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

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.

[1]  A. Simpson,et al.  Recent Advances in Halophilic Protozoa Research , 2018, The Journal of eukaryotic microbiology.

[2]  Kerwyn Casey Huang,et al.  Regulation of microbial growth by turgor pressure. , 2018, Current opinion in microbiology.

[3]  S. Filker,et al.  Identification of osmoadaptive strategies in the halophile, heterotrophic ciliate Schmidingerothrix salinarum , 2018, PLoS biology.

[4]  J. Theriot,et al.  Homeostatic Cell Growth Is Accomplished Mechanically through Membrane Tension Inhibition of Cell-Wall Synthesis. , 2017, Cell systems.

[5]  J. McCutcheon,et al.  Functional horizontal gene transfer from bacteria to eukaryotes , 2017, Nature Reviews Microbiology.

[6]  E. Bremer,et al.  Tinkering with Osmotically Controlled Transcription Allows Enhanced Production and Excretion of Ectoine and Hydroxyectoine from a Microbial Cell Factory , 2017, Applied and Environmental Microbiology.

[7]  Jeroen S. Dickschat,et al.  Transcriptional regulation of ectoine catabolism in response to multiple metabolic and environmental cues , 2017, Environmental microbiology.

[8]  R. Rosselló-Móra,et al.  Transition boundaries for protistan species turnover in hypersaline waters of different biogeographic regions , 2017, Environmental microbiology.

[9]  M. Moran,et al.  Bacterial transcriptome remodeling during sequential co-culture with a marine dinoflagellate and diatom , 2017, The ISME Journal.

[10]  A. Simpson,et al.  Adaptations to High Salt in a Halophilic Protist: Differential Expression and Gene Acquisitions through Duplications and Gene Transfers , 2017, Front. Microbiol..

[11]  S. Sukharev,et al.  Tension-activated channels in the mechanism of osmotic fitness in Pseudomonas aeruginosa , 2017, The Journal of general physiology.

[12]  G. Pielak,et al.  Osmotic Shock Induced Protein Destabilization in Living Cells and Its Reversal by Glycine Betaine. , 2017, Journal of molecular biology.

[13]  Haiwei Luo,et al.  Evolution of Dimethylsulfoniopropionate Metabolism in Marine Phytoplankton and Bacteria , 2017, Front. Microbiol..

[14]  A. Boersma,et al.  Microorganisms maintain crowding homeostasis , 2017, Nature Reviews Microbiology.

[15]  A. Roger,et al.  Lateral Gene Transfer in the Adaptation of the Anaerobic Parasite Blastocystis to the Gut , 2017, Current Biology.

[16]  D. Moreira,et al.  Protist Evolution: Stealing Genes to Gut It Out , 2017, Current Biology.

[17]  Matthew W. Brown,et al.  Osmoadaptative Strategy and Its Molecular Signature in Obligately Halophilic Heterotrophic Protists , 2016, Genome biology and evolution.

[18]  Jeroen S. Dickschat,et al.  Strangers in the archaeal world: osmostress-responsive biosynthesis of ectoine and hydroxyectoine by the marine thaumarchaeon Nitrosopumilus maritimus. , 2016, Environmental microbiology.

[19]  Lewis Stevens,et al.  No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini , 2016, Proceedings of the National Academy of Sciences.

[20]  J. Claverie,et al.  Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing. , 2015, Environmental microbiology.

[21]  A. Oren The ecology of Dunaliella in high-salt environments , 2014, Journal of Biological Research-Thessaloniki.

[22]  S. Hohmann An integrated view on a eukaryotic osmoregulation system , 2014, Current Genetics.

[23]  Erin A. Becker,et al.  Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response , 2014, PLoS genetics.

[24]  J. Heider,et al.  Biochemical Properties of Ectoine Hydroxylases from Extremophiles and Their Wider Taxonomic Distribution among Microorganisms , 2014, PloS one.

[25]  I. Booth,et al.  Bacterial mechanosensitive channels: progress towards an understanding of their roles in cell physiology☆ , 2014, Current opinion in microbiology.

