theophylline-induced glgP expression on glycogen storage and sucrose synthesis in XC14 facing salt stress, we supposed that this strategy might more possibly be valuable in non-hypersaline conditions to link the glycogen degradation metabolism and synthesis of desired metabolites. As for PCC 7942, sucrose synthesis would be activated through salt ion-induced activation of sucrose phosphate synthase and inhibition of invertase (Liang et al, 2020), while it has been confirmed that Sps from PCC 6803 (hereafter termed as Sps 6803 for short) was not a salt-activated enzyme, and introduction of the Sps 6803 in the another Synechococcus strain UTEX 2973 successfully resulted in a secretory synthesis of sucrose without the need for salt stress induction (Lin et al, 2020). We took the same strategy to construct a PCC 7942-derived cell factory producing sucrose under non-hypersaline conditions by overexpressing Sps 6803 in the FL92 strain which was previously FIGURE 5 | Effects of theophylline-induced glgP overexpression on salt-induced sucrose synthesis and secretion in PCC 7942 cell factories.…”

Assessment of Synechococcus elongatus PCC 7942 as an option for sustainable wastewater treatment

“…It is triggered by the natural reaction of S7942 to osmotic changes due to salinization of the environment via increased sucrose levels in the cytoplasm, regulating the inner-cell turgor pressure (Vayenos et al 2020). Worth mention is that S7942 is able to tolerate maximally salinity of approximately 0.5 M NaCl (Ladas & Papageorgiou 2000;Du et al 2013), a salinity (2.9%) lower than that of seawater (3.5%) (Liang et al 2020). The high tolerance of S7942 in relative saline conditions and the increase of its sucrose levels renders this specific strain an excellent candidate towards eco-friendly and resource/energy recovering treatment of industrial wastewaters.…”