Global Phylogeography of Marine <i>Synechococcus</i> in Coastal Areas Reveals Strong Community Shifts

Abstract

Marine <i>Synechococcus</i> 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 <i>Synechococcus</i> communities in these environments is based on only a few local studies. Here, we use the global metagenome data set of the Ocean Sampling Day (June 21^st, 2014) to get a snapshot of the taxonomic composition of coastal <i>Synechococcus</i> communities worldwide, by recruitment on a reference database of 141 picocyanobacterial genomes, representative of the whole <i>Prochlorococcus</i>, <i>Synechococcus</i>, and <i>Cyanobium</i> 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 <i>Synechococcus</i> 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 <i>Synechococcus</i> community in cold and temperate coastal areas. Altogether, this study reveals several important characteristics and specificities of the coastal communities of <i>Synechococcus</i> worldwide. <b>IMPORTANCE</b> <i>Synechococcus</i> is the second most abundant phytoplanktonic organism on Earth, and its wide genetic diversity allowed it to colonize all the oceans except for polar waters, with different clades colonizing distinct oceanic niches. In recent years, the use of global metagenomics data sets has greatly improved our knowledge of "who is where" by describing the distribution of <i>Synechococcus</i> clades or ecotypes in the open ocean. However, little is known about the global distribution of <i>Synechococcus</i> ecotypes in coastal areas, where <i>Synechococcus</i> is often the dominant phytoplanktonic organism. Here, we leverage the global Ocean Sampling Day metagenomics data set to describe <i>Synechococcus</i> community composition in coastal areas worldwide, revealing striking community shifts, in particular along the coasts of Europe. As temperature appears as an important driver of the community composition, we also characterize the thermal preferenda of 8 <i>Synechococcus</i> strains, bringing new insights into the adaptation to temperature of the dominant <i>Synechococcus</i> clades.