ABSTRACT
Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic organisms on Earth, an ecological success thought to be linked to the differential partitioning of distinct ecotypes into specific ecological niches. However, the underlying processes that governed the diversification of these microorganisms and the appearance of niche-related phenotypic traits are just starting to be elucidated. Here, by comparing 81 genomes, including 34 new Synechococcus, we explored the evolutionary processes that shaped the genomic diversity of picocyanobacteria. Time-calibration of a core-protein tree showed that gene gain/loss occurred at an unexpectedly low rate between the different lineages, with for instance 5.6 genes gained per million years (My) for the major Synechococcus lineage (sub-cluster 5.1), among which only 0.71/My have been fixed in the long term. Gene content comparisons revealed a number of candidates involved in nutrient adaptation, a large proportion of which are located in genomic islands shared between either closely or more distantly related strains, as identified using an original network construction approach. Interestingly, strains representative of the different ecotypes co-occurring in phosphorus-depleted waters (Synechococcus clades III, WPC1, and sub-cluster 5.3) were shown to display different adaptation strategies to this limitation. In contrast, we found few genes potentially involved in adaptation to temperature when comparing cold and warm thermotypes. Indeed, comparison of core protein sequences highlighted variants specific to cold thermotypes, notably involved in carotenoid biosynthesis and the oxidative stress response, revealing that long-term adaptation to thermal niches relies on amino acid substitutions rather than on gene content variation. Altogether, this study not only deciphers the respective roles of gene gains/losses and sequence variation but also uncovers numerous gene candidates likely involved in niche partitioning of two key members of the marine phytoplankton.
ABSTRACT
Understanding how microorganisms adjust their metabolism to maintain their ability to cope with short-term environmental variations constitutes one of the major current challenges in microbial ecology. Here, the best physiologically characterized marine Synechococcus strain, WH7803, was exposed to modulated light/dark cycles or acclimated to continuous high-light (HL) or low-light (LL), then shifted to various stress conditions, including low (LT) or high temperature (HT), HL and ultraviolet (UV) radiations. Physiological responses were analyzed by measuring time courses of photosystem (PS) II quantum yield, PSII repair rate, pigment ratios and global changes in gene expression. Previously published membrane lipid composition were also used for correlation analyses. These data revealed that cells previously acclimated to HL are better prepared than LL-acclimated cells to sustain an additional light or UV stress, but not a LT stress. Indeed, LT seems to induce a synergic effect with the HL treatment, as previously observed with oxidative stress. While all tested shift conditions induced the downregulation of many photosynthetic genes, notably those encoding PSI, cytochrome b6/f and phycobilisomes, UV stress proved to be more deleterious for PSII than the other treatments, and full recovery of damaged PSII from UV stress seemed to involve the neo-synthesis of a fairly large number of PSII subunits and not just the reassembly of pre-existing subunits after D1 replacement. In contrast, genes involved in glycogen degradation and carotenoid biosynthesis pathways were more particularly upregulated in response to LT. Altogether, these experiments allowed us to identify responses common to all stresses and those more specific to a given stress, thus highlighting genes potentially involved in niche acclimation of a key member of marine ecosystems. Our data also revealed important specific features of the stress responses compared to model freshwater cyanobacteria.
