Physiological and Molecular Responses to Main Environmental Stressors of Microalgae and Bacteria in Polar Marine Environments
Abstract
:1. Introduction
Environmental Factors Driving Microbial Life in Cold Marine Environments
2. Microalgae
2.1. Salinity
2.2. Light
2.3. Nutrient
2.4. pH
2.5. Temperature
2.6. -Omics Studies on Microalgae from Cold Environments
3. Bacteria
3.1. Physiological Responses to Environmental Stressors
3.2. -Omics Studies on Bacteria from Cold Environments
4. Phyto-Bacterioplankton Interactions in Cold Environments
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Stress Exposure | Main Effects/Responses | Reference |
---|---|---|
Physiological changes | ||
Low salt concentration | Increase in specific growth rate, biochemical composition shifting towards a lower POC:PON relationship with higher protein content, but reduced fatty acid and carbohydrate content. | [27,44] |
High salt concentration | Slowing down of cell division and growth rate, reduced cell size and motility, triggering “palmelloid” formation in Chlamydomonas, production of osmoregulatory compounds (e.g., glycerol and proline), increase in ion transmembrane transport and lipids. In the sea-ice diatom, Nitzschia lecointei, small changes in growth rate, effect on cellular metabolite pool sizes | [46,47,48] |
High levels of ultraviolet radiation (UVR) | Increase in photoprotective pigments | [49,50] |
Reduction in photosynthetic rate | [51] | |
Inactivation of specific enzymes | ||
affecting species diversity and richness. | ||
Increase in saturated fatty acids, decrease in polyunsaturated fatty acids (PUFAs), small increase in C18 PUFAs | [52] | |
Low light exposure | Protection from UVR | |
Limitation in primary production | ||
Nutrients: Fe limitation | Influence in microalgal growth and composition | [53] |
Increase in lipid production | [54] | |
Low pH | Increase in large diatoms, early senescence | [55] |
Increase in photosynthetic rate and growth rate | ||
Affecting membrane potential, energy partitioning and enzyme activity | [56] | |
Low temperature | Maintenance of membrane fluidity thanks to unsaturated fatty acids | [57] |
Maintenance of sufficient rates of enzyme-catalyzed reactions for key metabolic processes | ||
Evolution of cold shock and antifreeze proteins | ||
Photosynthetic electron transport chain adaptations | ||
Molecular changes | ||
Genome comparison between cold-adapted and temperate species | In the cold-adapted genome there were highly divergent alleles which were also differentially expressed across various environmental conditions. Main genes identified for cold adaptation were ice-binding proteins IBPs, proton-pumping proteorhodopsins and chlorophyll a/c light-harvesting complex LHC. | [58] |
Low temperature, high light | Genes encoding proteins of PSII (psbA, psbC) and for carbon fixation (rbcL) were down-regulated | [59] |
Chaperones (hsp70) and genes for plastid protein synthesis and turnover (elongation factor EfTs, ribosomal protein rpS4, ftsH protease) were up-regulated | ||
Low temperature, low light | Down-regulation of psbA, psbC, and rbcL | [59] |
Low temperature, high salinity | Ionic transporters and antiporters, heat shock proteins, genes related to oxidative stress, and three key genes involved in proline synthesis | [60] |
Low temperature | Expression of various DEAD-box RNA helicase genes, such as CiRH5, CiRH25, CiRH28, and CiRH55, were found significantly up-regulated under freezing treatment | [61] |
Increase in genes encoding proteins involved in protein translation and transport, including protein transport protein SEC61, signal recognition particle protein, protein involved in vacuolar protein sorting. Increase in Heat shock protein 70, matrix metalloproteinase M11, X-Pro dipeptidyl-peptidase, and protein binding 26S proteasome regulatory complex, nitrate reductase, ferredoxin-nitrite reductase, and nitrate/nitrite transporter. | [62] | |
Increased temperature | Up-regulation of cytoprotective genes, down-regulation of genes related to photosynthesis, increase in fucoxanthin chlorophyll a/c-binding proteins | [63] |
High light | Transcripts related to photosynthesis were affected | [64] |
Identification of an antifreeze protein gene (Cn-AFP) | [65] | |
High salinity | Increased expression of genes participating in the metabolism of carbohydrates, such as starch, sucrose, soluble sugar, and glucose | [66] |
Stress Exposure | Main Effects/Responses | Reference |
---|---|---|
Physiological changes | ||
Low temperature | Reduction of primary metabolism | [111] |
Modulation of PUFA amount for membrane fluidity maintenance, modulation of proteins and carotenoids | [91,112,113,114] | |
