Ecological and genomic features of two widespread freshwater picocyanobacteria

Abstract

We present two genomes of widespread freshwater picocyanobacteria isolated by extinction dilution from a Spanish oligotrophic reservoir. Based on microscopy and genomic properties, both picocyanobacteria were tentatively designated Synechococcus lacustris Tous, formerly described as a metagenome assembled genome (MAG) from the same habitat, and Cyanobium usitatum Tous, described here for the first time. Both strains were purified in unicyanobacterial cultures, and their genomes were sequenced. They are broadly distributed in freshwater systems; the first seems to be a specialist on temperate reservoirs (Tous, Amadorio, Dexter, Lake Lanier, Sparkling), and the second appears to also be abundant in cold environments including ice-covered lakes such as Lake Baikal, Lake Erie or the brackish Baltic Sea. Having complete genomes provided access to the flexible genome that does not assemble in MAGs. We found several genomic islands in both genomes, within which there were genes for nitrogen acquisition, transporters for a wide set of compounds and biosynthesis of phycobilisomes in both strains. Some of these regions of low coverage in metagenomes also included antimicrobial compounds, transposases and phage defence systems, including a novel type III CRISPR-Cas phage defence system that was only detected in Synechococcus lacustris Tous.

A new genomic taxonomy system for the Synechococcus collective

“…The two genera Inmanicoccus and Lacustricoccus gen. nov. share a similar characteristic: they also form a monophyletic grouping, but Lacustricoccus was described as a new species from freshwater sources (Ca. Synechococcus lacustris , Cabello‐Yeves et al ., 2017; Cabello‐Yeves et al ., 2018), and Inmanicoccus was isolated from coastal waters (the type species Inmanicoccus mediterranei RCC 307 was isolated from a depth of 15 m in the Mediterranean Sea).…”

Genomic Comparison and Spatial Distribution of Different Synechococcus Phylotypes in the Black Sea

“…Importantly, both BSD and BSS strains display type IIB pigmentation ( Supplementary Figure S3 ), a novel type of pigmentation that was first observed in freshwater and brackish picocyanobacteria ( Larsson et al, 2014 ; Cabello-Yeves et al, 2018 ; Sánchez-Baracaldo et al, 2019 ), and then described in marine strains ( Callieri et al, 2019 ). Furthermore, the fact that the above-mentioned unique genes were flanked by transposases in BSS genomes could indicate that these were transferred horizontally by other cyanobacteria, and were probably involved in the niche adaptation of the two coastal strains.…”

“…Indeed, genes of the phycobilisome operon flanked by mobile genetic elements were most similar to the ones from freshwater strains from sub-cluster 5.2, which once again opens up new evolutionary perspectives on the freshwater to marine transition suggested for this picocyanobacterial sub-cluster ( Sánchez-Baracaldo, 2015 ; Sánchez-Baracaldo et al, 2019 ). In general, all genes encoded in the flexible genome have been linked to genomic islands, previously associated with niche adaptation in marine and freshwater picocyanobacteria ( Dufresne et al, 2008 ; Scanlan et al, 2009 ; Cabello-Yeves et al, 2018 ). Overall, based on the genomic features observed in our Black Sea strains, we could conclude that BSS phylotypes seem to be more adapted to surface layers, as they were only detected in the upper layers of some Black Sea stations by qPCR (except for one station at 42 m) and were rare from the metagenomes.…”

“…Another unique feature of the BSS was the presence of a bidirectional hydrogenase (hox) and additional genes (hyp), putatively involved in the uptake and photoproduction of molecular hydrogen (Tamagnini et al, 2002). Hydrogenases are widespread in anoxygenic photosynthesizers and other filamentous N-fixing Cyanobacteria (Ludwig et al, 2006), but have recently been observed in planktonic freshwater picocyanobacteria (Di Cesare et al, 2018;Cabello-Yeves et al, 2018). Hence, it appears that the BSS phylotypes have many different mechanisms to produce and incorporate H + .…”

An Environmental Escherichia coli Strain Is Naturally Competent to Acquire Exogenous DNA

“…Sequencing was performed on an Illumina NovaSeq platform using paired-end sequencing of 150 bp fragments at IGA Technologies (Udine, Italy). The genome was assembled as described by Cabello-Yeves et al (2018) : briefly, Trimmomatic was used for read trimming and filtering and SPAdes for the genome assembly, while a preliminary gene annotation was done using NCBI ( Johnson M. et al, 2008 ). This Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBank under the accession JAAWVB000000000 .…”