Skip to main content
Log in

Signaling molecules hydrogen sulfide (H2S) and nitric oxide (NO): role in microalgae under adverse environmental conditions

  • Review
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

In the present time, reactive oxygen species (ROS) hydrogen peroxide (H2O2), and gases hydrogen sulfide (H2S), nitric oxide (NO) and carbon monoxide (CO) have been acknowledged as foremost signaling molecules in plants. Adverse environmental conditions are key hazard, which pointedly disturb growth and developmental processes of photoautotroph (algae) associated with decrease in the endogenous level of important gas transmitters such as NO and H2S. To oppose stress factors, NO and H2S directly involved in the modulation of physio-biochemical phenomenon correlated with minimizing the oxidative stress under stressful condition. These signaling molecules have diverse functions inside the cell, i.e., act as a plant growth regulator; therefore, it is significant to study their numerous attributes together with their biosynthetic pathways followed by biochemical (enzymatic and non-enzymatic proteins) and molecular regulations (post-translational modifications, PTMs) via stress responsive proteins by the key process of nitrosylation and persulfidation that involve in minimizing the stress. The versatile roles of NO and H2S under environmental stress have also been discussed briefly. Thus, the details given here will be helpful to better understand the diverse functions of NO and H2S in microalgae and cyanobacteria under adverse conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

References

  • Álvarez C, García I, Moreno I, Pérez-Pérez ME, Crespo JL, Romero LC, Gotor C (2012) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aroca A, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine post-translational modification in plant systems. Plant Physiol 168:334–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aroca A, Benito JM, Gotor C, Romero LC (2017) Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis. J Exp Bot 68:4915–4927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astier J, Lindermayr C (2012) Nitric oxide-dependent post translational modification in plants: an update. Int J Mol Sci 13:15193–15208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533

    Article  CAS  PubMed  Google Scholar 

  • Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411

    Article  CAS  PubMed  Google Scholar 

  • Bañares-España E, López-Rodas V, Salgado C, Costas E, Flores-Moya A (2006) Inter -strain variability in the photosynthetic use of inorganic carbon, exemplified by the pH compensation point, in the cyanobacterium Microcystis aeruginosa. Aquat Bot 85:159–162

    Article  CAS  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538

    Article  CAS  PubMed  Google Scholar 

  • Beinert H (2000) A tribute to sulfur. Eur J Biochem 267:5657–5664

    Article  CAS  PubMed  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    Article  CAS  PubMed  Google Scholar 

  • Bidyarani N, Prasanna R, Chawla G, Babu S, Singh R (2015) Deciphering the factors associated with the colonization of rice plants by cyanobacteria. J Basic Microbiol 55:407–419

    Article  CAS  PubMed  Google Scholar 

  • Bouchard JN, Yamasaki H (2008) Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: A possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol 49:641–652

    Article  CAS  PubMed  Google Scholar 

  • Burda K, Kruk J, Schmid GH, Strzalka K (2003) Inhibition of oxygen evolution in photosystem II by Cu (II) ions is associated with oxidation of cytochrome b559. Biochem J 371:597–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camejo D, Ortiz-Espín A, Lázaro JJ, Romero-Puertas MC, Lázaro- Payo A, Sevilla F (2015) Functional and structural changes in plant mitochondrial PrxIIF caused by NO. J Proteomics 119:112–125

    Article  CAS  PubMed  Google Scholar 

  • Chaki M, Shekariesfahlan A, Ageeva A, Mengel A, Von-Toerne C, Durner J, Lindermayr C (2015) Identification of nuclear target proteins for S-nitrosylation in pathogen- treated Arabidopsis thaliana cell cultures. Plant Sci 238:115–126

    Article  CAS  PubMed  Google Scholar 

  • Chaux F, Burlacot A, Mekhalfi M, Auroy P, Blangy S, Richaud P, Peltier G (2017) Flavodiiron proteins promote fast and transient O2 photoreduction in Chlamydomonas. Plant Physiol 174:1825–1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen JA, Xiao QA, Wu FH, Dong XJ, He JX, Pei ZM, Zheng HL (2010) Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol 30:1570–1585

