Screening and functional identification of antioxidant microRNA-size sRNAs from Spirulina platensis using high-throughput sequencing
Dechao Chen A , Shuya Chen A , Chenxi Zhao A , Jin Yan A , Zelong Ma A , Xiaokai Zhao B , Zhenfeng Wang A B C , Xuedong Wang B and Huili Wang
A C
+ Author Affiliations
- Author Affiliations
A School of Environmental Science and Engineering, Suzhou University of Science and Technology, Suzhou 215004, China.
B School of Life Science, Wenzhou Medical University, Wenzhou 325035, China.
C Corresponding authors. Email: whuili@163.com; wangzf@iwaterlab.com
Functional Plant Biology 48(10) 973-983 https://doi.org/10.1071/FP20405
Submitted: 26 December 2020 Accepted: 21 May 2021 Published: 11 June 2021
Abstract
MiRNA-size small RNAs, abbreviated as sRNAs, are increasingly being discovered as research progresses and omics technologies development in prokaryotes. However, there is a paucity of data concerning whether or not sRNAs exist in cyanobacteria and regulate the resistance to oxidative stress. In this investigation, small RNA libraries were constructed from the control, 50-nM and 100-nM H2O2 treatments of Spirulina platensis. By high-throughput sequencing, 23 candidate sRNAs showed significantly differential expression under oxidative stress, among which eight sRNAs were identified with the similar expression patterns as the sequencing results by real-time qPCR. By nucleic acid hybridisation, the corresponding expression changes also demonstrated that sequencing results of sRNAs were feasible and credible. By bioinformatics prediction and structure identification, 43 target genes were predicted for 8 sRNAs in plant miRNA database, among which 29 were annotated into the genome and related metabolic pathways of S. platensis. By COG functional classification and KEGG pathway analysis, 31 target genes were predicted to be directly or indirectly involved in the defence mechanism of H2O2 stress. Thirteen target genes displayed reversely changing patterns compared with those of their sRNAs under H2O2 treatment. These findings provide compelling evidence that these sRNAs in S. platensis play a crucial role in oxidative stress responses, and thus provide a theoretical reference for improving the stress-triggering physiological regulation.
Keywords: Spirulina platensis, sRNAs, target gene, oxidative stress, glycolysis, deep sequencing, chlorophyll metabolism, oxidative stress responses.
References
Alhasawi A, Thomas SC, Appanna VD (2016) Metabolic networks to generate pyruvate, PEP and ATP from glycerol in Pseudomonas fluorescens. Enzyme and Microbial Technology 85, 51–56.| Metabolic networks to generate pyruvate, PEP and ATP from glycerol in Pseudomonas fluorescens.Crossref | GoogleScholarGoogle Scholar | 26920481PubMed |
Almomani F, Bhosale RR (2021) Bio-sorption of toxic metals from industrial wastewater by algae strains Spirulina platensis and Chlorella vulgaris: Application of isotherm, kinetic models and process optimization. The Science of the Total Environment 755, 142654
| Bio-sorption of toxic metals from industrial wastewater by algae strains Spirulina platensis and Chlorella vulgaris: Application of isotherm, kinetic models and process optimization.Crossref | GoogleScholarGoogle Scholar | 33082037PubMed |
Alwaleed EA, El-Sheekh M, Abdel-Daim MM, Saber H (2021) Effects of Spirulina platensis and Amphora coffeaeformis as dietary supplements on blood biochemical parameters, intestinal microbial population, and productive performance in broiler chickens. Environmental Science and Pollution Research International 28, 1801–1811.
| Effects of Spirulina platensis and Amphora coffeaeformis as dietary supplements on blood biochemical parameters, intestinal microbial population, and productive performance in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 32857306PubMed |
Apura P, Saramago M, Peregrina A, Viegas SC, Carvalho SM, Saraiva LM, Arraiano CM, Domingues S (2020) Tailor-made sRNAs: a plasmid tool to control the expression of target mRNAs in Pseudomonas putida. Plasmid 109, 102503
| Tailor-made sRNAs: a plasmid tool to control the expression of target mRNAs in Pseudomonas putida.Crossref | GoogleScholarGoogle Scholar | 32209400PubMed |
Bustos DM, Bustamante CA, Iglesias A (2008) Involvement of non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase in response to oxidative stress. Journal of Plant Physiology 165, 456–461.
