Enhancement of exopolysaccharides production and reactive oxygen species level of Nostoc flagelliforme in response to dehydration.

Publisher: Springer Country of Publication: Germany NLM ID: 9441769 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1614-7499 (Electronic) Linking ISSN: 09441344 NLM ISO Abbreviation: Environ Sci Pollut Res Int Subsets: MEDLINE

Publication: <2013->: Berlin : Springer
Original Publication: Landsberg, Germany : Ecomed

Dehydration* ; Nostoc*/genetics; Humans ; Oxidation-Reduction ; Reactive Oxygen Species

Nostoc flagelliforme is a remarkable drought-resistant terrestrial cyanobacterium whose exopolysaccharides (EPS) have been found to exert important physiological and ecological functions, and the EPS are known to improve soil physicochemical properties. In this study, we used physiological and molecular methods to investigate the influences of three moisture loss levels on EPS production and the antioxidant system in N. flagelliforme. The aim was to reveal the EPS production mechanism involved in the gene differential expression and antioxidant system of N. flagelliforme in response to drought. Our results showed that EPS contents increased by 13% and 22% after 6-h and 48-h dehydration (6HAD and 48HAD) compared with 4-h rehydration (4HAR), respectively. The same trends were also detected for most EPS synthesis genes, especially glycosyltransferases. Furthermore, the intracellular reactive oxygen species (ROS) levels in N. flagelliforme were generally higher at 6HAD and 48HAD than at 4HAR. Superoxide dismutase (SOD) and peroxidase (POD) activities were restricted in N. flagelliforme under 6HAD and 48HAD compared with 4HAR, but the opposite result was found in catalase (CAT) activity. These results provide a new foundation for understanding the mechanism of EPS accumulation in N. flagelliforme in response to drought.
(© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature.)