Peptidoglycan thickening | [115,116] | |
LPS lacking O-chain component | [117] | |
Increase in short chain and/or unsaturated fatty acids | [117,118] | |
Increase in enzymes with high catalytic activity | [91,119] | |
Increase in antifreeze (AFPs) and ice nucleating (INPs) proteins | [120,121] | |
Increase in cryoprotective compounds, including compatible solutes, extracellular polymeric substances (EPSs) and polyhydroxyalkanoates (PHAs) | [116] | |
Molecular changes | ||
Genomic observations | Common genetic traits include those related to oxidative stress, metabolism and energy and nutrient acquisition, cell wall membrane structure and fatty acid biosynthesis, production of cold-shock protein (CSP) and chaperones, production of exopolysaccharides or other extracellular substances, biosynthesis or transport of compatible solutes (i.e., glycine betaine, ectoine, and trehalose), and presence of genes involved in antioxidant activity, such as superoxide dismutase, glutathione peroxidase, glutathione reductase, catalase, aconitase, thioredoxin and ascorbic acid | [122,123] |
Glycogen synthesis genes | [124] | |
Presence of gene cluster encoding for glycogen synthase and 4-oxoacyl-ACP reductase, putative secondary metabolite biosynthesis gene clusters for terpene, nonribosomal peptide synthetase (NRPS), and different polyketide synthases (T1PKS and T3PKS) | [125] | |
Presence of genes related to exopolysaccharide and polyunsaturated fatty acid biosynthesis, or involved in nutrient acquisition, production of proteins associated with ice-binding and light-sensing processes | [122] | |
Reduced G+C content and peculiar composition for certain aminoacids to increase protein flexibility | [126] | |
Transcriptome analyses at low temperature | Up-regulation of transcripts involved in oxidative stress, CSP and chaperone production, metabolism and energy management, membrane fluidity assessment | [127] |
Up-regulation of genes involved in ethanol oxidation (exaA, exaB and ExaC) encoding for a pyrroloquinoline quinone (PQQ)-dependent ethanol dehydrogenase, a cytochrome c550 and an aldehyde dehydrogenase | [128] | |
Induction of transcripts encoding for antioxidants (suggested by the up-regulation of sodA, bcp and bpoA2), and of genes encoding for key enzymes of the glioxylate cycle (isocitrate lyase and malate synthase) | [129] | |
Expression for several protein families (i.e., membrane and regulatory proteins, metabolic proteins, especially those involved in NADH and NADPH generation), DNA metabolism and translation apparatus components resulted up-regulated | [130] | |
Down-regulation of genes involved in transcription, translation, energy production, and most biosynthetic pathways was evidenced, while genes for specific biosynthesis processes (proline, tryptophan, and methionine), chaperones clpB and hsp33, RNases and peptidases were generally up-regulated | [131] | |
Up-regulation of genes for translation, ribosomal structure and biogenesis and a down-regulation of lipid transport and metabolism | [132] | |
Proteome analysis at low temperature | Up-regulation was detected for proteins involved in metabolite transport, protein folding, membrane fluidity and aminoacid biosynthesis (protein MetF, ScoB and MmsA). Proteins related to energy production and conversion were down-regulated | [132] |
Multi-omics (Genomic and Phenomic) analysis | High metabolic versatility, capacity to enhance the uptake of compounds with peculiar role in cryoprotection (i.e., spermine, glutathione, ornithine and other compounds related to glutathione metabolism). Enrichment in genes involved in lipid transport and metabolism and an up-regulation of protein synthesis metabolism | [2] |
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Lauritano, C.; Rizzo, C.; Lo Giudice, A.; Saggiomo, M. Physiological and Molecular Responses to Main Environmental Stressors of Microalgae and Bacteria in Polar Marine Environments. Microorganisms 2020, 8, 1957. https://doi.org/10.3390/microorganisms8121957
Lauritano C, Rizzo C, Lo Giudice A, Saggiomo M. Physiological and Molecular Responses to Main Environmental Stressors of Microalgae and Bacteria in Polar Marine Environments. Microorganisms. 2020; 8(12):1957. https://doi.org/10.3390/microorganisms8121957
Chicago/Turabian StyleLauritano, Chiara, Carmen Rizzo, Angelina Lo Giudice, and Maria Saggiomo. 2020. "Physiological and Molecular Responses to Main Environmental Stressors of Microalgae and Bacteria in Polar Marine Environments" Microorganisms 8, no. 12: 1957. https://doi.org/10.3390/microorganisms8121957