| Involvement of non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase in response to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 17913294PubMed |
Chang Y, Wu Z, Bian L, Feng D, Leung DYC (2013) Cultivation of Spirulina platensis For biomass production and nutrient removal from synthetic human urine. Applied Energy 102, 427–431.
| Cultivation of Spirulina platensis For biomass production and nutrient removal from synthetic human urine.Crossref | GoogleScholarGoogle Scholar |
Chen S, Yuan M, Feng W, Liu W, Zhang W, Xu H, Zheng X, Shen G, Guo C, Wang L (2020) Catalytic degradation mechanism of sulfamethazine via photosynergy of monoclinic BiVO4and microalgae under visible-light irradiation. Water Research 185, 116220
| Catalytic degradation mechanism of sulfamethazine via photosynergy of monoclinic BiVO4and microalgae under visible-light irradiation.Crossref | GoogleScholarGoogle Scholar | 32736282PubMed |
Chetri S, Bhowmik D, Dhar (Chanda) D, Chakravarty A, Bhattacharjee A (2019) Effect of concentration gradient carbapenem exposure on expression of blaNDM-1 and acrA in carbapenem resistant Escherichia coli. Infection, Genetics and Evolution 73, 332–336.
| Effect of concentration gradient carbapenem exposure on expression of blaNDM-1 and acrA in carbapenem resistant Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 31170528PubMed |
Conway B, Bechtel LJ, Adler KA, D’Aquila RT, Kaplan JC, Hirsch MS (1992) Comparison of spot-blot and microtitre plate methods for the detection of HIV-1 PCR products. Molecular and Cellular Probes 6, 245–249.
| Comparison of spot-blot and microtitre plate methods for the detection of HIV-1 PCR products.Crossref | GoogleScholarGoogle Scholar | 1406733PubMed |
Deng Y, Su Y, Liu S, Bei L, Guo Z, Li H, Chen C, Feng J (2019) A novel sRNA srvg17985 identified in Vibrio alginolyticus involving into metabolism and stress response. Microbiological Research 229, 126295
| A novel sRNA srvg17985 identified in Vibrio alginolyticus involving into metabolism and stress response.Crossref | GoogleScholarGoogle Scholar | 31450184PubMed |
Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2, e219
| High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes.Crossref | GoogleScholarGoogle Scholar | 17299599PubMed |
Herrera-Vásquez A, Fonseca A, Ugalde JM, Lamig L, Seguel A, Moyano TC, Gutiérrez RA, Salinas P, Vidal EA, Holuigue L (2021) TGA class II transcription factors are essential to restrict oxidative stress in response to UV-B stress in Arabidopsis. Journal of Experimental Botany 72, 1891–1905.
| TGA class II transcription factors are essential to restrict oxidative stress in response to UV-B stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 33188435PubMed |
Hu H, Jia K, Wang H, Xu X, Zhou G, He S (2020) Novel sRNA and regulatory genes repressing the adhesion of Salmonella enteritidis exposed to meat-related environment. Food Control 110, 107030
| Novel sRNA and regulatory genes repressing the adhesion of Salmonella enteritidis exposed to meat-related environment.Crossref | GoogleScholarGoogle Scholar |
Irani S, Todd CD (2018) Exogenous allantoin increases Arabidopsis seedlings tolerance to NaCl stress and regulates expression of oxidative stress response genes. Journal of Plant Physiology 221, 43–50.
| Exogenous allantoin increases Arabidopsis seedlings tolerance to NaCl stress and regulates expression of oxidative stress response genes.Crossref | GoogleScholarGoogle Scholar | 29245127PubMed |
Jiang Y, Liu Y, Zhang J (2020) Antibiotic contaminants reduced the treatment efficiency of UV-C on Microcystis aeruginosa through hormesis. Environmental Pollution 261, 114193
| Antibiotic contaminants reduced the treatment efficiency of UV-C on Microcystis aeruginosa through hormesis.Crossref | GoogleScholarGoogle Scholar | 32088440PubMed |
Jørgensen MG, Pettersen JSH, Kallipolitis B (2020) sRNA-mediated control in bacteria: An increasing diversity of regulatory mechanisms. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms 1863, 194504
| sRNA-mediated control in bacteria: An increasing diversity of regulatory mechanisms.Crossref | GoogleScholarGoogle Scholar |
Kang SM, Choi JW, Lee Y, Hong SH, Lee HJ (2013) Identification of microRNA-size, small RNAs in Escherichia coli. Current Microbiology 67, 609–613.