Adessi A, Cruz de Carvalho R, De Phillippis R, Branquinho C, Marques D, Silva J (2018) Microbial extracellular polymeric substances improve water retention in dryland biological soil crusts. Soil Biol Biochem 116:67–69. (PMID: 10.1016/j.soilbio.2017.10.002)
Ahmada B, Azeema F, Alib MA, Nawazd MA, Nadeema H, Abbasb A, Batoole R, Atiff RM, Ijaza U, Nieves-Cordonesh M, Chung G (2020) Genome-wide identification and expression analysis of two component system genes in Cicer arietinum. Genomics 112:1371–1383. (PMID: 10.1016/j.ygeno.2019.08.006)
Anders S (2010) HTSeq: analysing high-throughput sequencing data with Python.
Anders S, Huber W (2012) Differential expression of RNA-Seq data at the gene level-the DESeq package. European Molecular Biology Laboratory (EMBL), Heidelberg. pp 24.
Belnap J, Phillips SL, Flint SD, Money J, Caldwell MM (2008) Global change and biological soil crusts: effects of ultraviolet augmentation under altered precipitation regimes and nitrogen additions. Glob Chang Biol 14:670–686. (PMID: 10.1111/j.1365-2486.2007.01509.x)
Bergman B, Gallon JR, Rai AN, Stal LJ (1997) N 2 -fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19:139–185. (PMID: 10.1016/S0168-6445(96)00028-9)
Bhaskar PV, Bhosle NB (2005) Microbial extracellular polymeric substances in marine geochemical processes. Curr Sci 88:45–53.
Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, Delucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33:1597–1613. (PMID: 10.1111/j.1365-3040.2010.02167.x)
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. (PMID: 10.1016/0003-2697(76)90527-3)
Cameron RE (1962) Species of Nostoc voucher occurring in the Sonoran Desert in Arizona. Trans Am Microsc Soc 81:379–384. (PMID: 10.2307/3223790)
Capra EJ, Laub MT (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66:325–347. (PMID: 10.1146/annurev-micro-092611-150039)
Chen F, Schnick S, Schroder P (2018) Concentration effects of the UV filter oxybenzone in Cyperus alternifolius: assessment of tolerance by stress-related response. Environ Sci Pollut Res Int 25:16080–16090. (PMID: 10.1007/s11356-018-1839-z)
Cristiano S, Carvalho MEA, Azevedo RA, Fidalgo F (2018) Plants facing oxidative challenges-A little help from the antioxidant networks. Environ Exp Bot 161:4–25.
De Philippis R, Margheri MC, Materassi R, Vincenzini M (1998) Potential of unicellular cyanobacteria from saline environments as exopolysaccharide producers. Appl Environ Microbiol 64:1130–1132. (PMID: 10.1128/AEM.64.3.1130-1132.1998)
Diekmann F, Nepovim A, Schröder P (2004) Influence of Serratia liquefaciens and a xenobiotic glutathione conjugate on the detoxification enzymes in a hairy root culture of horseradish (Armoracia rusticana). J Appl Bot 78:64–67.
Dubois M, Gilles KA, Harmilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. (PMID: 10.1021/ac60111a017)
Ekman M, Sandh G, Nenninger A, Oliveira P, Stensjo K (2014) Cellular and functional specificity among ferritin-like proteins in the multicellular cyanobacterium Nostoc punctiforme. Environ Microbiol 16:829–844. (PMID: 10.1111/1462-2920.12233)
Elsner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Annu Biochem 70:616–620. (PMID: 10.1016/0003-2697(76)90488-7)
Fresnedo O, Serra JL (1992) Effect of nitrogen starvation on the biochemistry of Phormidium laminosum (Cyanophyceae). J Phycol 28:786–793. (PMID: 10.1111/j.0022-3646.1992.00786.x)
Gao X, Ai YF, Qiu BS (2012) Drought adaptation of a terrestrial macroscopic cyanobacterium, Nostoc flagelliforme, in arid areas: a review. Afr J Microbiol Res 6:5728–5735.
Gao X, Liu LT, Liu B (2019) Dryland cyanobacterial exopolysaccharides show protection against acid deposition damage. Environ Sci Pollut Re 26:24300–24304. (PMID: 10.1007/s11356-019-05798-4)
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. (PMID: 10.1016/j.plaphy.2010.08.016)
Graham N, Amna M, Christine HF (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648. (PMID: 10.1104/pp.113.233478)
