Novel Synechococcus Genomes Reconstructed from Freshwater Reservoirs.

Pedro J. Cabello-Yeves,Rohit Ghai,Francisco Rodriguez-Valera,Jose M. Haro-Moreno,Ana-Belen Martin-Cuadrado,Antonio Picazo,Antonio Camacho

doi:10.3389/fmicb.2017.01151

Abstract

Freshwater picocyanobacteria including Synechococcus remain poorly studied at the genomic level, compared to their marine representatives. Here, using a metagenomic assembly approach we discovered two novel Synechococcus sp. genomes from two freshwater reservoirs Tous and Lake Lanier, both sharing 96% average nucleotide identity and displaying high abundance levels in these two lakes located at similar altitudes and temperate latitudes. These new genomes have the smallest estimated size (2.2 Mb) and average intergenic spacer length (20 bp) of any previously sequenced freshwater Synechococcus, which may contribute to their success in oligotrophic freshwater systems. Fluorescent in situ hybridization confirmed that Synechococcus sp. Tous comprises small cells (0.987 ± 0.139 μm length, 0.723 ± 0.119 μm width) that amount to 90% of the picocyanobacteria in Tous. They appear together in a phylogenomic tree with Synechococcus sp. RCC307 strain, the main representative of sub-cluster 5.3 that has itself one of the smallest marine Synechococcus genomes. We detected a type II phycobilisome (PBS) gene cluster in both genomes, which suggests that they belong to a phycoerythrin-rich pink low-light ecotype. The decrease of acidic proteins and the higher content of basic transporters and membrane proteins in the novel Synechococcus genomes, compared to marine representatives, support their freshwater specialization. A sulfate Cys transporter which is absent in marine but has been identified in many freshwater cyanobacteria was also detected in Synechococcus sp. Tous. The RuBisCo subunits from this microbe are phylogenetically close to the freshwater amoeba Paulinella chromatophora symbiont, hinting to a freshwater origin of the carboxysome operon of this protist. The novel genomes enlarge the known diversity of freshwater Synechococcus and improve the overall knowledge of the relationships among members of this genus at large.

Highlights

Cyanobacteria are among the most diverse and widely distributed group of bacteria
The determinations of abundances by flow cytometry showed that Synechococcus cells were distributed throughout the water column at moderate abundances of around 2 × cells·mL−1, whereas heterotrophic bacteria reached around 6 × cells·mL−1 at all tested depths
The taxonomic composition based on 16S rRNA coding raw read fragments found in the Tous reservoir shows that taxa are present in similar proportions to the ones found in Amadorio (10 m, 0.22 μm collected sample), the closest freshwater water body to Tous (Ghai et al, 2014)

Summary

Introduction

Cyanobacteria are among the most diverse and widely distributed group of bacteria They are the only prokaryotes capable of performing oxygenic photosynthesis, and greatly contribute to global primary production, fixing a substantial amount of carbon both in marine and freshwater environments. Pcy clades (Synechococcus, Prochlorococcus, and Cyanobium) are designated as nonbloomers (Steffen et al, 2012) and are either single or colonial rod-shaped cells ranging from 0.2 to 3 μm They can form dense populations of up to several million cells per ml at the deep chlorophyll maximum (DCM) of mesotrophic stratified lakes (Camacho et al, 2003a,b) and, though less abundant, they peak at the DCM of oceans and some seas (Partensky et al, 1999). Freshwater Synechococcus strains play a critical role in the ecological health of water bodies that are important human resources

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