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

Abstract

The oldest species of bacteria capable of oxygenic photosynthesis today are the freshwater Cyanobacteria Gloeobacter spp., belonging to the class Oxyphotobacteria. Several modern molecular evolutionary studies support the freshwater origin of cyanobacteria during the Archaean and their subsequent acquisition of salt tolerance mechanisms necessary for their expansion into the marine environment. This study investigated the effect of a sudden washout event from a freshwater location into either a brackish or marine environment on the photosynthetic efficiency of two unicellular freshwater cyanobacteria: the salt‐tolerant Chroococcidiopsis thermalis PCC7203 and the cyanobacterial phylogenetic root species, Gloeobacter violaceus PCC7421. Strains were cultured under present atmospheric levels (PAL) of CO2 or an atmosphere containing elevated levels of CO2 and reduced O2 (eCO2rO2) in simulated shallow water or terrestrial environmental conditions. Both strains exhibited a reduction in growth rates and gross photosynthesis, accompanied by significant reductions in chlorophyll a content, in brackish water, with only C. thermalis able to grow at marine salinity levels. While the experimental atmosphere caused a significant increase in gross photosynthesis rates in both strains, it did not increase their growth rates, nor the amount of O2 released. The differences in growth responses to increasing salinities could be attributed to genetic differences, with C. thermalis carrying additional genes for trehalose synthesis. This study demonstrates that, if cyanobacteria did evolve in a freshwater environment, they would have been capable of withstanding a sudden washout into increasingly saline environments. Both C. thermalis and G. violaceus continued to grow and photosynthesise, albeit at diminished rates, in brackish water, thereby providing a route for the evolution of open ocean‐dwelling strains, necessary for the oxygenation of the Earth's atmosphere.

Cryo-EM Structure of a Tetrameric Photosystem I from Chroococcidiopsis TS-821, a Thermophilic, Non-heterocyst-forming Cyanobacteria

“…We and others have shown that the genus Chroococcidiopsis includes species with unique survival abilities under nitrogen-limiting conditions and can grow quite well in salt water (39). These authors speculated that Chroococcidiopsis was capable of surviving, following a sudden washout, into an increasingly saline environment, thereby providing a route for the evolution of open, oceandwelling cyanobacterial strains (40). Recently Sánchez-Baracaldo and colleagues proposed that closest relative of the chloroplast was an ancient freshwater cyanobacterium, Gloeomargarita.…”

Gloeobacter and the implications of a freshwater origin of Cyanobacteria

“…While experimental evolution has been applied to cyanobacteria, none of these studies have addressed variations in salinity (Leister 2018). The suggestion that the ability to synthesize trehalose is an indicator of salinity tolerance (Blank 2013a;Herrmann & Gehringer 2019) contrasts with an earlier suggestion in a literature review (Hagemann 2011). The review suggests that sucrose and trehalose occur in freshwater cyanobacteria, while glucosylglycerol and glucoosylglycerate are compatible solute osmoregulators in moderately halotolerant (marine) cyanobacteria, and that halophilic cyanobacteria are characterized by glycine betaine and glutamate betaine (Hagemann 2011).…”

“…Herrmann & Gehringer (2019) examined salinity tolerance of Gloeobacter violaceus and the later-evolving Chrococcidiopsis thermalis Geitler as an indicator of their potential to establish in estuarine and marine environments following washout from their typical low-salinity habitats. Both Gloeobacter and Chrococcidiopsis grew in brackish culture media, although more slowly than in freshwater; only Chrococcidiopsis grew at seawater salinities, probably related to its ability to synthesize the osmoregulant trehalose (Blank 2013a;Herrmann & Gehringer 2019). Growth periods were 12 days for Chrococcidiopsis and 24 days for Gloeobacter, so the experiment was not experimental evolution that requires many more generations, as used in experimental evolution studies of salinity adaptation using the freshwater chlorophycean microalga Chlamydomonas reinhardtii P.A.…”

Microbial helpers allow cyanobacteria to thrive in ferruginous waters

“…The emergence of oxygenic photosynthesis in cyanobacteria occurred in the Archean (Chisholm, 2017; Kendall et al., 2010; Konhauser et al., 2011; Lalonde & Konhauser, 2015; Lyons et al., 2014; Olson et al., 2013; Planavsky et al., 2014; Reinhard et al., 2013). The metabolic expansion of cyanobacteria before the GOE may reflect their transition from land to Fe 2+ ‐rich Archean oceans (Herrmann & Gehringer, 2019). This transition would have been physiologically challenging due to Fe 2+ toxicity from its reactions with reactive oxygen species (ROS) produced during photosynthesis (Swanner, Mloszewska, et al., 2015).…”