Strain-specific transcriptional responses overshadow salinity effects in a marine diatom sampled along the Baltic Sea salinity cline

Abstract

The salinity gradient separating marine and freshwater environments represents a major ecological divide for microbiota, yet the mechanisms by which marine microbes have adapted to and ultimately diversified in freshwater environments are poorly understood. Here, we take advantage of a natural evolutionary experiment: the colonization of the brackish Baltic Sea by the ancestrally marine diatom Skeletonema marinoi. To understand how diatoms respond to low salinity, we characterized transcriptomic responses of acclimated S. marinoi grown in a common garden. Our experiment included eight strains from source populations spanning the Baltic Sea salinity cline. Gene expression analysis revealed that low salinities induced changes in the cellular metabolism of S. marinoi, including upregulation of photosynthesis and storage compound biosynthesis, increased nutrient demand, and a complex response to oxidative stress. However, the strain effect overshadowed the salinity effect, as strains differed significantly in their response, both regarding the strength and the strategy (direction of gene expression) of their response. The high degree of intraspecific variation in gene expression observed here highlights an important but often overlooked source of biological variation associated with how diatoms respond to environmental change.

Morphological plasticity in response to salinity change in the euryhaline diatom Pleurosira laevis (Bacillariophyta)

“…In the case of Skeletonema marinoi documented in Pinseel et al. (2022), the optimal salinity for growth also did not necessarily correspond to the salinity conditions of the collection localities (note that this result is different from Sjöqvist et al. 2015, which studied the S. marinoi population from the same locality, i.e., Baltic Sea).…”

Resolving marine–freshwater transitions by diatoms through a fog of discordant gene trees

“…Adaptation to variable environmental conditions may be more likely linked to modifications of gene expression (Wray 2007). In diatoms, exposure to freshwater induces profound changes gene expression related to cellular metabolism, ion transport, photosynthesis, and storage compound biosynthesis (Bussard et al 2017; Nakov et al 2020; Downey et al 2022; Pinseel et al 2022). Diatoms exhibit high levels of inter- and intraspecific variation in gene expression in response to reduced salinity (Nakov et al 2020; Pinseel et al 2022), providing numerous targets for natural selection to optimize gene expression for a particular salinity environment (López-Maury et al 2008; Bedford and Hartl 2009; Gomez-Mestre and Jovani 2013).…”

“…In diatoms, exposure to freshwater induces profound changes gene expression related to cellular metabolism, ion transport, photosynthesis, and storage compound biosynthesis (Bussard et al 2017; Nakov et al 2020; Downey et al 2022; Pinseel et al 2022). Diatoms exhibit high levels of inter- and intraspecific variation in gene expression in response to reduced salinity (Nakov et al 2020; Pinseel et al 2022), providing numerous targets for natural selection to optimize gene expression for a particular salinity environment (López-Maury et al 2008; Bedford and Hartl 2009; Gomez-Mestre and Jovani 2013). Finally, differences in codon usage (Prabha et al 2017), nucleotide substitution rates (Mitterboeck et al 2016), transposable element activity (Yuan et al 2018), epigenetic responses (Artemov et al 2017), and epistatic interactions (Stern et al 2022) have been implicated in adaptation to freshwaters in other groups.…”

“…Indeed, some of these transitions have become some of our most powerful model systems for studying convergent evolution (Elmer and Meyer 2011). Low salinity provokes a broad range of physiological and metabolic responses in diatoms (Nakov et al 2020; Downey et al 2022; Pinseel et al 2022), but the current genetic architectures of freshwater adaptation reflect tens of millions of years of optimization and change since the earliest transitions. As a result, it may not be possible to distinguish the derived alleles that currently allow these diatoms to thrive in freshwaters from the ancestral ones that made the first transitions possible.…”

“…in the response to low salinity (Nakov et al 2020;Downey et al 2022;Pinseel et al 2022), so an adaptive allele in one of the many possible target genes might have made it possible simply to survive in freshwaters initially. In the tens of millions of years since then, the hemiplasious alleles could have been overwritten in one or more freshwater lineages, leaving the shared mechanism itself (e.g., enhanced transport of sodium ions) as the only remaining direct evidence of the hemiplasy.…”