Unveiling membrane thermoregulation strategies in marine picocyanobacteria

Abstract

Summary The wide latitudinal distribution of marine Synechococcus cyanobacteria partly relies on the differentiation of lineages adapted to distinct thermal environments. Membranes are highly thermosensitive cell components, and the ability to modulate their fluidity can be critical for the fitness of an ecotype in a particular thermal niche. We compared the thermophysiology of Synechococcus strains representative of major temperature ecotypes in the field. We measured growth, photosynthetic capacities and membrane lipidome variations. We carried out a metagenomic analysis of stations of the Tara Oceans expedition to describe the latitudinal distribution of the lipid desaturase genes in the oceans. All strains maintained efficient photosynthetic capacities over their different temperature growth ranges. Subpolar and cold temperate strains showed enhanced capacities for lipid monodesaturation at low temperature thanks to an additional, poorly regiospecific Δ9‐desaturase. By contrast, tropical and warm temperate strains displayed moderate monodesaturation capacities but high proportions of double unsaturations in response to cold, thanks to regiospecific Δ12‐desaturases. The desaturase genes displayed specific distributions directly related to latitudinal variations in ocean surface temperature. This study highlights the critical importance of membrane fluidity modulation by desaturases in the adaptive strategies of Synechococcus cyanobacteria during the colonization of novel thermal niches.

Synergic Effects of Temperature and Irradiance on the Physiology of the Marine Synechococcus Strain WH7803

“…Consistent with the data of Pittera et al (2018) showing that after a shift from 22 to 13 • C, the level of double unsaturations of the MGDG sn-1 chain increased, the delta-12 fatty acid desaturase gene desA3 was found to be upregulated in response to LT, while it was downregulated in the opposite thermal shift (LLHT). The gene encoding the delta-9-desaturase DesC4, which is absent from warm Synechococcus thermotypes (clades II and III; Varkey et al, 2016;Pittera et al, 2018;Breton et al, 2019), also appeared strongly DE at LT but also in other stress conditions. At last, genes coding for DesA2, a delta-12 desaturase mostly found in warm thermotypes (Pittera et al, 2018) and DesC3, a core delta-9 desaturase, were in contrast mostly responsive to UV stress, even though desA2 was also upregulated in HLLT conditions.…”

“…Variations in the relative content of glycolipids are well known to be crucial for cell acclimation to temperature changes by modulating membrane fluidity. Thinner membranes (i.e., with a lower fatty acid average length) and/or highly unsaturated membranes, both favoring their fluidity, are indeed commonly observed in cold-adapted organisms (Chintalapati et al, 2007;Iskandar et al, 2013) and in response to cold stress, notably in marine Synechococcus (Varkey et al, 2016;Pittera et al, 2018;Breton et al, 2019). Here, although strong correlations and anticorrelations were found between length and saturation levels of the different lipids and blue and turquoise modules, respectively (Figure 4), most genes involved in fatty acid chain biosynthesis, in their insertion into membranes as well as in polar head biosynthesis were not significantly or only slightly DE.…”

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

“…TS-821 is a thermophilic cyanobacteria that will have predominantly saturated fatty acids possibly due to limited fatty acid desaturase genes (FAD) as observed in T. elongatus (36). However the marine cyanobacteria (Prochlorococcus/ Synechococcus) are mesophiles and have been shown to have highly unsaturated fatty acids due to their multiple FAD genes (36,37) and possibly due to recently identified activity of a cyanophage-encoded lipid desaturases (38). Future work will be needed to see if the marine cyanobacteria contain a stable dimeric or tetrameric form of PSI when grown in high light.…”

Modelling the Effects of Traits and Abiotic Factors on Viral Lysis in Phytoplankton

“…There is also a clear potential for a linkage of virus replication to temperature simply through impacts (advantageous or deleterious) on host physiology (Breton et al, 2020;Demory et al, 2020b). Thus, the host could be of good nutritional status with respect to C:N:P but growing at a sub-optimal rate because of temperature-limitation or light-limitation (Maat et al, 2017;Derelle et al, 2018;Demory et al, 2020a,b).…”