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2012) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318

    Article  CAS  Google Scholar 

  • Chen J, Xiong DY, Wang WH, Hu WJ, Simon M, Xiao Q, Liu TW, Liu X, Zheng HL (2013) Nitric Oxide mediates root K+/Na+ balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-Type K+ channel and Na+/H+antiporter under high salinity. PLoS One 8:71543

    Article  CAS  Google Scholar 

  • Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:12516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng J, Wang Z, Lu H, Xu J, He Y, Cen K (2019) Hydrogen sulfide promotes cell division and photosynthesis of Nannochloropsis oceanica with 15% Carbon Dioxide. ACS Sustain Chem Eng 7:16344–16354

    Article  CAS  Google Scholar 

  • Cheng J, Wang Z, Lu H, Yang W, Fan Z (2020) Hydrogen sulfide improves lipid accumulation in Nannochloropsis oceanica through metabolic regulation of carbon allocation and energy supply. J Sustain Energy Eng 8:2481–2489

    CAS  Google Scholar 

  • Chittora D, Meena M, Barupal T, Swapnil P (2020) Cyanobacteria as a source of biofertilizers for sustainable agriculture. Biochem Biophys 22:100737

    Google Scholar 

  • Choi CS, Savage DB, Abu-Elheiga L, Liu Z, Kim S, Kulkarni A, Distefano A, Hwang Y, Reznick RM, Codella R, Zhang D, Cline GW, Wakil SJ, Shulman GI (2007) Continuous fat oxidation in acetyl-CoA carboxylase 2 knockout mice increases total energy expenditure, reduces fat mass, and improves insulin sensitivity. Proc Natl Acad Sci USA 104:16480–16485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow F, Pedersén M, Oliveira MC (2013) Modulation of nitrate reductase activity by photosynthetic electron transport chain and nitric oxide balance in the red macroalga Gracilaria chilensis (gracilariales, rhodophyta). J Appl Phycol 25:1847–1853

    Article  CAS  Google Scholar 

  • Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defense pathways. J Exp Bot 64:1953–1966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung CC, Hwang SPL, Chang J (2008) Nitric oxide as a signaling factor to upregulate the death specific protein in a marine diatom, Skeletonema costatum, during blockage of electron flow in photosynthesis. Appl Environ Microbiol 74:6521–6527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clausen T, Kaiser JT, Steegborn C, Huber R, Kessler D (2000) Crystal structure of the cysteine C-S lyase from Synechocystis: stabilization of cysteine persulfide for FeS clusture biosynthesis. Proc Natl Acad Sci USA 97:3856–3861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Kok LJ, Stahl K, Rennenberg H (1989) Fluxes of atmospheric hydrogen sulphide to plant shoots. New Phytol 112:533–542

    Article  Google Scholar 

  • Deng X, Cai J, Fei X (2013) Effect of the expression and knockdown of citrate synthase gene on carbon flux during triacylglycerol biosynthesis by green algae Chlamydomonas reinhardtii. BMC Biochem 14:1–11

    Article  CAS  Google Scholar 

  • Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8:62048

    Article  CAS  Google Scholar 

  • Dorman DC, Moulin FJ, McManus BE, Mahle KC, James RA, Struve MF (2002) Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the Rat Brain, Liver, Lung, and Nasal Epithelium. Toxicol Sci 65:18–25

    Article  CAS  PubMed  Google Scholar 

  • Filipovic MR (2015) Persulfidation (S-sulfhydration) and H2S. Handb Exp Pharmacol 230:29–59

    Article  CAS  PubMed  Google Scholar 

  • Filipovic MR, Jovanovic VM (2017) More than just an intermediate: hydrogen sulfide signalling in plants. J Exp Bot 68:4733–4736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fotopoulos V, Christou A, Antoniou C, Manganaris GA (2015) Hydrogen sulphide: a versatile tool for the regulation of growth and defense responses in horticultural crops. J Hortic Sci Biotech 90:227–234