[26]  E. Girard,et al.  An experimental point of view on hydration/solvation in halophilic proteins , 2014, Front. Microbiol..

[27]  C. Gostinčar,et al.  Adaptation to high salt concentrations in halotolerant/halophilic fungi: a molecular perspective , 2014, Front. Microbiol..

[28]  A. Oren Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes , 2013, Front. Microbiol..

[29]  N. Youssef,et al.  Trehalose/2-sulfotrehalose biosynthesis and glycine-betaine uptake are widely spread mechanisms for osmoadaptation in the Halobacteriales , 2013, The ISME Journal.

[30]  J. Banfield,et al.  Gene Transfer from Bacteria and Archaea Facilitated Evolution of an Extremophilic Eukaryote , 2013, Science.

[31]  Douglas W. Raiford,et al.  An Extremely Halophilic Proteobacterium Combines a Highly Acidic Proteome with a Low Cytoplasmic Potassium Content* , 2012, The Journal of Biological Chemistry.

[32]  Liran Carmel,et al.  Origin and evolution of spliceosomal introns , 2012, Biology Direct.

[33]  J. M. Wood Bacterial osmoregulation: a paradigm for the study of cellular homeostasis. , 2011, Annual review of microbiology.

[34]  A. Oren Thermodynamic limits to microbial life at high salt concentrations. , 2011, Environmental microbiology.

[35]  E. Bremer,et al.  Ectoine and Hydroxyectoine as Protectants against Osmotic and Cold Stress: Uptake through the SigB-Controlled Betaine-Choline- Carnitine Transporter-Type Carrier EctT from Virgibacillus pantothenticus , 2011, Journal of bacteriology.

[36]  E. Rocha,et al.  Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes , 2011, PLoS genetics.

[37]  M. Salvador,et al.  Ectoines in cell stress protection: uses and biotechnological production. , 2010, Biotechnology advances.

[38]  Waldemar Vollmer,et al.  Architecture of peptidoglycan: more data and more models. , 2010, Trends in microbiology.

[39]  Nuno Empadinhas,et al.  Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. , 2008, International microbiology : the official journal of the Spanish Society for Microbiology.

[40]  M. Burg,et al.  Intracellular Organic Osmolytes: Function and Regulation* , 2008, Journal of Biological Chemistry.

[41]  G. Rose,et al.  A molecular mechanism for osmolyte-induced protein stability , 2006, Proceedings of the National Academy of Sciences.

[42]  L. Gierasch,et al.  Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant , 2006, Proceedings of the National Academy of Sciences.

[43]  A. Simpson,et al.  Halocafeteria seosinensis gen. et sp. nov. (Bicosoecida), a halophilic bacterivorous nanoflagellate isolated from a solar saltern , 2006, Extremophiles.

[44]  J. Thevelein,et al.  Why do microorganisms have aquaporins? , 2006, Trends in microbiology.

[45]  P. Yancey,et al.  Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses , 2005, Journal of Experimental Biology.

[46]  Peter Agre,et al.  From structure to disease: the evolving tale of aquaporin biology , 2004, Nature Reviews Molecular Cell Biology.

[47]  V. Müller,et al.  Osmoadaptation in bacteria and archaea: common principles and differences. , 2001, Environmental microbiology.

[48]  T. Reinikainen,et al.  Extreme Halophiles Synthesize Betaine from Glycine by Methylation* , 2000, The Journal of Biological Chemistry.

[49]  D. Welsh,et al.  Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. , 2000, FEMS microbiology reviews.

[50]  E. Bremer Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes in B. subtilis , 2000 .

[51]  Long-Fei Wu,et al.  Glycine Betaine-assisted Protein Folding in a lysAMutant of Escherichia coli * , 2000, The Journal of Biological Chemistry.

[52]  E. Bremer,et al.  Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments , 1998, Archives of Microbiology.

[53]  A. D. Brown,et al.  Microbial water stress. , 1976, Bacteriological reviews.

[54]  D. Caron,et al.  Protists are microbes too: a perspective , 2009, The ISME Journal.

[55]  E. Bremer Coping with osmotic challenges : osmoregulation through accumulation and release of compatible solutes in bacteria , 2000 .