| Identification of microRNA-size, small RNAs in Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 23783561PubMed |
Kruszka K, Pieczynski M, Windels D, Bielewicz D, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F (2012) Role of microRNAs and other sRNAs of plants in their changing environments. Journal of Plant Physiology 169, 1664–1672.
| Role of microRNAs and other sRNAs of plants in their changing environments.Crossref | GoogleScholarGoogle Scholar | 22647959PubMed |
Li T, Li CT, Butler K, Hays SG, Guarnieri MT, Oyler GA, Betenbaugh MJ (2017) Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. Biotechnology for Biofuels 10, 55
| Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform.Crossref | GoogleScholarGoogle Scholar | 28344645PubMed |
Ling J, Söll D (2010) Severe oxidative stress induces protein mistranslation through impairment of an aminoacyl-tRNA synthetase editing site. Proceedings of the National Academy of Sciences of the United States of America 107, 4028–4033.
| Severe oxidative stress induces protein mistranslation through impairment of an aminoacyl-tRNA synthetase editing site.Crossref | GoogleScholarGoogle Scholar | 20160114PubMed |
Liu B, Sun G (2019) Transcriptome and miRNAs analyses enhance our understanding of the evolutionary advantages of polyploidy. Critical Reviews in Biotechnology 39, 173–180.
| Transcriptome and miRNAs analyses enhance our understanding of the evolutionary advantages of polyploidy.Crossref | GoogleScholarGoogle Scholar | 30372634PubMed |
Liu S, Jiang W, Wu B, Yu J, Yu H, Zhang XX, Torres-Duarte C, Cherr G (2016) Low levels of graphene and graphene oxide inhibit cellular xenobiotic defense system mediated by efflux transporters. Nanotoxicology 10, 597–606.
| Low levels of graphene and graphene oxide inhibit cellular xenobiotic defense system mediated by efflux transporters.Crossref | GoogleScholarGoogle Scholar | 26554512PubMed |
Liu Y, Yang M, Zheng L, Nguyen H, Ni L, Song S, Sui Y (2020) Antioxidant responses of triangle sail mussel Hyriopsis cumingii exposed to toxic Microcystis aeruginosa and thermal stress. The Science of the Total Environment 743, 140754
| Antioxidant responses of triangle sail mussel Hyriopsis cumingii exposed to toxic Microcystis aeruginosa and thermal stress.Crossref | GoogleScholarGoogle Scholar | 32758840PubMed |
Maiti M, Nauwelaerts K, Lescrinier E, Schuit FC, Herdewijn P (2010) Self-complementary sequence context in mature miRNAs. Biochemical and Biophysical Research Communications 392, 572–576.
| Self-complementary sequence context in mature miRNAs.Crossref | GoogleScholarGoogle Scholar | 20097176PubMed |
Marri L, Thieulin-Pardo G, Lebrun R, Puppo R, Zaffagnini M, Trost P, Gontero B, Sparla F (2014) CP12-mediated protection of Calvin-Benson cycle enzymes from oxidative stress. Biochimie 97, 228–237.
| CP12-mediated protection of Calvin-Benson cycle enzymes from oxidative stress.Crossref | GoogleScholarGoogle Scholar | 24211189PubMed |
McFarlane CR, Shah NR, Kabasakal BV, Echeverria B, Cotton CAR, Bubeck D, Murray JW (2019) Structural basis of light-induced redox regulation in the Calvin-Benson cycle in cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America 116, 20984–20990.
| Structural basis of light-induced redox regulation in the Calvin-Benson cycle in cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 31570616PubMed |
Elsonbaty SM, Ismail AFM (2020) Nicotine encourages oxidative stress and impairment of rats’ brain mitigated by Spirulina platensis lipopolysaccharides and low-dose ionizing radiation. Archives of Biochemistry and Biophysics 689, 108382
| Nicotine encourages oxidative stress and impairment of rats’ brain mitigated by Spirulina platensis lipopolysaccharides and low-dose ionizing radiation.Crossref | GoogleScholarGoogle Scholar | 32343976PubMed |
Panyakampol J, Cheevadhanarak S, Sutheeworapong S, Chaijaruwanich J, Senachak J, Siangdung W, Jeamton W, Tanticharoen M, Paithoonrangsarid K (2015) Physiological and transcriptional responses to high temperature in Arthrospira (Spirulina) platensis C1. Plant & Cell Physiology 56, 481–496.
