Physiological and Metabolic Responses of Freshwater and Brackish-Water Strains of Microcystis aeruginosa Acclimated to a Salinity Gradient: Insight into Salt Tolerance

Abstract

Proliferation of microcystin (MC)-producing Microcystis aeruginosa in brackish waters has been described in several locations and represents a new concern for public and environmental health. While the impact of a sudden salinity increase on M. aeruginosa physiology has been studied, less is known about the mechanisms involved in salt tolerance after acclimation. This study aims to compare the physiological responses of two strains of M. aeruginosa (PCC 7820 and PCC 7806), which were isolated from contrasted environments, to increasing salinities. After acclimation, growth and MC production rates were determined and metabolomic analyses were conducted. For both strains, salinity decreased the biovolume, growth, and MC production rates and induced the accumulation of polyunsaturated lipids identified as monogalactosyldiacylglycerol. The distinct salt tolerances (7.5 and 16.9) obtained between the freshwater (PCC 7820) and the brackish-water (PCC 7806) strains suggested different strategies to cope with the osmotic pressure, as revealed by targeted and untargeted metabolomic analyses. An accumulation of trehalose as the main compatible solute was obtained in the freshwater strain, while sucrose was mainly accumulated in the brackish one. Moreover, distinct levels of glycine betaine and proline accumulation were noted. Altogether, metabolomic analysis illustrated a strain-specific response to salt tolerance, involving compatible solute production. IMPORTANCE Blooms of Microcystis aeruginosa and the production of microcystins are major issues in eutrophic freshwater bodies. Recently, an increasing number of proliferations of M. aeruginosa in brackish water has been documented. The occurrence of both M. aeruginosa and microcystins in coastal areas represents a new threat for human and environmental health. In order to better describe the mechanisms involved in Microcystis sp. proliferation in brackish water, this study used two M. aeruginosa strains isolated from fresh and brackish waters. High salinity reduced the growth rate and microcystin production rate of M. aeruginosa. In order to cope with higher salinities, the strains accumulated different cyanobacterial compatible solutes, as well as unsaturated lipids, explaining their distinct salt tolerance.

Salt Shock Responses of Microcystis Revealed through Physiological, Transcript, and Metabolomic Analyses

“…The strain PCC 7806 exhibited a higher salt tolerance (up to 8.4) with no negative growth rate at higher salinity conditions. Hence, as previously observed, these two strains exhibited distinct salt tolerances, with the freshwater PCC 7820 strain less tolerant compared to the brackish PCC 7806 one [30].…”

“…Interestingly, sucrose is not only accumulated in M. aeruginosa as a response to salt shock. Indeed, it also constitutes a long-term response in salt-tolerant strains as a key metabolite during salt variation [18,30]. Despite the fact that trehalose was identified in M. aeruginosa PCC 7820, it was not significantly accumulated in response to salt stress contrary to what we previously found with acclimated cultures [30].…”

“…After the report of glucosylglycerol accumulation [37], sucrose was identified in the particularly salt-tolerant M. aeruginosa strain PCC 7806 [38] and further confirmed in the field where the occurrence of the "sucrose" gene was correlated with the brackish origin of M. aeruginosa [18]. Hence, the accumulation of several compatible solutes could explain the differences in salt tolerance among M. aeruginosa strains [18,30,39].…”

“…Subsequently, several studies showed that the growth rate of Microcystis remained unaffected by salt addition up to a salinity of 10 [26,27]. Based on field and laboratory experiments, M. aeruginosa salt tolerance now ranges between 0 and 18 [27][28][29][30][31]. Salinity variation may affect cyanobacteria physiology through osmotic and ionic stresses, thus disturbing the cellular osmotic balance [32].…”

The limit of resistance to salinity in the freshwater cyanobacterium Microcystis aeruginosa is modulated by the rate of salinity increase

“…Recently, Tanabe, Hodoki, Sano, Tada, and Watanabe (2018), Tanabe, Yamaguchi, Sano, and Kawachi (2019) showed that some genes involved in the synthesis of sucrose could be responsible for the salinity resistance of M. aeruginosa strains from brackish waters and that their presence could be related with horizontal gene transfer (HGT). Moreover, Des Aulnois et al (2019) also identified an accumulation of trehalose in freshwater strains grown in high salinity, concluding that the use of one or other solute to maintain osmotic equilibrium could be one of the causes of the difference in salt tolerance of M. aeruginosa strains, as well as horizontal gene transfer events. Clearly, more studies to explore the limit of resistance of different M. aeruginosa strains isolated from water bodies with diverse salinity levels are still necessary.…”