Dryland endolithic Chroococcidiopsis and temperate fresh water Synechocystis have distinct membrane lipid and photosynthesis acclimation strategies upon desiccation and temperature increase

Damien Douchi (1) , Gregory Si Larbi (1) , Benjamin Fel (1) , Marlène Bonnanfant (1) , Mathilde Louwagie (1) , Juliette Jouhet (1) , Mathias Agnely (2) , Stéphanie Pouget (3) , Eric Maréchal (1)

1 LIPID
2 Saint Gobain
3 MEM - Modélisation et Exploration des Matériaux

An effect of climate change is the expansion of drylands in temperate regions, predicted to affect microbial biodiversity. Photosynthetic organisms being at the base of ecosystem’s trophic networks, we compared an endolithic desiccation-tolerant Chroococcidiopsis cyanobacteria isolated from gypsum rocks in the Atacama Desert, with a freshwater desiccation-sensitive Synechocystis. We sought whether some acclimation traits in response to desiccation and temperature variations were shared, to evaluate the potential of temperate species to possibly become resilient to future arid conditions. When temperature varies, Synechocystis tunes the acyl composition of its lipids, via a homeoviscuous acclimation mechanism known to adjust membrane fluidity, whereas no such change occurs in Chroococcidiopsis. Vice versa, a combined study of photosynthesis and pigment content shows that Chroococcidiopsis remodels its photosynthesis components and keeps an optimal photosynthetic capacity at all temperatures, whereas Synechocystis is unable to such adjustment. Upon desiccation on a gypsum surface, Synechocystis is rapidly unable to revive, whereas Chroococcidiopsis is capable to recover after three weeks. Using X-ray diffraction, we found no evidence that Chroococcidiopsis could use water extracted from gypsum crystal in such conditions, as a surrogate of missing water. The sulfolipid sulfoquinovosyldiacylglycerol becomes the prominent membrane lipid in both dehydrated cyanobacteria, highlighting an overlooked function for this lipid. Chroococcidiopsis keeps a minimal level of monogalactosyldiacylglycerol, which may be essential for the recovery process. Results support that two independent adaptation strategies have evolved in these species to cope with temperature and desiccation increase, and suggest some possible scenarios for microbial biodiversity change triggered by climate change.

Keywords: Cyanobacteria; lipid; photosynthesis; temperature stress; adaptation; Synechocystis Chroococcidiopsis endolithic cyanobacteria sulfoquinovosyldiacylglycerol gypsum photosynthesis; Synechocystis; Chroococcidiopsis; endolithic cyanobacteria; sulfoquinovosyldiacylglycerol; gypsum

Domains: Life Sciences [q-bio]; Vegetal Biology

Damien Douchi, Gregory Si Larbi, Benjamin Fel, Marlène Bonnanfant, Mathilde Louwagie, et al.. Dryland endolithic Chroococcidiopsis and temperate fresh water Synechocystis have distinct membrane lipid and photosynthesis acclimation strategies upon desiccation and temperature increase. Plant and Cell Physiology, 2023, ⟨10.1093/pcp/pcad139⟩. ⟨hal-04281075⟩