    Article  CAS  Google Scholar 

  • Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallina A, Brunet C, Palumbo A, Casotti R (2014) The effect of polyunsaturated aldehydes on Skeletonema marinoi (Bacillariophyceae): the involvement of reactive oxygen species and nitric oxide. Mar Drugs 12:4165–4187

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • García-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 202:66–73

    Article  CAS  Google Scholar 

  • Ge Y, Hu KD, Wang SS, Hu LY, Chen XY, Li YH (2017) Hydrogen sulfide alleviates postharvest ripening and senescence of banana by antagonizing the effect of ethylene. PLoS One 12:0180113

    Article  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol 48:909–930

    CAS  Google Scholar 

  • Gonzalez A, Cabrera MDEL, Henriquez MJ, Contreras RA, Morales B, Moenne A (2012) Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiol 158:1451–1462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22:2058–2084

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defense responses. Front Plant Sci 4:419

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17:3436–3450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Xiao T, Zhou H, Xie Y, Sn W (2016) Hydrogen sulfide: a versatile regulator of environmental stress in plants. Acta Physiol Plant 38:16

    Article  CAS  Google Scholar 

  • Hamilton TL, Klatt JM, de Beer D, Macalady JL (2018) Cyanobacterial photosynthesis under sulfidic conditions: insights from the isolate Leptolyngbya sp. strain hensonii. ISME J 12:568–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hancock JT (2019) Hydrogen sulfide and environmental stresses. Environ Exp Bot 161:50–56

    Article  CAS  Google Scholar 

  • Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol 78:37–42

    CAS  Google Scholar 

  • Hancock JT, Whiteman M (2016) Hydrogen sulfide signaling: interactions with nitric oxide and reactive oxygen species. Ann Acad Sci 1365:5–14

    Article  CAS  Google Scholar 

  • Hancock JT, Whiteman M (2018) Reactive oxygen species, nitric oxide and hydrogen sulfide in plant cell regulation. Free Radical Bio Med 120:6–23

    Article  Google Scholar 

  • Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000) b-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123:1163–1172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkins D, Davy SK (2013) Nitric oxide and coral bleaching: is peroxynitrite generation required for symbiosis collapse? J Exp Biol 216:3185–3188

    CAS  PubMed  Google Scholar 

  • He H, Li Y, He LF (2019) Role of nitric oxide and hydrogen sulfide in plant aluminum tolerance. Biometals 32:1–9

    Article  CAS  PubMed  Google Scholar 

  • Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66:989–999

    Article  CAS  PubMed  Google Scholar 

  • Hsu YT, Lee TM (2011) Nitric oxide up-regulates the expression of methionine sulfoxide reductase genes in the intertidal macroalga Ulva fasciata for high light acclimation. Plant Cell Physiol 53:445–456

    Article  PubMed  CAS  Google Scholar 

  • Ida T, Sawa T, Ihara H, Tsuchiya Y, Watanabe Y, Kumagai Y (2014) Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. PNAS USA 111:7606–7611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeandroz S, Lamotte O, Astier J, Rasul S, Trapet P, Besson-Bard A, Bourque S, Nicolas-Francès V, Ma W, Berkowitz GA, Wendehenne D (2013) There’s more to the picture than meets the eye: Nitric oxide cross talk with Ca2+signalling. Plant Physiol 163:459–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol 62:41–46

    CAS  Google Scholar 

  • Joshi MM, Ibrahium IKA, Hollis JP (1975) Hydrogen sulphide: effects on the physiology of rice plants and relation to straight head disease. Phytopathol 65:1170–1175

    Article  Google Scholar 

  • Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant 148:371–386

    Article  CAS  PubMed  Google Scholar 

  • Kaushik MS, Srivastava M, Srivastava A, Singh A, Mishra AK (2016) Nitric oxide ameliorates the damaging oxidative stress induced by iron deficiency in cyanobacterium Anabaena 7120. Environ Sci Pollut Res 23:21805–21821

    Article  CAS  Google Scholar 

  • Kaya C, Higgs D, Ashraf M, Alyemeni MN, Ahmad P (2019) Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol Plant 168:256–277