| Physiological and transcriptional responses to high temperature in Arthrospira (Spirulina) platensis C1.Crossref | GoogleScholarGoogle Scholar |
Patel A, Tiwari S, Singh M, Prasad SM (2020) Chapter 17 – Role of sRNAs in abiotic stress tolerance. In ‘Plant Life Under Changing Environment: Responses and Management’. pp. 467-480. (Academic Press: London)
Prosecka J, Orlov AV, Fantin YS, Zinchenko VV, Babykin MM, Tichy M (2009) A novel ATP-binding cassette transporter is responsible for resistance to viologen herbicides in the cyanobacterium Synechocystis sp. PCC 6803. The FEBS Journal 276, 4001–4011.
| A novel ATP-binding cassette transporter is responsible for resistance to viologen herbicides in the cyanobacterium Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 19594831PubMed |
Ranjan T, Kumar M, Prasad BD, Kumar RR, Pal AK, Ansar D, Singh B (2020) Chapter 13 – Cyanobacterial stress-responsive small RNAs (sRNAs): players of stress and developmental responses. In ‘Advances in Cyanobacterial Biology’. (Eds PK Singh, A Kumar, VK Singh, AK Shrivastava.) pp. 195–204. (Academic Press: Cambridge, MA)
Ré DA, Lang PLM, Yones C, Arce AL, Stegmayer G, Milone D, Manavella PA (2019) Alternative use of miRNA-biogenesis co-factors in plants at low temperatures. Development 146, dev172932
| Alternative use of miRNA-biogenesis co-factors in plants at low temperatures.Crossref | GoogleScholarGoogle Scholar | 30760482PubMed |
Serrà A, Artal R, García-Amorós J, Sepúlveda B, Gómez E, Nogués J, Philippe L (2020) Hybrid Ni@ZnO@ZnS-Microalgae for circular economy: a smart route to the efficient integration of solar photocatalytic water decontamination and bioethanol production. Advanced Science (Weinheim, Baden-Wurttemberg, Germany) 7, 1902447
| Hybrid Ni@ZnO@ZnS-Microalgae for circular economy: a smart route to the efficient integration of solar photocatalytic water decontamination and bioethanol production.Crossref | GoogleScholarGoogle Scholar |
Shu PC, Wu C, Ruan XB, Liu W, Fu HY, Wang M, Liu C, Zeng Y, Chen P, Yin B, Yuan JG, Qiang BQ, Peng XZ, Zhong WM (2019) Opposing gradients of microRNA expression temporally pattern layer formation in the developing neocortex. Developmental Cell 49, 764–785.e4.
| Opposing gradients of microRNA expression temporally pattern layer formation in the developing neocortex.Crossref | GoogleScholarGoogle Scholar |
Srisuk T, Pornputtapong N, Cheevadhanarak S, Thammarongtham C (2010) Prediction of non-coding RNA and their targets in Spirulina platensis genome. Communications in Computer and Information Science 115, 106–117.
| Prediction of non-coding RNA and their targets in Spirulina platensis genome.Crossref | GoogleScholarGoogle Scholar |
Tiwari S, Verma N, Prasad SM, Singh VP (2020) Cytokinin alleviates cypermethrin toxicity in Nostoc muscorum by involving nitric oxide: Regulation of exopolysaccharides secretion, PS II photochemistry and reactive oxygen species homeostasis. Chemosphere 259, 127356
| Cytokinin alleviates cypermethrin toxicity in Nostoc muscorum by involving nitric oxide: Regulation of exopolysaccharides secretion, PS II photochemistry and reactive oxygen species homeostasis.Crossref | GoogleScholarGoogle Scholar | 32650176PubMed |
Toyoda T, Okano S, Shibata Y, Abiko Y (2010) Oxidative stress induces phosphorylation of the ABC transporter, ATP-binding protein, in Porphyromonas gingivalis. Journal of Oral Science 52, 561–566.
