Parallel phylogeography of Prochlorococcus and Synechococcus

Abstract

The globally abundant marine Cyanobacteria Prochlorococcus and Synechococcus share many physiological traits but presumably have different evolutionary histories and associated phylogeography. In Prochlorococcus, there is a clear phylogenetic hierarchy of ecotypes, whereas multiple Synechococcus clades have overlapping physiologies and environmental distributions. However, microbial traits are associated with different phylogenetic depths. Using this principle, we reclassified diversity at different phylogenetic levels and compared the phylogeography. We sequenced the genetic diversity of Prochlorococcus and Synechococcus from 339 samples across the tropical Pacific Ocean and North Atlantic Ocean using a highly variable phylogenetic marker gene (rpoC1). We observed clear parallel niche distributions of ecotypes leading to high Pianka's Index values driven by distinct shifts at two transition points. The first transition point at 6°N distinguished ecotypes adapted to warm waters but separated by macronutrient content. At 39°N, ecotypes adapted to warm, low macronutrient vs. colder, high macronutrient waters shifted. Finally, we detected parallel vertical and regional single-nucleotide polymorphism microdiversity within clades from both Prochlorococcus and Synechococcus, suggesting uniquely adapted populations at very specific depths, as well as between the Atlantic and Pacific Oceans. Overall, this study demonstrates that Prochlorococcus and Synechococcus have shared phylogenetic organization of traits and associated phylogeography.

Fig. 1

Similar phylogenetic structure of Prochlorococcus and Synechococcus clades common in open ocean surface waters. Maximum likelihood phylogenetic trees based on previous constructions [23, 43]. Strains are colored based on their clade and clade names are at the base of each group. Metagenomic assembled genomes HNLC1 and HNLC2 are from Rusch et al. [6]. Hypothesized ecotype labels are listed in the center and tested in this study (color figure online)

Fig. 2

Variation in environmental conditions and phytoplankton abundances. a Temperature profiles across three cruise transects in the Pacific and Atlantic Oceans, b soluble reactive phosphate, c flow cytometry counts for Prochlorococcus, d Synechococcus, and e picoeukaryotic phytoplankton

Fig. 3

Clade frequencies across three ocean regions. Prochlorococcus a clades HLI with white dots representing DNA sampling points for all plots, b HLII, and c HLIII/IV. Synechococcus d clade I/IV, e II/III, and f CRD1. Clade relative abundances are normalized to Prochlorococcus or Synechococcus total number of sequences per sample. Gray areas indicate no data

Fig. 4

Niche overlap of Prochlorococcus and Synechococcus clades. A Pianka index value of 0 represents no overlap and a value of 1 signifies complete overlap [38]. Significance values (*p < 0.01) come from testing observations against a null model with latitude randomization. Synechococcus clades are colored in orange and Prochlorococcus clades are colored in green (color figure online)

Fig. 5

Parallel microdiversity between Prochlorococcus and Synechococcus clades. Clades a Prochlorococcus HLII, b Synechococcus Clade II/III, c Prochlorococcus HLIII/IV, and d Synechococcus CRD1. Each row represents a sample. Rows were clustered by UniFrac sample distance, nodes with unfilled circles represent > 50 bootstrap support and filled circles represent > 75 out of 100 resampled trees. Side columns are colored by ocean origin, depth, latitude, and temperature followed by SNPs colored by the most prevalent nucleotide in each position for each sample. SNP profiles highlight single-nucleotide differences from overall SNP profile consensus across sites for each clade. Reference sequences from Fig. 1 isolates and metagenomic assemblies are included for each corresponding group, which are grouped phylogenetically in Supplementary Figure S5 (color figure online)