    PubMed  Google Scholar 

  • Kim D, Yamaguchi K, Oda T (2006) Nitric oxide synthase-like enzyme mediated nitric oxide generation by harmful red tide phytoplankton, Chattonella marina. J Plankton Res 28:613–620

    Article  CAS  Google Scholar 

  • Kim D, Kang YS, Lee Y, Yamaguchi K, Matsuoka K, Lee KW, Choi KS, Oda T (2008) Detection of nitric oxide (NO) in marine phytoplankters. J Biosci Bioeng 105:414–417

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Koike S, Shibuya N, Lefer D, Ogasawara Y, Kia H (2017) 3-Mercaptopyruvate sulfurtransferase produces potential redox regulators cysteine- and glutathione-persulfide (Cys-SSH and GSSH) together with signaling molecules H2S2, H2S3 and H2S. Sci Rep 7:10459

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kitajima S, Kurioka M, Yoshimoto T, Shindo M, Kanaori K, Tajima K (2008) A cysteine residue near the propionate side chain of heme is the radical site in ascorbate peroxidase. FEBS J 275:470–480

    Article  CAS  PubMed  Google Scholar 

  • Klatt JM, Haas S, Yilmaz P, de Beer D, Polerecky L (2015) Hydrogen sulfide can inhibit and enhance oxygenic photosynthesis in a cyanobacterium from sulfidic springs. Environ Microbiol 17:3301–3313

    Article  CAS  PubMed  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolluru GK, Shen X, Bir SC, Kevil CG (2013) Hydrogen sulfide chemical biology: pathophysiological roles. Nitric Oxide 35:5–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon E, Feechan A, Yun BW, Hwang BH, Pallas JA, Kang JG, Loake GJ (2012) AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236:887–900

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Lancaster JR (2013) Chemical foundations of hydrogen sulfide biology. Nitric Oxide 35:21–34

    Article  PubMed  CAS  Google Scholar 

  • Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Bio Met 25:617–631

    CAS  Google Scholar 

  • Li ZG, Yi XY, Li YT (2014) Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia 69:1001–1009

    Article  CAS  Google Scholar 

  • Lin YT, Li MY, Cui WT, Lu W, Shen WB (2012) Haem oxygenase-1 in involved in hydrogen sulfide induced cucumber adventitious root formation. J Plant Growth Regul 31:519–528

    Article  CAS  Google Scholar 

  • Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol 48:931–935

    CAS  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signaling molecule? Plant Cell Environ 36:1607–1616

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Zhang J, Lü C, Xia Y, Liu H, Jiao N, Xun L, Liu J (2020) Synechococcus sp. strain PCC 7002 uses sulfide: quinone oxidoreductase to detoxify exogenous sulfide and to convert endogenous sulfide to cellular sulfane sulfur. JAEBS 11:3419–3420

    Google Scholar 

  • Mallick N, Mohn FH, Soeder CJ, Grobbelaar JU (2002) Ameliorative role of nitric oxide on H2O2 toxicity to a chlorophycean alga Scenedesmus obliquus. J Gen Appl Microbiol 48:1–7

    Article  CAS  PubMed  Google Scholar 

  • Manjunatha M, Prasannaa R, Sharma P, Nain L, Singh R (2011) Developing PGPR consortia using novel genera Providencia and Alcaligenes along with cyanobacteria for wheat. Arch Agron Soil Sci 57:873–887

    Article  CAS  Google Scholar 

  • Martín-Clemente E, Melero-Jiménez IJ, Bañares-España E, Flores-Moya A, García-Sánchez MJ (2019) Adaptation dynamics and evolutionary rescue under sulfide selection in cyanobacteria: a comparative study between Microcystis aeruginosa and Oscillatoria sp. (cyanobacteria). J Phycol. https://doi.org/10.1111/jpy.12911

    Article  PubMed  Google Scholar 

  • Mia MD, Lemaire SD, Choquet Y, Wollman FA (2019) Nitric oxide remodels the photosynthetic apparatus upon S- starvation in Chlamydomonas reinhardtii. Plant Physiol 179:718–731

    Article  PubMed  CAS  Google Scholar 

  • Mostofa MG, Rahman A, Ansary MU, Watanabe A, Fujita M (2015) Tran L-SP: hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078

