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

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 data set of the Ocean Sampling Day (June 21^st, 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 reveals several important characteristics and specificities of the coastal communities of Synechococcus worldwide. IMPORTANCE Synechococcus 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 Synechococcus clades or ecotypes in the open ocean. However, little is known about the global distribution of Synechococcus ecotypes in coastal areas, where Synechococcus is often the dominant phytoplanktonic organism. Here, we leverage the global Ocean Sampling Day metagenomics data set to describe Synechococcus 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 Synechococcus strains, bringing new insights into the adaptation to temperature of the dominant Synechococcus clades.

Keywords: Ocean Sampling Day; Synechococcus; coastal areas; marine cyanobacteria; metagenomics; niche partitioning; temperature.

FIG 1

Relative abundance of marine Synechococcus clades in Ocean Sampling Day stations. Stations are located at the bottom of barplots of relative abundance. The insert shows a closeup version of Europe. Station numbers are shown in Fig. S1. Categories 5.1 and Syn correspond to reads that could not be assigned to a clade but were assigned to the higher taxonomic levels of Synechococcus SC 5.1 or Synechococcus genus, respectively.

FIG 2

Temperature preferenda of 8 marine Synechococcus strains. Growth rate as a function of temperature of acclimated growth. Two strains were chosen within each of the 4 major clades I, II, III, and IV (top to bottom). All cultures were grown at a light intensity of 20 μmol quanta m⁻² s⁻¹. Error bars are standard deviation from the mean based on at least 3 replicates (n ≥ 3). The line represents the best fit of the Cardinal Temperature Model with Inflection (BR model; 86).

FIG 3

Clusters of Ocean Sampling Day (OSD) stations based on relative abundance profiles of Synechococcus clades. OSD stations were clustered based on the relative abundance profiles of marine Synechococcus clades using Bray-Curtis distance: two stations will cluster together if they have a similar composition in Synechococcus clades. The clustering dendrogram is available as Fig. S2. (A) The upper panel indicates water temperature. The lower panel shows the nine clusters of relative abundance profiles of Synechococcus clades. Categories 5.1 and Syn correspond to reads that could not be assigned to a clade but were assigned to the higher taxonomic levels of Synechococcus SC 5.1 or Synechococcus genus, respectively. (B) Geographical distribution of the nine clusters of OSD stations along the European coasts. A global map of cluster distribution is available as Fig. S3.

FIG 4

Violin plots showing the distribution of temperature and salinity for each cluster of Ocean Sampling Day (OSD) stations defined in Fig. 3. (A) Temperature. (B) Salinity. Panels are numbered according to cluster numbers in Fig. 3. The black dot in each violin plot shows the median value. Different letters indicate significantly different distributions (Dunn test. adjusted P-value < 0.05). The same analysis considering distance to the nearest coast gave no significant result.