Phylogenetic distribution of compatible solute synthesis genes support a freshwater origin for cyanobacteria

Abstract

Previous work using ancestral state reconstruction of habitat salinity preference proposed that the early cyanobacteria likely lived in a freshwater environment. The aim of this study was to test that hypothesis by performing phylogenetic analyses of the genes underlying salinity preferences in the cyanobacteria. Phylogenetic analysis of compatible solute genes shows that sucrose synthesis genes were likely ancestral in the cyanobacteria, and were also likely inherited during the cyanobacterial endosymbiosis and into the photosynthetic algae and land plants. In addition, the genes for the synthesis of compatible solutes that are necessary for survival in marine and hypersaline environments (such as glucosylglycerol, glucosylglycerate, and glycine betaine) were likely acquired independently high up (i.e., more recently) in the cyanobacterial tree. Because sucrose synthesis is strongly associated with growth in a low salinity environment, this independently supports a freshwater origin for the cyanobacteria. It is also consistent with geologic evidence showing that the early oceans were much warmer and saltier than modern oceans-sucrose synthesis alone would have been insufficient for early cyanobacteria to have colonized early Precambrian oceans that had a higher ionic strength. Indeed, the acquisition of an expanded set of new compatible solute genes may have enabled the historical colonization of marine and hypersaline environments by cyanobacteria, midway through their evolutionary history.

An investigation into the effects of increasing salinity on photosynthesis in freshwater unicellular cyanobacteria during the late Archaean

“…Our study supports the hypothesis of cyanobacterial evolution in freshwater environments and their transition into brackish or marine saline environments (Blank, ; Sánchez‐Baracaldo, ; Sánchez‐Baracaldo, Raven, et al., ; Sánchez‐Baracaldo, Bianchini, et al., ) as illustrated in Figure . The evolution of cyanobacteria in a freshwater environment would have allowed the formation of loose microbial mats on solid substrates along the edges of the water body.…”

“…Tria, Landan, and Dagan () utilised a novel phylogenetic rooting approach to genomic sequence analysis that suggested cyanobacteria evolved in the ocean. Phylogenetic approaches involving analysis of present‐day cyanobacterial genetic sequences, using established calibration points (Sánchez‐Baracaldo, Bianchini, et al., ; Sánchez‐Baracaldo, Raven, Pisani, & Knoll, ; Sánchez‐Baracaldo, Ridgwell, & Raven, ; Uyeda, Harmon, & Bank, ), and compatible solute gene distribution (Blank, ) suggest that early cyanobacteria lived in freshwater environments and gradually evolved to occupy higher salinity environments. The ensuing debate regarding the methodologies employed (Nakov, Boyko, Alverson, & Beaulieu, ; Sánchez‐Baracaldo, Bianchini, et al., ) clearly highlighted the need for experiments to investigate the mechanisms behind the genetic pathways for “salt tolerance” to better understand the evolution of cyanobacterial ecological preferences, particularly during the late Archaean.…”

“…Other strategies to overcome UV exposure would have been to grow in shaded areas under rocks (Nürnberg et al., ), in caves (Saw et al., ) or benthically (Heubeck et al., ; Homann et al., ). Salt tolerance would have been necessary for oxygenic phototrophs living in marine and brackish environments (Blank, ).…”

Origin and early evolution of photosynthetic eukaryotes in freshwater environments: reinterpreting proterozoic paleobiology and biogeochemical processes in light of trait evolution

“…S9 and S10 in the Supporting Information). This hypothesis is supported by the phylogenetic distribution of compatible solute synthesis genes in the Cyanobacteria and photosynthetic eukaryotes, and in the phylogenetic distribution of contractile vacuoles in the photosynthetic eukaryotes (Blank , in review).…”

“…Our analyses suggest that the plastid endosymbiosis occurred at a time when the Cyanobacteria were unicellular and restricted to freshwater ecosystems. The ancestry of Cyanobacteria and photosynthetic eukaryotes in freshwater was further supported by phylogenetic analysis of compatible solute genes and contractile vacuoles in the photosynthetic eukaryotes (Blank ). The chloroplast ancestor likely emerged in freshwater environments, in the early Paleoproterozoic, and the early plastid diversifications likely also occurred in freshwater environments up through the middle Mesoproterozoic.…”