Global phylogeography of marine Synechococcus in coastal areas reveals strikingly different communities than in the open ocean

Abstract

Marine Synechococcus comprise a numerically and ecologically prominent phytoplankton group, playing a major role in both carbon cycling and trophic networks in all oceanic regions except in the polar oceans. Despite their high abundance in coastal areas, our knowledge of Synechococcus communities in these environments is based on only a few local studies. Here, we use the global metagenome dataset of the Ocean Sampling Day (June 21st 2014) to get a snapshot of the taxonomic composition of coastal Synechococcus communities worldwide, by recruitment on a reference database of 141 picocyanobacterial genomes, representative of the whole Prochlorococcus, Synechococcus and Cyanobium diversity. This allowed us to unravel drastic community shifts over small to medium scale gradients of environmental factors, in particular along European coasts. The combined analysis of the phylogeography of natural populations and the thermophysiological characterization of eight strains, representative of the four major Synechococcus lineages (clades I to IV), also brought novel insights about the differential niche partitioning of clades I and IV, which most often co-dominate the Synechococcus community in cold and temperate coastal areas. Altogether, this study tackles the main differences between open-ocean and coastal communities worldwide.

Differential acclimation kinetics of the two forms of type IV chromatic acclimaters occurring in marine Synechococcus cyanobacteria

“…In contrast to Exc 495:545 ratios, light quality had no significant effect on growth rates, while the latter varied with PT, temperature and light quantity. In HL, the growth rates of all six chromatic acclimaters used for acclimation experiments were significantly higher at 25°C than 18°C, the former being an optimal growth temperature for most marine Synechococcus strains tested so far (Figure 1; Mackey et al, 2013;Pittera et al, 2014;Breton et al, 2020;Doré et al, 2022;Ferrieux et al, 2022). The impact of increasing temperature on growth rate was however much less important at LL, confirming that temperature and irradiance have a synergistic effect on growth, as previously observed in the model strain WH7803 .…”

Nested PCR Approach for petB Gene Metabarcoding of Marine Synechococcus Populations

“…In addition, Synechococcus cells from SC 5.2 and SC 5.3 were probably absent in our samples. SC 5.2 representatives are mainly found in estuaries and river-influenced coastal waters ( 39 – 42 ), and although SC 5.3 contains both freshwater and marine representatives ( 32 , 43 ), the latter have been sporadically detected at high abundance only in some regions, such as the Red Sea, the Mediterranean Sea, and the northwestern Atlantic Ocean ( 32 , 44 , 45 ).…”

“…Prior studies conducted in surrounding areas report different proportions of clades I to IV. Both clades were detected in similar proportions along the coast of New Zealand at overlapping latitudes (45°S) by a PCR-independent method ( 42 ). Clade IV has been observed in a higher proportion than clade I in the western and eastern South Pacific Ocean at slightly lower latitudes with warmer conditions (around 30°S compared to 42°S in this study) ( 9 , 32 , 45 ).…”

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

“…Clades I and IV mainly thrive in temperate and cold, nutrient-rich waters, while clades II and III reside in warm, oligotrophic or mesotrophic areas ( Zwirglmaier et al, 2008 ; Mella-Flores et al, 2011 ), suggesting the existence of cold (I/IV) and warm (II/III) Synechococcus “thermotypes.” This hypothesis was subsequently confirmed by work demonstrating that strains representative of these different clades exhibit distinct thermal preferenda ( Mackey et al, 2013 ; Pittera et al, 2014 ; Breton et al, 2020 ; Six et al, 2021 ), a feature notably linked to differences in the thermostability of light-harvesting complexes ( Pittera et al, 2017 ), lipid desaturase gene content ( Pittera et al, 2018 ) and the ability of some strains to induce photoprotective light dissipation at colder temperatures using the orange carotenoid protein (OCP; Six et al, 2021 ). Field studies using global ocean datasets have allowed to refine the respective ecological niches of the different thermotypes, with clade I extending further north than clade IV ( Paulsen et al, 2016 ; Doré et al, 2022 ) and clades II and III predominating in N- and P-depleted waters, respectively, but also to highlight the importance of a fifth clade within SC 5.1, the CRD1 clade ( Farrant et al, 2016 ; Sohm et al, 2016 ; Kent et al, 2019 ). Initially thought to be limited to the Costa Rica dome area ( Saito et al, 2005 ; Gutiérrez-Rodríguez et al, 2014 ), the latter clade was recently found to be a major component of Synechococcus communities in iron (Fe)-depleted areas ( Farrant et al, 2016 ; Sohm et al, 2016 ; Ahlgren et al, 2020 ).…”