Comparative Thermophysiology of Marine Synechococcus CRD1 Strains Isolated From Different Thermal Niches in Iron-Depleted Areas

Abstract

Marine Synechococcus cyanobacteria are ubiquitous in the ocean, a feature likely related to their extensive genetic diversity. Amongst the major lineages, clades I and IV preferentially thrive in temperate and cold, nutrient-rich waters, whilst clades II and III prefer warm, nitrogen or phosphorus-depleted waters. The existence of such cold (I/IV) and warm (II/III) thermotypes is corroborated by physiological characterization of representative strains. A fifth clade, CRD1, was recently shown to dominate the Synechococcus community in iron-depleted areas of the world ocean and to encompass three distinct ecologically significant taxonomic units (ESTUs CRD1A-C) occupying different thermal niches, suggesting that distinct thermotypes could also occur within this clade. Here, using comparative thermophysiology of strains representative of these three CRD1 ESTUs we show that the CRD1A strain MITS9220 is a warm thermotype, the CRD1B strain BIOS-U3-1 a cold temperate thermotype, and the CRD1C strain BIOS-E4-1 a warm temperate stenotherm. Curiously, the CRD1B thermotype lacks traits and/or genomic features typical of cold thermotypes. In contrast, we found specific physiological traits of the CRD1 strains compared to their clade I, II, III, and IV counterparts, including a lower growth rate and photosystem II maximal quantum yield at most temperatures and a higher turnover rate of the D1 protein. Together, our data suggests that the CRD1 clade prioritizes adaptation to low-iron conditions over temperature adaptation, even though the occurrence of several CRD1 thermotypes likely explains why the CRD1 clade as a whole occupies most iron-limited waters.

Global Phylogeography of Marine Synechococcus in Coastal Areas Reveals Strong Community Shifts

“…Physiological measurement of temperature preferenda of strains belonging to clades I, II, III, IV, and V isolated across different latitudes further confirmed the existence of warm (clades II, III, V) and cold (clades I and IV) ‘thermotypes’ ( 38 – 42 ). Despite being phylogenetically distant, clades I and IV were further demonstrated to share a number of physiological adaptations to cold water, including a higher thermal sensitivity of phycobiliproteins ( 43 ), a similar change in membrane lipids ( 40 , 44 ) and an increase of the photoprotection capacities using the orange carotenoid protein (OCP; 45).…”

“…2 ). While several strains belonging to clade I were previously shown to withstand colder temperatures than their tropical clade II counterparts ( 38 – 40 , 53 ), growth optima and boundary limits for temperature were only available for 1 clade IV ( 38 , 40 , 42 ) and 2 closely related clade III strains ( 38 , 40 , 41 , 54 ), and results were obtained in different light conditions, making them difficult to compare. Here, the direct comparison of clades I and IV strains, grown under the same conditions, showed quite similar thermal preferences.…”

“…Finally, SC 5.1, a lineage that rapidly diversified after the advent of the Prochlorococcus radiation ( 34 , 35 ), is by far the most widespread and abundant Synechococcus lineage in the open ocean environment, e.g., representing more than 93% of total Tara Oceans metagenomic reads assigned to SC 5.1 to 5.3 ( 12 ). From 10 to 15 phylogenetic clades have been defined within SC 5.1 depending on the phylogenetic marker ( 10 , 30 , 36 ) but studies of the global distribution patterns of Synechococcus populations in open ocean waters have shown that there are 5 major clades in situ (I, II, III, IV, and CRD1), with clades I and IV co-dominating Synechococcus communities in cold and temperate, nutrient-rich areas, while clades II, III, and CRD1 preferentially thrive in warm waters ( 5 , 12 , 31 , 32 , 37 , 38 ).…”

Genomic and Transcriptomic Insights into Salinity Tolerance-Based Niche Differentiation of Synechococcus Clades in Estuarine and Coastal Waters

“…A combination of gene gains or losses, and sequence divergence are thought to be responsible for the niche separation of Synechococcus ecotypes ( 27 ). For example, a genome comparison indicated that clade CRD1 has a larger collection of Fe-related genes than the other ecotypes, which helps it survive and succeed in low-iron habitats ( 27 , 28 ). It has also been reported that heterotrophy genes, such as bzt and potE (polar amino acid permease genes), are important for the survival of Synechococcus in harsh mesopelagic environments ( 29 ).…”

Ecophysiological analysis reveals distinct environmental preferences in closely related Baltic Sea picocyanobacteria

“…Sub‐cluster 5.1 is mainly composed of pelagic marine strains and it is the most widespread lineage in the open ocean environment (Farrant et al, 2016). Extensive work combining global field observations, metagenomics, and physiological work with isolates has revealed a high genetic and functional diversity within this sub‐cluster and multiple genetic lineages (clades) have been identified (Doré et al, 2020; Farrant et al, 2016; Ferrieux et al, 2022; Mackey et al, 2017; Pittera et al, 2014; Six et al, 2021; Sohm et al, 2016). These lineages are physiologically specialized in different niches, revealing the existence of ecotypes defined by environmental factors such as temperature and light.…”