Adaptation dynamics and evolutionary rescue under sulfide selection in cyanobacteria: a comparative study between Microcystis aeruginosa and Oscillatoria sp. (cyanobacteria)

Abstract

Experimental evolution studies using cyanobacteria as model organisms are scarce despite the role of cyanobacteria in the evolution of photosynthesis. Three different experimental evolution approaches have been applied to shed light on the sulfide adaptation process, which played a key role in the evolution of this group. We used a Microcystis aeruginosa sulfide‐sensitive strain, unable to grow above ~0.1 mM, and an Oscillatoria sp. strain, isolated from a sulfureous spa (~0.2 mM total sulfide). First, performing a fluctuation analysis design using the spa waters as selective agent, we proved that M. aeruginosa was able to adapt to this sulfide level by rare spontaneous mutations. Second, applying a ratchet protocol, we tested if the limit of adaptation to sulfide of the two taxa was dependent on their initial sulfide tolerance, finding that M. aeruginosa adapted to 0.4 mM sulfide, and Oscillatoria sp. to ~2 mM sulfide, twice it highest tolerance level. Third, using an evolutionary rescue approach, we observed that both speed of exposure to increasing sulfide concentrations (deterioration rate) and populations’ genetic variation determined the survival of M. aeruginosa at lethal sulfide levels, with a higher dependence on genetic diversity. In conclusion, sulfide adaptation of sensitive cyanobacterial strains is possible by rare spontaneous mutations and the adaptation limits depend on the sulfide level present in strain’s original habitat. The high genetic diversity of a sulfide‐sensitive strain, even at fast environmental deterioration rates, could increase its possibility of survival even to a severe sulfide stress.

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

“…Therefore, it was assumed that the strains had no previous evolutionary history of salinity exposure. Culture conditions were similar to those described in our previous studies (Bañares‐España et al, 2016, Carrillo et al, 2003; Costas et al, 2007; Fernández‐Arjona et al, 2013; López‐Rodas et al, 2007, 2009; Huertas, Rouco, López‐Rodas, & Costas, 2010; Huertas et al, 2011; Rouco et al, 2014; García‐Villada et al, 2004; Martín‐Clemente, Melero‐Jiménez, Bañares‐España, Flores‐Moya, & García‐Sánchez, 2019; Melero‐Jiménez, et al, 2019). Cultures were grown axenically in 250 mL ventilated cell culture flasks sealed with filter screw‐caps (Greiner; Bio‐One), containing 60 mL of half‐diluted BG11 medium (Sigma‐Aldrich Chemie).…”

“…In order to analyze the effects of environmental deterioration rate on the limit of resistance to salinity of each of the three strains of M. aeruginosa , a ratchet experiment was performed as described by Huertas et al (2010, 2011), Rouco et al (2014), Melero‐Jiménez et al (2019), and Martín‐Clemente et al (2019). Two ratchet experiments were carried out to simulate fast and slow environmental deterioration rates (Figure 1).…”

What Triggers the Annual Cycle of Cyanobacterium Oscillatoria sp. in an Extreme Environmental Sulfide-Rich Spa?

“…La Hedionda is a sulfide-rich (200 µM) thermal (20 • C) spring outflow in southern Spain [1,2] (Figure 1). While the sulfide-rich water of La Hedionda has been appreciated in thermal baths since almost 61 before Christ [3,4], sulfide is also a biocide because it blocks photosystem II (PSII) and respiratory electron transport [5][6][7][8][9].…”

“…population of La Hedionda not only is sulfide-resistant, but requires sulfide in its optimal niche.Water 2020, 12, 883 2 of 13 can usually overcome the toxic effect of sulfide, maintaining oxygenic photosynthesis through the sulfide-resistance of PSII [6,10-12] and/or enabling PSII-independent anoxygenic photosynthesis with sulfide as an electron donor to PSI [11,[13][14][15][16]. For this reason, we initially addressed the study of the adaptation processes of cyanobacteria to La Hedionda water [2] and, in this study, we hypothesized that the levels of sulfide in this habitat could be the main trigger of cyanobacteria populations. However, despite the fact that sulfide-rich spas are natural laboratories for studying eco-evolutionary processes involved in the adaptation of photosynthetic organisms to sulfide [2,4,17,18], little information exists about the seasonal variability of the sulfide concentration and low diversity populations of photosynthetic organisms inhabiting these extreme ecosystems [4].…”

“…For this reason, we initially addressed the study of the adaptation processes of cyanobacteria to La Hedionda water [2] and, in this study, we hypothesized that the levels of sulfide in this habitat could be the main trigger of cyanobacteria populations. However, despite the fact that sulfide-rich spas are natural laboratories for studying eco-evolutionary processes involved in the adaptation of photosynthetic organisms to sulfide [2,4,17,18], little information exists about the seasonal variability of the sulfide concentration and low diversity populations of photosynthetic organisms inhabiting these extreme ecosystems [4]. It must be highlighted that the usual phytoplankton succession has been widely studied in epicontinental waters where annual cycles depend on physical control, nutrients and grazing [19].…”