Han PP, Sun Y, Jia SR, Zhong C, Tan ZL (2014) Effects of light wavelengths on extracellular and capsular polysaccharide production by Nostoc flagelliforme. Carbohydr Polym 105:145–151. (PMID: 10.1016/j.carbpol.2014.01.061)
Han PP, Shen SG, Wang HY, Sun Y, Dai YJ, Jia SR (2015) Comparative metabolomic analysis of the effects of light quality on polysaccharide production of cyanobacterium Nostoc flagelliforme. Algal Res 9:143–150. (PMID: 10.1016/j.algal.2015.02.019)
Han PP, Shen SG, Wang HY, Yao SY, Tan ZL, Zhong C, Jia SR (2017) Applying the strategy of light environment control to improve the biomass and polysaccharide production of Nostoc flagelliforme. J Appl Phycol 29:55–65. (PMID: 10.1007/s10811-016-0963-8)
Han PP, Guo RJ, Shen SG, Yan RR, Wu YK, Yao SY, Wang HY, Jia SR (2018) Proteomic profiling of Nostoc flagelliforme reveals the common mechanism in promoting polysaccharide production by different light qualities. Biochem Eng J 132:68–78. (PMID: 10.1016/j.bej.2017.12.006)
Han PP, Shen SG, Guo RJ, Zhao DX, Lin YH, Jia SR, Yan RR, Wu YK (2019) ROS is a factor regulating the increased polysaccharide production by light quality in the edible cyanobacterium Nostoc flagelliforme. J Agric Food Chem 67:2235–2244. (PMID: 10.1021/acs.jafc.8b06176)
Hill DR, Keenan TW, Felm HR, Potts M, Crowe LM, Crowe JH (1997) Extracellular polysaccharide of Nostoc commune (Cyanobacteria) inhibits fusion of membrane vesicles during dessication. J Appl Phycol 9:237–248. (PMID: 10.1023/A:1007965229567)
Huang LF, Lin JY, Pan KY, Huang CK, Chu YK (2015) Overexpressing ferredoxins in Chlamydomonas reinhardtii increase starch and oil yields and enhance electric power production in a photo microbial fuel cell. Int J Mol Sci 16:19308–19325. (PMID: 10.3390/ijms160819308)
Iida S, Kobiyama A, Ogata T, Murakami A (2008) The D1 and D2 proteins of dinoflagellates: unusually accumulated mutations which influence on PSII photoreaction. Photosynth Res 98:415–425. (PMID: 10.1007/s11120-008-9378-y)
Ji XL, Liu F, Peng Q, Wang M (2017) Purification, structural characterization, and hypolipidemic effects of a neutral polysaccharide from Ziziphus Jujuba cv. Muzao. Food Chem 15:1124–1130.
Jiang MY, Zhang JH (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410. (PMID: 10.1093/jxb/erf090)
Kanekiyo K, Lee JB, Hayashi K, Takenaka H, Hayakawa Y, Endo S, Hayashi T (2005) Isolation of an antiviral polysaccharide, nostoflan, from a terrestrial cyanobacterium, Nostoc flagelliforme. J Nat Prod 68:1037–1041. (PMID: 10.1021/np050056c)
Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258–278. (PMID: 10.1111/j.1574-6976.2008.00134.x)
Li H, Xu J, Liu Y, Ai S, Qin F, Li Z, Zhang H, Huang Z (2011) Antioxidant and moisture-retention activities of the polysaccharide from Nostoc commune. Carbohydr Polym 83:1821–1827. (PMID: 10.1016/j.carbpol.2010.10.046)
Liang W, Zhou Y, Wang L, You X, Zhang Y, Cheng C-L, Chen W (2012) Ultrastructural, physiological and proteomic analysis of Nostoc flagelliforme in response to dehydration and rehydration. J Proteome 75:5604–5627. (PMID: 10.1016/j.jprot.2012.07.041)
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 ^-ΔΔCt method. Methods 25:402–408.
Logan B (2005) Reactive oxygen species and photosynthesis. In Antioxidants and Reactive Oxygen Species in Plants; Smrinoff, N., Ed.; Blackwell: Oxford, UK. pp 250-267.
Looijesteijn PJ, Boels IC, Kleerebezem M, Hugenholtz J (1999) Regulation of exopolysaccharide production by lactococcus lactis subsp. cremoris by the sugar source. Appl En Microbiol 65:5003–5008. (PMID: 10.1128/AEM.65.11.5003-5008.1999)
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. (PMID: 10.1016/S1360-1385(02)02312-9)
Mylona PV, Polidoros AN, Scandalios JG (2007) Antioxidant gene responses to ROS-generating xenobiotics in developing and germinated scutella of maize. J Exp Bot 58:1301–1312. (PMID: 10.1093/jxb/erl292)
Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism indrought: not so cut and dried. Plant Physiol 164:1636–1648. (PMID: 10.1104/pp.113.233478)
