Synechococcus Assemblages across the Salinity Gradient in a Salt Wedge Estuary

Abstract

Synechococcus are the most abundant and widely distributed picocyanobacteria in the ocean. The salt-wedge type of estuary possesses the complete horizontal and vertical gradient of salinity together with other physical and chemical parameters. In order to reveal whether such a complex environmental gradient harbors a high diversity of Synechococcus, we investigated the abundance, taxonomic composition and pigment genetic diversity of Synechococcus in surface and bottom waters across the salinity gradient in a salt-wedge estuary by flow cytometric analysis and pyrosequencing of the rpoC1 gene and cpcBA operon (encoding phycocyanin). Synechococcus were ubiquitously distributed in the studied region, with clear spatial variations both horizontally and vertically. The abundance and diversity of Synechococcus were low in the freshwater-dominated low salinity waters. By pyrosequencing of the rpoC1 gene, we have shown that with the increase of salinity, the dominant Synechococcus shifted from the freshwater Synechococcus to the combination of phylogenetic subcluster 5.2 and freshwater Synechococcus, and then the strictly marine subcluster 5.1 clade III. Besides, the composition of Synechococcus assemblage in the deep layer was markedly different from the surface in the stratified waters (dissimilarities: 40.32%-95.97%, SIMPER analysis). High abundance of clade III Synechococcus found in the brackish waters may revise our previous understanding that strains of this clade prefers oligotrophic environment. Our data also suggested that both the phylogenetic subcluster 5.3 Synechococcus, a lineage that was not well understood, and subcluster 5.1 clade I, a typical cold water lineage, were widely distributed in the bottom layer of the estuary. Clade I detected in the studied region was mainly contributed by subclade IG. Analysis of the cpcBA operon sequences revealed niche partitioning between type 1 and type 3 Synechococcus, with type 2 distributed broadly across the whole environmental gradients. Our results suggest that the salt wedge estuary provides various niches for different lineages of Synechococcus, making it an environment with high Synechococcus diversity compared with adjacent freshwater and shelf sea environments.

Light color acclimation is a key process in the global ocean distribution ofSynechococcus cyanobacteria

“…PT 3 was found to be largely dominant over PT 1 and 2 along the oceanic Tara Oceans transect, in agreement with the coastalrestricted distribution of the latter PTs (18,22,27,(31)(32)(33)(34)(37)(38)(39). Biogeography and correlation analyses with environmental pa-rameters provided several important insights concerning niche partitioning of PT 3 subtypes.…”

“…Marine Synechococcus display a large pigment diversity, with different PTs preferentially harvesting distinct regions of the light spectrum. Previous studies based on optical properties or on a single genetic marker could not differentiate all PTs (17,(29)(30)(31), and thus neither assess their respective realized environmental niches (43) nor the role of light quality on the relative abundance of each PT. Here, we showed that a metagenomic read recruitment approach combining three genetic markers can be used to reliably predict all major PTs.…”

“…As there is no correspondence between pigmentation and core genome phylogeny (7,16,17), deciphering the relative abundance and niche partitioning of Synechococcus PTs in the environment requires specific approaches. In the past 30 y, studies have been based either on (i) proxies of the PUB:PEB ratio as assessed by flow cytometry (18)(19)(20), fluorescence excitation spectra (21)(22)(23)(24)(25)(26)(27), and epifluorescence microscopy (28); or (ii) phylogenetic analyses of cpcBA or cpeBA (17,(29)(30)(31)(32)(33)(34). These studies showed that PT 1 is restricted to and dominates in low salinity surface waters and/or estuaries, which are characterized by a high turbidity resulting in a red-wavelengths-dominated light field (18,22,(31)(32)(33)(34)(35)(36)(37)(38), whereas PT 2 is found in coastal shelf waters or in the transition zones between brackish and oceanic environments with intermediate optical properties (18,27,34,(36)(37)(38)(39).…”

Evolution as an ecosystem process: insights from genomics

“…Another ubiquitous marine cyanobacterium, Synechococcus, has been shown to have high genetic diversity associated with pigment diversity. Multiple gene variants, gene organisations, and even polymorphic intergenic spacer regions have been shown to be associated with unique geographic, thermal, and turbidity niches (Xia et al 2015(Xia et al , 2017. Possession of these unique genomic sequences and motifs appears to result in niche differentiation that expands the geographic range of the genus beyond where individual phylotypes could persist.…”

“…Possession of these unique genomic sequences and motifs appears to result in niche differentiation that expands the geographic range of the genus beyond where individual phylotypes could persist. Further whole-genome analysis could provide new insights into the genomic basis of these pigment-related traits, constraints on their variation owing to linkage or epistasis, and their associations with other traits under selection (Xia et al 2017). The existing genomic studies of natural populations of keystone primary producers reveal our staggering ignorance about the functional importance of genomic diversity in our global ecosystems.…”