Towards deciphering dynamic changes and evolutionary mechanisms involved in the adaptation to low salinities in Ectocarpus (brown algae)

Abstract

Colonizations of freshwater by marine species are rare events, and little information is known about the underlying mechanisms. Brown algae are an independent lineage of photosynthetic and multicellular organisms from which few species inhabit freshwater. As a marine alga that is also found in freshwater, Ectocarpus is of particular interest for studying the transition between these habitats. To gain insights into mechanisms of the transition, we examined salinity tolerance and adaptations to low salinities in a freshwater strain of Ectocarpus on physiological and molecular levels. We show that this isolate belongs to a widely distributed and highly stress-resistant clade, and differed from the genome-sequenced marine strain in its tolerance of low salinities. It also exhibited profound, but reversible, morphological, physiological, and transcriptomic changes when transferred to seawater. Although gene expression profiles were similar in both strains under identical conditions, metabolite and ion profiles differed strongly, the freshwater strain exhibiting e.g. higher cellular contents of amino acids and nitrate, higher contents of n-3 fatty acids, and lower intracellular mannitol and sodium concentrations. Moreover, several stress markers were noted in the freshwater isolate in seawater. This finding suggests that, while high stress tolerance and plasticity may be prerequisites for the colonization of freshwater, genomic alterations have occurred that produced permanent changes in the metabolite profiles to stabilize the transition.

Host–microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures

“…Exclusively vegetative reproduction in the sporophyte life cycle stage has previously been reported in Fucus populations adapted to low salinities in the Baltic Sea (Tatarenkov et al, 2005), and the freshwater strain 371 is indeed a sporophyte that, to our knowledge, has never produced haploid gametophytes in a laboratory setting (see Charrier et al, 2008 for a review of the Ectocarpus life cycle). In connection with this, we have previously identified the alga's capacity to modify its cell wall composition, and in particular the degree of sulfation, as another possible factor for acclimation (Dittami et al, 2012;Torode et al, 2015). Here, we have shown that bacteria also have a role in algal acclimation, but so far, there was no indication that they produce compounds that specifically aid algae to acclimate to freshwater.…”

“…All experiments were carried out in triplicates and yielded highly similar results, but only one replicate is shown here. Differences in morphology between algae cultivated in DSWM and SWM have been previously described (Dittami et al, 2012), and may be related to the described differences in the bacterial phycosphere. …”

“…Particularly high tolerance ranges were observed with respect to salinity: while most Ectocarpus isolates are marine, at least one strain was isolated from a true freshwater habitat at Hopkins River Falls, Australia (West and Kraft, 1996). This freshwater strain (strain 371) is able to grow in both freshwater and seawater, adjusting its metabolism and cell wall structure to the corresponding conditions (Dittami et al, 2012;Meslet-Cladière et al, 2013;Torode et al, 2015). In addition, Ectocarpus strains related to the freshwater strain based on their internal transcribed spacer sequences, have been found in other 'extreme' environments, such as on driftwood, or in areas of highly variable temperature (Bolton, 1983).…”

“…The transition from marine environments to freshwater is a particularly rare event in brown algae, and only about 1% of brown algal species have colonized this habitat (Bold and Wynne, 1985). Although the exact taxonomic position of the freshwater strain and its relatives remains to be established, they do not belong to the genome-sequenced Ectocarpus siliculosus but constitute a sister species (Dittami et al, 2011) that has separated from E. siliculosus roughly 16 million years ago (Dittami et al, 2012).…”

Structure/Function Analysis of a Type III Polyketide Synthase in the Brown Alga Ectocarpus siliculosus Reveals a Biochemical Pathway in Phlorotannin Monomer Biosynthesis

“…These strains are adapted to marine (Ectocarpus [Ec] 32 genome-sequenced strain) and freshwater (Ec 371) environments, respectively, and were recently compared at a transcriptional and metabolic level to study the mechanisms that may allow the transition between these habitats (Dittami et al, 2012a). As shown in Supplemental Figure 3 online, phloroglucinol was identified from total ion chromatograms of extracts prepared from these isolates by extracted ion monitoring at a m/z of 342 and retention time of 46.8 min, and the corresponding mass spectra for the peaks revealed characteristic fragment ions supporting this identification and similar retention time as the authentic standard (see Supplemental Figure 3C online).…”