    Article  PubMed  PubMed Central  Google Scholar 

  • Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagy V, Vidal-Meireles A, Podmaniczki A, Szentmihályi K, Rákhely G, Zsigmond L, Kovács L, Tóth SZ (2018) The mechanism of photosystem-II inactivation during sulphur deprivation-induced H2 production in Chlamydomonas reinhardtii. Plant J 94:548–561

    Article  CAS  PubMed  Google Scholar 

  • Oren A, Shilo M (1979) Anaerobic heterotrophic dark metabolism in the cyanobacterium Oscillatoria limnetica: sulfur respiration and lactate fermentation. Arch Microbiol 122:77–84

    Article  CAS  Google Scholar 

  • Ozfidan-Konakci C, Elbasan F, Kucukoduk M, Turkan I (2020) Hydrogen sulfide (H2S) and nitric oxide (NO) alleviate cobalt toxicity in wheat (Triticum aestivum L.) by modulating photosynthesis, chloroplastic redox and antioxidant capacity. J Hazard Mater 388:122061

    Article  CAS  PubMed  Google Scholar 

  • Pandey A, Pathak J, Singh DK, Ahmed H, Singh V, Kumar D, Sinha RP (2020) Photoprotective role of UV-screening pigment scytonemin against UV-B-induced damages in the heterocyst-forming cyanobacterium Nostoc sp. strain HKAR-2. Rev Bras Bot. https://doi.org/10.1007/s40415-020-00589-5

    Article  Google Scholar 

  • Patel A, Tiwari S, Prasad SM (2018) Toxicity assessment of arsenate and arsenite on growth, chlorophyll a fluorescence and antioxidant machinery in Nostoc muscorum. Ecotoxicol Environ Saf 157:369–379

    Article  CAS  PubMed  Google Scholar 

  • Patel A, Tiwari S, Prasad SM (2020) Effect of time interval on arsenic toxicity to paddy field cyanobacteria as evident by nitrogen metabolism, biochemical constituent, and exopolysaccharide content. Biol Trace Elem Res 199:2031–2046

    Article  PubMed  CAS  Google Scholar 

  • Paul BD, Snyder SH (2012) H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13:499–507

    Article  CAS  PubMed  Google Scholar 

  • Pedrajas JR, Carreras A, Valderrama R, Barroso JB (2010) Mitochondrial 1-Cys-peroxiredoxin/thioredoxin system protects manganese- containing super oxide dismutase (Mn-SOD) against inactivation by peroxynitrite in Saccharomyces cerevisiae. Nitric Oxide 23:206–213

    Article  CAS  PubMed  Google Scholar 

  • Perez S (2006) Nitric oxide and cnidarian bleaching: An eviction notice mediates breakdown of a symbiosis. J Exp Biol 209:2804–2810

    Article  CAS  PubMed  Google Scholar 

  • Pohnert G, Boland W (2002) The oxylipin chemistry of attraction and defense in brown algae and diatoms. Nat Prod Rep 19:108–122

    Article  CAS  PubMed  Google Scholar 

  • Radi R (2013) Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc Chem 46:550–559

    Article  CAS  Google Scholar 

  • Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AME (2007) S-nitrosylation of peroxiredoxin IIE promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakihama Y, Nakamura S, Yamasaki H (2002) Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: An alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol 43:290–297

    Article  CAS  PubMed  Google Scholar 

  • Santana MM, Gonzalez JM, Cruz C (2017) Nitric oxide accumulation: the evolutionary trigger for phytopathogenesis. Front Microbiol 8:01947

    Article  Google Scholar 

  • Shan CJ, Zhang SL, Li DF, Zhao YZ, Tian XL, Zhao XL, Wu YX, Wei XY, Liu RQ (2011) Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. Acta Physiol Plant 33:2533–2540

    Article  CAS  Google Scholar 

  • Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodondactylon (L). Pers.). Plant Physiol 74:99–107

