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 compatible solute upon salt stress, and is thereby an ideal model microorganism to study the metabolism of compatible solute dynamics. Here, we focused on elucidating the regulatory mechanisms involved in salt-induced sucrose accumulation of 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 develop our current understandings on microbial adaptation to salt.

IMPORTANCE Most of microbes de novo synthesize compatible solutes for the adaption 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 employing a 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 progress, it may represent a common strategy of microbes for the adaption to the fluctuating salinity environments.

盐度是微生物在各种自然栖息地中最重要的非生物因素之一。蓝细菌是盐度波动的环境中分布最广泛的光合微生物家族。响应盐胁迫，许多从头开始的蓝细菌可以合成兼容的溶质以维持细胞中的渗透平衡。然而，对这些化合物的细胞内积累的调节仍不十分了解。淡水蓝藻伸长菌PCC 7942（Syn7942）在盐胁迫下专门累积蔗糖作为相容性溶质，因此是研究相容性溶质动力学代谢的理想模型微生物。在这里，我们集中于阐明参与盐诱导的Syn7942蔗糖积累的调控机制。通过一系列生理和生化实验，我们发现盐胁迫的离子效应在诱导蔗糖合成中起着重要作用，其中升高的离子浓度直接激活了蔗糖合成酶蔗糖磷酸合成酶，同时抑制了蔗糖降解酶转化酶，导致蔗糖迅速积累。因此，我们提出了一种蓝藻适应盐胁迫和盐度波动的新机制，即 离子诱导的酶的协同调制，合成和降解相容性溶质。这些发现极大地发展了我们目前对微生物对盐的适应性的认识。

重要多数微生物从头开始合成兼容的溶质，以适应盐胁迫或波动的盐度环境。然而，迄今为止，这些生理过程中涉及的核心问题之一，即盐诱导的相容性溶质生物合成的调控仍未得到很好的理解。在这里，使用模型淡水蓝藻长棘突球菌进行了系统地调查PCC7942。提出了一种蓝藻适应盐胁迫和盐度波动的新机制，即离子诱导的相容性溶质关键合成酶和降解酶的协同调节。由于离子诱导的酶的激活/抑制是一项快速而有效的进步，因此它可能代表了微生物适应变化的盐度环境的常见策略。