With a pinch of extra salt—Did predatory protists steal genes from their food?

Abstract

The cellular adjustment of Bacteria and Archaea to high-salinity habitats is well studied and has generally been classified into one of two strategies. These are to accumulate high levels either of ions (the “salt-in” strategy) or of physiologically compliant organic osmolytes, the compatible solutes (the “salt-out” strategy). Halophilic protists are ecophysiological important inhabitants of salt-stressed ecosystems because they are not only very abundant but also represent the majority of eukaryotic lineages in nature. However, their cellular osmostress responses have been largely neglected. Recent reports have now shed new light on this issue using the geographically widely distributed halophilic heterotrophic protists Halocafeteria seosinensis, Pharyngomonas kirbyi, and Schmidingerothrix salinarum as model systems. Different approaches led to the joint conclusion that these unicellular Eukarya use the salt-out strategy to cope successfully with the persistent high salinity in their habitat. They accumulate various compatible solutes, e.g., glycine betaine, myo-inositol, and ectoines. The finding of intron-containing biosynthetic genes for ectoine and hydroxyectoine, their salt stress–responsive transcription in H. seosinensis, and the production of ectoine and its import by S. salinarum come as a considerable surprise because ectoines have thus far been considered exclusive prokaryotic compatible solutes. Phylogenetic considerations of the ectoine/hydroxyectoine biosynthetic genes of H. seosinensis suggest that they have been acquired via lateral gene transfer by these bacterivorous Eukarya from ectoine/hydroxyectoine-producing food bacteria that populate the same habitat.

Role of the Extremolytes Ectoine and Hydroxyectoine as Stress Protectants and Nutrients: Genetics, Phylogenomics, Biochemistry, and Structural Analysis

“…The recent discovery of ectoine/5-hydroxyectoine biosynthetic genes in the halophilic protist H. seosinensis [ 100 , 101 ] and the salt-stress-responsive production and import of ectoine in S. salinarum [ 102 ] came at a considerable surprise for scholars of microbial osmostress response systems [ 104 ]. The data reported by Harding et al [ 100 , 101 ] suggest the presence of ectoine/5-hydroxyectoine biosynthetic genes in Eukarya other than H. seosinensis and S. salinarum .…”

“…Producers of ectoines are primarily found among members of the domain of the Bacteria [ 91 , 93 , 99 ] and in a rather restricted number of the Archaea [ 92 ]. Surprisingly, ectoine/5-hydroxyectoine biosynthetic genes and production of ectoine have recently also been detected in some bacteriovorus unicellular Eukarya [ 100 , 101 , 102 ] that live in permanently high-salinity ecosystems [ 103 ]; these protists probably acquired the ectoine/5-hydroxyectoine biosynthetic genes through lateral gene transfer from their food bacteria [ 100 , 104 ].…”

“…Ectoines have so far been considered as compatible solutes exclusively synthesized and used as stress protectants by members of the Bacteria, and by a few Archaea [ 91 , 92 , 93 , 94 ]. Recent studies with halophilic protists now change this picture substantially [ 104 ], since ectoine/5-hydroxyectoine biosynthetic genes have been detected in Halocafeteria seosinensis [ 100 , 101 ] and ectoine production has been directly observed in Schmidingerothrix salinarum [ 102 ]. H. seosinensis is a heterotrophic, borderline extreme halophilic nano-flagelate that actively ingests bacteria as its food source; 18S rRNA-based phylogenetic analysis placed this protist into the stramenophile linage, and it was taxonomically positioned into the order Bicosoecida [ 295 ].…”

“…It is well established that Eukarya can acquire novel metabolic traits and stress resistance determinants by stealing pre-formed gene clusters from microorganisms [ 302 ]. Since ectoines are potent protectants against osmotic, desiccation, and temperature stress, it is highly likely that the acquisition of ect genes by H. seosinensis and S. salinarum from their microbial food prey [ 100 , 101 , 104 ] will provide a distinct growth and survival advantage to these eukaryotic cells in their physiologically challenging high-salinity habitats [ 103 ].…”

Ectoine from Bacterial and Algal Origin Is a Compatible Solute in Microalgae

“…Likewise, in Gram-positive and Gram-negative bacteria, transport systems for compatible solutes are part of the strategy used by microbial cells to overcome stress. Often there are several systems involved in the uptake of these osmolytes in order to provide a robust strategy to counter the adverse condition [32]. Several ectoine transport systems involved in adaptation to osmotic stress, temperature, and nutrient stress conditions were characterized in bacteria and assigned to four different transport families: (i) binding protein-dependent ABC transporters, (ii) major facilitator family (MFS), (iii) BCCT, and (iv) periplasmatic binding protein-dependent tripartite ATP independent periplasmatic transporter family (TRAP-T) [33,34].…”