| Oxidative stress induces phosphorylation of the ABC transporter, ATP-binding protein, in Porphyromonas gingivalis.Crossref | GoogleScholarGoogle Scholar | 21206157PubMed |
Trabelsi S, Ben Mabrouk S, Kriaa M, Ameri R, Sahnoun M, Mezghani M, Bejar S (2019) The optimized production, purification, characterization, and application in the bread making industry of three acid-stable alpha-amylases isoforms from a new isolated Bacillus subtilis strain US586. Journal of Food Biochemistry 43, e12826
| The optimized production, purification, characterization, and application in the bread making industry of three acid-stable alpha-amylases isoforms from a new isolated Bacillus subtilis strain US586.Crossref | GoogleScholarGoogle Scholar | 31353531PubMed |
Wang C, Chao Y, Xu W, Liu Z, Wang H, Huang K (2020) Myeloid FBW7 deficiency disrupts redox homeostasis and aggravates dietary-induced insulin resistance. Redox Biology 37, 101688
| Myeloid FBW7 deficiency disrupts redox homeostasis and aggravates dietary-induced insulin resistance.Crossref | GoogleScholarGoogle Scholar | 32853822PubMed |
Wilson T, Mouriño S, Wilks A (2021) The heme-binding protein PhuS transcriptionally regulates the Pseudomonas aeruginosa tandem sRNA prrF1,F2 locus. The Journal of Biological Chemistry 296, 100275
| The heme-binding protein PhuS transcriptionally regulates the Pseudomonas aeruginosa tandem sRNA prrF1,F2 locus.Crossref | GoogleScholarGoogle Scholar |
Xu T, Ding W, Ao X, Chu X, Wan Q, Wang Y, Xiao D, Yu W, Li M, Yu F, Wang J (2019) ARC regulates programmed necrosis and myocardial ischemia/reperfusion injury through the inhibition of mPTP opening. Redox Biology 20, 414–426.
| ARC regulates programmed necrosis and myocardial ischemia/reperfusion injury through the inhibition of mPTP opening.Crossref | GoogleScholarGoogle Scholar | 30415165PubMed |
Xu S, Yi X, Liu W, Zhang C, Massey IY, Yang F, Tian L (2020) A review of nephrotoxicity of microcystins. Toxins 12, E693
| A review of nephrotoxicity of microcystins.Crossref | GoogleScholarGoogle Scholar | 33142924PubMed |
Yang M, Wang X (2019) Interactions between Microcystis aeruginosa and coexisting bisphenol A at different phosphorus levels. The Science of the Total Environment 658, 439–448.
| Interactions between Microcystis aeruginosa and coexisting bisphenol A at different phosphorus levels.Crossref | GoogleScholarGoogle Scholar | 30579201PubMed |
Yang B, Dai Z, Zhang G, Hu Z, Yao X, Wang S, Liu Q, Zheng X (2020) Ultrasmall ternary FePtMn nanocrystals with acidity-triggered dual-ions release and hypoxia relief for multimodal synergistic chemodynamic/photodynamic/photothermal cancer therapy. Advanced Healthcare Materials 9, 1901634
| Ultrasmall ternary FePtMn nanocrystals with acidity-triggered dual-ions release and hypoxia relief for multimodal synergistic chemodynamic/photodynamic/photothermal cancer therapy.Crossref | GoogleScholarGoogle Scholar | 32959536PubMed |
Zhang BH (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. Journal of Experimental Botany 66, 1749–1761.
| MicroRNA: a new target for improving plant tolerance to abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Zhang B, Unver T (2018) A critical and speculative review on microRNA technology in crop improvement: Current challenges and future directions. Plant Science 274, 193–200.
| A critical and speculative review on microRNA technology in crop improvement: Current challenges and future directions.Crossref | GoogleScholarGoogle Scholar | 30080603PubMed |
Zhao XK, Wang XD, Zhou JP, Chen BB, Zeng AB, Bao QY, Wang HL (2013) Proteomic analysis and qRT-PCR verification of Arthrospira platensis strain YZ under dark stress. Phycologia 52, 538–549.
| Proteomic analysis and qRT-PCR verification of Arthrospira platensis strain YZ under dark stress.Crossref | GoogleScholarGoogle Scholar |
Zhou AP, Zhong YY, Li SQ, Fei X, Gan PH, Zong D, He CZ (2021) Genome-wide identification of polar auxin transporter gene families reveals a possible new polar auxin flow in inverted cuttings of Populus yunnanensis. Gene 772, 145349
| Genome-wide identification of polar auxin transporter gene families reveals a possible new polar auxin flow in inverted cuttings of Populus yunnanensis.Crossref | GoogleScholarGoogle Scholar | 33338511PubMed |
