Functional Tradeoffs Underpin Salinity-Driven Divergence in Microbial Community Composition

Abstract

Bacterial community composition and functional potential change subtly across gradients in the surface ocean. In contrast, while there are significant phylogenetic divergences between communities from freshwater and marine habitats, the underlying mechanisms to this phylogenetic structuring yet remain unknown. We hypothesized that the functional potential of natural bacterial communities is linked to this striking divide between microbiomes. To test this hypothesis, metagenomic sequencing of microbial communities along a 1,800 km transect in the Baltic Sea area, encompassing a continuous natural salinity gradient from limnic to fully marine conditions, was explored. Multivariate statistical analyses showed that salinity is the main determinant of dramatic changes in microbial community composition, but also of large scale changes in core metabolic functions of bacteria. Strikingly, genetically and metabolically different pathways for key metabolic processes, such as respiration, biosynthesis of quinones and isoprenoids, glycolysis and osmolyte transport, were differentially abundant at high and low salinities. These shifts in functional capacities were observed at multiple taxonomic levels and within dominant bacterial phyla, while bacteria, such as SAR11, were able to adapt to the entire salinity gradient. We propose that the large differences in central metabolism required at high and low salinities dictate the striking divide between freshwater and marine microbiomes, and that the ability to inhabit different salinity regimes evolved early during bacterial phylogenetic differentiation. These findings significantly advance our understanding of microbial distributions and stress the need to incorporate salinity in future climate change models that predict increased levels of precipitation and a reduction in salinity.

Microbial Community Structure and Interannual Change in the Last Epishelf Lake Ecosystem in the North Polar Region

“…However, at least one abundant taxon, the eukaryote Radicarteria, was abundant at all depths. Samples were clustered by depths based on the abundance and phylogenetic distances between different rRNA sequences, in contrast to other studies which found that community composition of particleattached and free-living bacteria correlated with different environmental variables (Dupont et al, 2014). This may be because, in the Milne Fiord epishelf lake, most physico-chemical variables are so strongly correlated with depth (Figure 2) that their differing effects cannot be disentangled.…”

Global biogeography of Prochlorococcus genome diversity in the surface ocean

“…Questions regarding the relationship between phylogeny and functional gene diversity are critical to understanding the ecological and evolutionary mechanisms structuring microbial populations (Martiny et al, 2009c;Burke et al, 2011;Raes et al, 2011;Wiedenbeck and Cohan, 2011;Brown et al, 2014;Dupont et al, 2014). Increasing amounts of evidence suggest that using the whole genome rather than simply a single-gene classification is often needed to define microbial lineages and, more importantly, determine its role in the environment (Brown et al, 2014).…”

“…Open reading frames on scaffolds were called using MetaGene (Noguchi et al, 2006). To determine the putative phylogenetic origin of the scaffolds, each predicted peptide was phylogenetically annotated using Automated Phylogenetic Inference System (APIS) (Dupont et al, 2014), which annotates according to the position of the peptide within a phylogenetic tree. Thus a peptide 99% similar to a Prochlorococcus protein will be annotated as Prochlorococcus (with the associated taxonomic tree), while a peptide that branches basally within the phylogenetic tree next to Cyanobacteria would only be annotated as Cyanobacteria.…”

Salinity influences disease-induced mortality of the oyster Crassostrea gigas and infectivity of the ostreid herpesvirus 1 (OsHV-1)

“…Indeed, several non-pathogenic bacteria contribute to the mortality of oysters (Lemire et al 2015), and salinity is a major factor shaping the bacterial community in marine ecosystems (Herlemann et al 2011, Dupont et al 2014.…”