Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates

Abstract

Background Cyanobacteria are the major prokaryotic primary producers occupying a range of aquatic habitats worldwide that differ in levels of salinity, making them a group of interest to study one of the major unresolved conundrums in aquatic microbiology which is what distinguishes a marine microbe from a freshwater one? We address this question using ecogenomics of a group of picocyanobacteria (cluster 5) that have recently evolved to inhabit geographically disparate salinity niches. Our analysis is made possible by the sequencing of 58 new genomes from freshwater representatives of this group that are presented here, representing a 6-fold increase in the available genomic data. Results Overall, freshwater strains had larger genomes (≈2.9 Mb) and %GC content (≈64%) compared to brackish (2.69 Mb and 64%) and marine (2.5 Mb and 58.5%) isolates. Genomic novelties/differences across the salinity divide highlighted acidic proteomes and specific salt adaptation pathways in marine isolates (e.g., osmolytes/compatible solutes - glycine betaine/ggp/gpg/gmg clusters and glycerolipids glpK/glpA), while freshwater strains possessed distinct ion/potassium channels, permeases (aquaporin Z), fatty acid desaturases, and more neutral/basic proteomes. Sulfur, nitrogen, phosphorus, carbon (photosynthesis), or stress tolerance metabolism while showing distinct genomic footprints between habitats, e.g., different types of transporters, did not obviously translate into major functionality differences between environments. Brackish microbes show a mixture of marine (salt adaptation pathways) and freshwater features, highlighting their transitional nature. Conclusions The plethora of freshwater isolates provided here, in terms of trophic status preference and genetic diversity, exemplifies their ability to colonize ecologically diverse waters across the globe. Moreover, a trend towards larger and more flexible/adaptive genomes in freshwater picocyanobacteria may hint at a wider number of ecological niches in this environment compared to the relatively homogeneous marine system.

Adaptive genetic traits in pelagic freshwater microbes

“…Rhodanases, (aryl)sulfatases and ABC transporters for sulfate (e.g. CysWT, CysPA) were detected in freshwater members, but not in marine isolates, probably as adaptations to limited sulfur amounts available in freshwater systems (Cabello‐Yeves, Callieri, et al, 2022; Cabello‐Yeves, Scanlan, et al, 2022). As expected, genes involved in the transport and biosynthesis of compatible solutes (betaine biosynthesis/transport–sarcosine N ‐methyltransferase, dimethylglycine N ‐methyltransferase; high‐affinity choline uptake protein BetP) are only present in marine and/or brackish isolates, providing a molecular basis for the salinity divide (Cabello‐Yeves, Callieri, et al, 2022; Cabello‐Yeves, Scanlan, et al, 2022).…”

Linking prokaryotic genome size variation to metabolic potential and environment

“…Within freshwater ecosystems, isolates from the family Methylophilaceae (class Gammaproteobacteria) show a smaller genome size for pelagic than for sediment dwellers [ 20 ]. Additionally, two studies have shown that marine Cyanobacteria have smaller genome sizes than freshwater [ 21 , 22 ]. This literature already provides some insights on how genome size is linked to the environmental heterogeneity of freshwater and marine ecosystems.…”

Linking prokaryotic genome size variation to metabolic potential and environment

“…The copyright holder for this preprint this version posted October 21, 2022. ; https://doi.org/10.1101/2022.10.20.512849 doi: bioRxiv preprint freshwaters (Hugerth et al, 2015), while picocyanobacteria show the opposite trend (Cabello-Yeves et al, 2022). Further research must be done to understand how genome sizes vary between and within different aquatic environments, particularly brackish water bodies including pelagic and benthic microorganisms.…”

“…Within freshwater ecosystems, we can observe that isolates from the family Methylophilaceae (class Gammaproteobacteria) show a decrease in genome size in the transition from sediments to pelagic forms (Salcher et al, 2019). Additionally, several studies have shown that marine microbes have smaller genome sizes than freshwater microorganisms (Cabello-Yeves et al, 2022; Chen et al, 2021; Rodríguez-Gijón et al, 2022). Yet, genome size variation in the brackish realm remains debated: Actinobacteria in the brackish Baltic Sea show bigger genome sizes than in freshwaters (Hugerth et al, 2015), while picocyanobacteria show the opposite trend (Cabello-Yeves et al, 2022).…”

“…Additionally, several studies have shown that marine microbes have smaller genome sizes than freshwater microorganisms (Cabello-Yeves et al, 2022; Chen et al, 2021; Rodríguez-Gijón et al, 2022). Yet, genome size variation in the brackish realm remains debated: Actinobacteria in the brackish Baltic Sea show bigger genome sizes than in freshwaters (Hugerth et al, 2015), while picocyanobacteria show the opposite trend (Cabello-Yeves et al, 2022). Further research must be done to understand how genome sizes vary between and within different aquatic environments, particularly brackish water bodies including pelagic and benthic microorganisms.…”