    CAS  Google Scholar 

  • Shoman ME, Aly OM (2016) Nitroxyl (HNO): a reduced form of nitric oxide with distinct chemical, pharmacological, and therapeutic properties. Oxid Med Cell Longev. https://doi.org/10.1155/2016/4867124

    Article  PubMed  Google Scholar 

  • Singh VP, Srivastava PK, Prasad SM (2012) UV-B induced differential effect on growth and nitrogen metabolism in two cyanobacteria under copper toxicity. Cell Mol Biol 58:85–95

    CAS  PubMed  Google Scholar 

  • Singh R, Parihar P, Singh M, Bajguz A, Kumar J, Singh S, Singh VP, Prasad SM (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front Microbiol 8:515

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh S, Prasad SM, Sharma S, Ramawat N, Prasad R, Singh VP, Tripathi DK, Chauhan DK (2020) Silicon and nitric oxide mediated mechanisms of cadmium toxicity alleviation in wheat seedlings. Physiol Plant. https://doi.org/10.1111/ppl.13065

    Article  PubMed  Google Scholar 

  • Singh VP, Tripathi DK, Fotopoulos V (2020b) Hydrogen sulfide and nitric oxide signal integration and plant development under stressed/ non-stressed conditions. Physiol Plant 168:239–240

    Article  CAS  PubMed  Google Scholar 

  • Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V (2012) Oxidative and nitrosative-based signalling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599

    Article  CAS  PubMed  Google Scholar 

  • Tejada-Jimenez M, Llamas A, Galván A, Fernández E (2019) Role of nitrate reductase in NO production in photosynthetic eukaryotes. Plants 8:56

    Article  CAS  PubMed Central  Google Scholar 

  • Tiwari S, Verma N, Singh VP, Prasad SM (2019) Nitric oxide ameliorates aluminium toxicity in Anabaena PCC 7120: Regulation of aluminium accumulation, exopolysaccharides secretion, photosynthesis and oxidative stress markers. Environ Exp Bot 161:218–227

    Article  CAS  Google Scholar 

  • Tiwari S, Verma N, Prasad SM, Singh VP (2021) Cytokinin alleviates cypermethrin toxiciry in Nostoc muscorum by involving nitric oxide: Regulation of exopolysaccharides secretion, PS II photochemistry and reactive oxygen species homeostasis. Chemosphere 259:127356

    Article  CAS  Google Scholar 

  • Trapido-Rosenthal H, Zielke S, Owen R, Buxton L, Boeing B, Bhagooli R, Archer J (2005) Increased zooxanthellae nitric oxide synthase activity is associated with coral bleaching. Biol Bull 208:3–6

    Article  CAS  PubMed  Google Scholar 

  • Vardi A, Formiggini F, Casotti R, Martino AD, Ribalet F, Miralto A, Bowler C (2006) A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biol 4:e60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vardi A, Bidle D, Kwityn C, Hirsh DJ, Thompson SM, Callow JA, Falkowski P, Bowler C (2008) A diatom gene regulating nitric-oxide signaling and susceptibility to diatom-derived aldehydes. Curr Biol 18:895–899

    Article  CAS  PubMed  Google Scholar 

  • Verma N, Prasad SM (2021) Regulation of redox homeostasis in cadmium stressed rice field cyanobacteria by exogenous hydrogen peroxide and nitric oxide. Sci Rep 11:1–15

    Article  CAS  Google Scholar 

  • Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798

    Article  CAS  PubMed  Google Scholar 

  • Wang R (2003) The gasotransmitter role of hydrogen sulfide. Antioxid Redox Sign 5:493–501

    Article  CAS  Google Scholar 

  • Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119

    Article  CAS  Google Scholar 

  • Wang Y, Loake GJ, Chu C (2013a) Cross-talk of nitric oxide and reactive oxygen species in plant programmed cell death. Front Plant Sci 4:314

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang YXX, Zhong Y, Jing B (2013b) Effects of nitric oxide on photosynthesis rate of Phaeodactylum tricornutum. Nitric Oxide 31:25–26

    Article  Google Scholar 

  • Wang H, Ji F, Zhang Y, Hou J, Liu W, Huang J, Liang W (2019) Interactions between hydrogen sulfide and nitric oxide regulate two soybean citrate transporters during the alleviation of aluminum toxicity. Plant Cell Environ 42:2340–2356