Otero A, Vincenzini M (2003) Extracellular polysaccharide synthesis by Nostoc strains as affected by N source and light intensity. J Biotechnol 102:143–152. (PMID: 10.1016/S0168-1656(03)00022-1)
Pavel P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. BBA-Bioenergetics 1:218–231.
Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol Rev 33:917–941. (PMID: 10.1111/j.1574-6976.2009.00183.x)
Polle A, Krings B, Rennenberg H (1989) Superoxide dismutase activityin needles of norwegian spruce trees (Picea abies L.). Plant Physiol 90:1310–1315. (PMID: 10.1104/pp.90.4.1310)
Prasanna R, Sood A, Ratha SK, Singh PK (2014) Cyanobacteria as a “green option” for sustainable agriculture. In: Sharma NK, Stal LJ, Rai AK (eds) Cyanobacteria: an economic perspective. Wiley, Chichester, pp 145–166.
Provencher C, Lapointe G, Sirois S, Van Calsteren MR, Roy D (2003) Consensusdegenerate hybrid oligonucleotide primers for amplification of priming glycosyltransferase genes of the exopolysaccharide locus in strains of the Lactobacillus casei Group. Appl Environ Microb 69:3299–3307. (PMID: 10.1128/AEM.69.6.3299-3307.2003)
Rossi F, De Philippis R (2016) Exocellular polysaccharides in microalgae and cyanobacteria: chemical features, role and enzymes and genes involved in their biosynthesis. Springer International Publishing, Switzerland, pp 565–590.
Rossi F, De Phillippis R (2015) Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats. Life 5:1218–1238. (PMID: 10.3390/life5021218)
Rossi F, Mugnai G, De Phillippis R (2018) Complex role of the polymeric matrix in biological soil crusts. Plant Soil 429:19–34. (PMID: 10.1007/s11104-017-3441-4)
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot Article ID 217037:26.
Shirkey B, Kovarcik DP, Wright DJ, Wilmoth G, Prickett TF, Helm RF (2000) Active Fe-containing superoxide dismutase and abundant sodF mRNA in Nostoc commune (Cyanobacteria) after years of desiccation. J Bacteriol 182:189–197. (PMID: 10.1128/JB.182.1.189-197.2000)
Soares C, Carvalho MEA, Azevedo RA, Fidalgo F (2018) Plants facing oxidative challenges-A little help from the antioxidant networks. Environ Exp Bot 161:4–25. (PMID: 10.1016/j.envexpbot.2018.12.009)
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66. (PMID: 10.1016/S0168-9452(99)00197-1)
Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655. (PMID: 10.1016/S0168-9452(03)00022-0)
Vijayabaskar P, Babinastarlin S, Shankar T, Sivakumar T, Anandapandian KT (2011) Quantification and characterization of exopolysaccharides from Bacillus subtilis (MTCC 121). Adv Biol Res 5:71–76.
Wang B, Yang L, Zhang YQ, Chen SL, Gao X, Wan CH (2018) Investigation of the dynamical expression of Nostoc flagelliforme proteome in response to rehydration. J Proteome 192:160–168. (PMID: 10.1016/j.jprot.2018.08.019)
Yilancioglu K, Cokol M, Pastirmaci I, Erman B, Cetiner S (2014) Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina Strain. PLoS One. 9:No. e91957.
Yu H, Jia SR, Dai YJ (2010) Accumulation of exopolysaccharides in liquid suspension culture of Nostoc flagelliforme cells. Appl Biochem Biotechnol 160:552–560. (PMID: 10.1007/s12010-008-8428-4)
Zhao RZ, Jiang S, Zhang L, Yu ZB (2019) Mitochondrial electron transport chain, ROS generation and uncoupling (Review). Int J Mol Med 44:3–15.
Zhou YW, Zhang YP, Yang J, Xu Q, Lei XT, Liang WY (2012) Effects of drought stress on ultrastructure and stress physiology of Nostoc flagelliforme. Bulletin of Botanical Research 32:171–176.

no. 31960060 Instituto Nacional de Ciência e Tecnologia Centro de Estudos das Adaptações da Biota Aquática da Amazônia (BR); no. 31660066 the National Natural Science Grant of China; no. 31660114 the National Natural Science Grant of China

Keywords: Antioxidant enzymes; Drought tolerance; Exopolysaccharides; Gene differential expression; Nostoc flagelliforme; ROS

0 (Reactive Oxygen Species)

Nostoc flagelliforme

Date Created: 20210301 Date Completed: 20210714 Latest Revision: 20210714

20231215

10.1007/s11356-021-13051-0

33646551