Picocyanobacteria containing a novel pigment gene cluster dominate the brackish water Baltic Sea

John Larsson,Bigitta Bergman,Martin Ekman,Narin Celepli,Christopher L Dupont,Karolina Ininbergs,Shibu Yooseph

doi:10.1038/ismej.2014.35

Abstract

Photoautotrophic picocyanobacteria harvest light via phycobilisomes (PBS) consisting of the pigments phycocyanin (PC) and phycoerythrin (PE), encoded by genes in conserved gene clusters. The presence and arrangement of these gene clusters give picocyanobacteria characteristic light absorption properties and allow the colonization of specific ecological niches. To date, a full understanding of the evolution and distribution of the PBS gene cluster in picocyanobacteria has been hampered by the scarcity of genome sequences from fresh- and brackish water-adapted strains. To remediate this, we analysed genomes assembled from metagenomic samples collected along a natural salinity gradient, and over the course of a growth season, in the Baltic Sea. We found that while PBS gene clusters in picocyanobacteria sampled in marine habitats were highly similar to known references, brackish-adapted genotypes harboured a novel type not seen in previously sequenced genomes. Phylogenetic analyses showed that the novel gene cluster belonged to a clade of uncultivated picocyanobacteria that dominate the brackish Baltic Sea throughout the summer season, but are uncommon in other examined aquatic ecosystems. Further, our data suggest that the PE genes were lost in the ancestor of PC-containing coastal picocyanobacteria and that multiple horizontal gene transfer events have re-introduced PE genes into brackish-adapted strains, including the novel clade discovered here.

Highlights

Unicellular picocyanobacteria are widespread in aquatic ecosystems across the globe (Scanlan et al, 2009)
As a result of thorough annotations of the phycobilisome gene cluster (Six et al, 2007) our reciprocal homology search allowed us to efficiently detect relevant genes, it should be noted that the biochemical function has not been shown for the genes we identified in this study
As we focused on PBS genes in cluster 5 picocyanobacteria, the phylogeny of this clade is shown in Figure 2a, while the full cyanobacterial phylogeny is presented in the Supplementary Material (Supplementary data set 1)

Summary

Introduction

Unicellular picocyanobacteria are widespread in aquatic ecosystems across the globe (Scanlan et al, 2009). Types II and III gene clusters in addition contain the phycoerythrin-I (PEI) subunit genes cpeBA and are found in red strains adapted to clear waters of the Only five genome sequences are available for the open ocean where blue wavelengths dominate. Genomes of 13 marine picocyanobacterial strains picocyanobacteria, we analysed genomes of unculwith types II or III pigmentation have been tivated picocyanobacterial populations in a total of sequenced to date (Table 2), and in nine of these 94 aquatic samples separated spatially along a the PBS gene cluster has been studied in detail (Six 1800 km salinity gradient (Dupont et al, 2014) and et al, 2007). These results further our understanding of molecular adaptations to light in brackish and coastal water ecosystems and the evolution of light-harvesting genes in cyanobacteria

Materials and methods

Findings

14 June 29 June 20 July 3 August 17 August 30 August