    Article  CAS  PubMed  Google Scholar 

  • Wedmann R, Onderka C, Wei S (2016) Improved tag-switch method reveals that thioredoxin acts as depersulfidase and controls the intracellular levels of protein persulfidation. Chem Sci 7:3414–3426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whiteman M, Li L, Kostetski I, Chu SH, Siau JL, Bhatia M, Moore PK (2006) Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochem Bioph Res Commun 343:303–310

    Article  CAS  Google Scholar 

  • Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622–631

    Article  CAS  PubMed  Google Scholar 

  • Wodala B, Deak Z, Vass I, Erdei L, Altorjay I, Horvath F (2008) In vivo target sites of nitric oxide in photosynthetic electron transport as studied by chlorophyll fluorescence in pea leaves. ASPB 146:1920–1927

    CAS  Google Scholar 

  • Xue L, Li S, Sheng H, Feng H, Xu S, An L (2007) Nitric oxide alleviates oxidative damage induced by enhanced ultraviolet-b radiation in cyanobacterium. Curr Microbiol 55:294–301

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H (2000) Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos T R Soc A 355:1477–1488

    Article  CAS  Google Scholar 

  • Zaffagnini M, Morisse S, Bedhomme M, Marchand CH, Festa M, Rouhier N, Lemaire SD, Trost P (2013) Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J Biol Chem 288:22777–22789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaffagnini M, De-Mia M, Morisse S, Di-Giacinto N, Marchand CH, Maes A, Lemaire SD, Trost P (2016) Protein S-nitrosylation in photosynthetic organisms: a comprehensive overview with future perspectives. BBA Mol Cell Res 1864:952–966

    CAS  Google Scholar 

  • Zahra Z, Hyun Choo D, Lee H, Parveen A (2020) Cyanobacteria: review of current potentials and applications. Environments 7:2076–3298

    Article  Google Scholar 

  • Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173

    Article  CAS  PubMed  Google Scholar 

  • Zhan N, Wang C, Chen L, Yang H, Feng J, Gong X, Ren B, Wu R, Mu J, Li Y (2018) S-nitrosylation targets GSNO reductase for selective autophagy during hypoxia responses in plants. Mol Cell 71:142–154

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Lin C, Liu C, Sun M, Ding H (2003) The effect of nitric oxide on the growth of marine phytoplankton. J Ocean Univ China 2:185–188

    Article  CAS  Google Scholar 

  • Zhang ZB, Liu CY, Wu ZZ, Xing L, Li PF (2006) Detection of nitric oxide in culture media and studies on nitric oxide formation by marine microalgae. Med Sci Monit 12:75–85

    Google Scholar 

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide treatment promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. J Plant Growth Regul 58:243–250

    Article  CAS  Google Scholar 

  • Zou H, Zhang NN, Pan Q, Zhang JH, Chen J, Wei GH (2019) Hydrogen sulfide promotes nodulation and nitrogen fixation in soybean-rhizobia symbiotic system. Mol Plant Microbe Interact 32:972–985

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

For all the necessary laboratory facilities, the authors are thankful to the Head, Department of Botany, University of Allahabad. Garima Singh and Divya Gupta are thankful to UGC, Sanjesh Tiwari to (CSIR-UGC) New Delhi as ‘SRF (letter number 2121430412, EU-V)’ and Anuradha Patel to NFO as ‘SRF (NFO-2015-17-OBC-UTT-41056).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sheo Mohan Prasad.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

In the present study, no human, animals or human tissues are used and not applicable.

Consent for publication

Not applicable and the manuscript do not contain individual’s person data.

Additional information

Communicated by P. Wojtaszek.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, G., Patel, A., Tiwari, S. et al. Signaling molecules hydrogen sulfide (H2S) and nitric oxide (NO): role in microalgae under adverse environmental conditions. Acta Physiol Plant 44, 68 (2022). https://doi.org/10.1007/s11738-022-03404-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-022-03404-8

Keywords

Navigation