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

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.

Meta‐omic analyses of Baltic Sea cyanobacteria: diversity, community structure and salt acclimation

“…() suggested a divergence of limnic and marine clades into a global brackish water adapted microbiome, which potentially arose long before the formation of the modern day Baltic Sea. Together with the recent discovery of a unique pigment gene cluster organization in Baltic Sea picocyanobacteria (Larsson et al ., ), this further highlights the untapped genomic diversity and physiological capacities of microorganisms such as cyanobacteria in brackish ecosystems. Temperature and salinity has been identified as main drivers of the cyanobacterial community structure in a local region of the Baltic Sea proper (Bertos‐Fortis et al ., ), but thus far no specific genetic adaptations have been identified in the Baltic Sea cyanobacterial community in situ to link the community composition to environmental parameters.…”

“…Despite their small size, the emerging picture suggests that picocyanobacteria may also be significant players in Baltic Sea waters (Stal et al ., ). Recently, some were shown to have evolved novel pigment‐gene characteristics thus far not observed elsewhere (Larsson et al ., ). Global analyses show that environmental factors (light, nutrients and temperature) greatly influence picocyanobacterial community composition.…”

A new class of marine Euryarchaeota group II from the mediterranean deep chlorophyll maximum

“…They were also absent in marine collections from polar regions (Alonso-Saez et al, 2012) and from the Baltic collections (Larsson et al, 2014). The Red Sea DCM metagenome (365 Mb) (Thompson et al, 2013) was also analyzed, and although the sample was described as recovered at the DCM (50 m), no significant recruitment was found.…”

Techniques for Quantifying Phytoplankton Biodiversity

“…Furthermore, the lack of oxygen production explained the ability to fix nitrogen during the day. In a study of GOS samples, Larsson et al (2014) identified novel configurations of the phycobilisome in Synechococcus that could provide an adaptation to low-salinity environments. Metagenomic studies have also revealed extensive variation in the presence or absence of nutrient acquisition genes.…”