Adaptation of the Freshwater Bloom-Forming Cyanobacterium Microcystis aeruginosa to Brackish Water Is Driven by Recent Horizontal Transfer of Sucrose Genes

Abstract

Microcystis aeruginosa is a bloom-forming cyanobacterium found in eutrophic water bodies worldwide. M. aeruginosa blooms usually occur in freshwater; however, they have also been reported to occur in brackish water. Because M. aeruginosa often produces the cyanotoxin microcystin, they are a major concern to public health and environment. Despite this, the ecology, genomic basis, and evolutionary process underlying the M. aeruginosa bloom invasion from fresh to brackish water have been poorly investigated. Hence, in the present study, we have sequenced and characterized genomes of two newly discovered salt-tolerant M. aeruginosa strains obtained from Japanese brackish water lakes (Lakes Shinji and Tofutsu). Both genomes contain a set of genes for the synthesis of osmolyte sucrose (sppA, spsA, and susA), hitherto identified in only one strain (PCC 7806) of M. aeruginosa. Chemical and gene expression analyses confirmed sucrose accumulation induced by salt. A comprehensive genetic survey of >200 strains indicated that sucrose genes are extremely rare in M. aeruginosa. Most surprisingly, comparative genome analyses of the three strains indicated extremely low genetic diversity in the sucrose genes compared with other core genome genes, suggesting very recent acquisitions via horizontal transfer. Invasion of M. aeruginosa blooms into brackish water may be a recent event triggered by anthropogenic eutrophication of brackish water.

Adaptation of the toxic freshwater cyanobacterium Microcystis aeruginosa to salinity is achieved by the selection of spontaneous mutants

“…However, the presence of the genes responsible for sucrose synthesis is rare in M. aeruginosa strains (Tanabe et al . ), although the existence of these genes has been observed in two strains obtained from brackish waters (Sandrini et al . ; Tanabe et al .…”

“…), which could be a result of horizontal gene transfer (Tanabe et al . ). On the other hand, in a DNA microarray study made with Synechocystis strain 6803, 200–300 genes were upregulated by high‐salt conditions and a similar number were downregulated (Kanesaki et al .…”

“…Moreover, Tanabe et al . () recently suggested that horizontal gene transfer could modulate the appearance of genes that allow the synthesis of compatible solutes, and then contribute to a potential increase in salinity tolerance.…”

“…In the case of low salt-tolerant species like M. aeruginosa, the main compatible solutes are glucose and trehalose. However, the presence of the genes responsible for sucrose synthesis is rare in M. aeruginosa strains (Tanabe et al 2018), although the existence of these genes has been observed in two strains obtained from brackish waters (Sandrini et al 2015;Tanabe et al 2018), which could be a result of horizontal gene transfer (Tanabe et al 2018). On the other hand, in a DNA microarray study made with Synechocystis strain 6803, 200-300 genes were upregulated by highsalt conditions and a similar number were downregulated (Kanesaki et al 2002;Marin et al 2003Marin et al , 2004.…”

“…Therefore, taking into account that the experiments in this study were performed with single-celled culture inoculums, we would surely be underestimating the capacity of adaptation of the population in nature. Moreover, Tanabe et al (2018) recently suggested that horizontal gene transfer could modulate the appearance of genes that allow the synthesis of compatible solutes, and then contribute to a potential increase in salinity tolerance.…”