Novel vanadium-dependent haloperoxidases from macroalgae and their expression in response to biotic and abiotic stressors in Saccharina latissima

Timo Jensen , Mira Wilkens , Holger Rehmann , Maria Mucke , Dominik Bents , Petra Janning , Andreas Brockmeyer , Stefan Veltel , Matthias Peipp , Antje Labes , Wolfgang Bilger , Levent Piker

Marine Life Science & Technology ›› : 1 -15.

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Marine Life Science & Technology ›› :1 -15. DOI: 10.1007/s42995-026-00367-4
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Novel vanadium-dependent haloperoxidases from macroalgae and their expression in response to biotic and abiotic stressors in Saccharina latissima
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Abstract

Vanadium-dependent haloperoxidases (vHPOs) are essential enzymes in macroalgae, known for their ability to catalyze halogenation reactions using halides and hydrogen peroxide. These enzymes facilitate the biosynthesis of halogenated compounds that contribute to the defense mechanisms of algae and are considered to play a crucial role in the oxidative stress response. Using a transcriptomic approach, we discovered and analyzed about 70 novel vHPO sequences from nine different macroalgae species collected in the Baltic Sea. All sequences were carefully selected for their universal catalytic center characterized by structurally conserved residues essential for catalysis and vanadate-binding. Mass spectrometry provided evidence for eight of those proteins in extract fractions of the brown alga Saccharina latissima. Using RT-qPCR, we also investigated the role of vHPO gene expression in stress response on a subset of S. latissima vHPO transcripts by exposing it to different stressors including copper excess, oxidative stress, and biotic stress mimicked by elicitor treatment using a S. latissima tissue homogenate. The optimal quantum yield of photosystem ll served as a physiological plant stress parameter (FV/FM). Our data support the hypothesis that these enzymes are involved in mitigating oxidative stress, as suggested by up-regulation in gene expression following H2O2 and elicitor treatments, and are likely involved in environmental stress response. This work advances our understanding of vHPO function in marine algae and highlights their potential role in responding to environmental stress.

Keywords

Vanadium-dependent haloperoxidases / Algae / Stress / Saccharina latissima / Transcriptomics / Gene expression

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Timo Jensen, Mira Wilkens, Holger Rehmann, Maria Mucke, Dominik Bents, Petra Janning, Andreas Brockmeyer, Stefan Veltel, Matthias Peipp, Antje Labes, Wolfgang Bilger, Levent Piker. Novel vanadium-dependent haloperoxidases from macroalgae and their expression in response to biotic and abiotic stressors in Saccharina latissima. Marine Life Science & Technology 1-15 DOI:10.1007/s42995-026-00367-4

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References

[1]

Almagro Armenteros JJ, Sønderby CK, Sønderby SK, Nielsen H, Winther O. DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics, 2017, 33: 3387-3395

[2]

Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol, 2019, 37: 420-423

[3]

Almagro Armenteros JJ, Salvatore M, Emanuelsson O, Winther O, von Heijne G, Elofsson A, Nielsen H. Detecting sequence signals in targeting peptides using deep learning. Life Sci Alliance, 2019, 2 e201900429

[4]

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol, 1990, 215: 403-410

[5]

Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol, 2004, 55: 373-399

[6]

Ashraf M, Harris PJC. Photosynthesis under stressful environments: an overview. Photosynthetica, 2013, 51: 163-190

[7]

Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The protein data bank. Nucleic Acids Res, 2000, 28: 235-242

[8]

Bindoli A, Rigobello MPLennarz WJ, Lane MD. Peroxidase biochemistry and redox signaling. Encyclopedia of biological chemistry, 2013, 2Amsterdam. Academic Press: 407-412

[9]

Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, Frutiger S, Hochstrasser D. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis, 1993, 14: 1023-1031

[10]

Bushmanova E, Antipov D, Lapidus A, Prjibelski AD. rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data. Gigascience, 2019, 8 giz100

[11]

Bushnell B, Rood J, Singer E. BBMerge - accurate paired shotgun read merging via overlap. PLoS ONE, 2017, 12 e0185056

[12]

Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 2018, 34: i884-i890

[13]

Chen PY-T, Adak S, Chekan JR, Liscombe DK, Miyanaga A, Bernhardt P, et al. . Structural basis of stereospecific vanadium-dependent haloperoxidase family enzymes in napyradiomycin biosynthesis. Biochemistry, 2022, 61: 1844-1852

[14]

Colin C, Leblanc C, Wagner E, Delage L, Leize-Wagner E, van Dorsselaer A, Kloareg B, Potin P. The brown algal kelp Laminaria digitata features distinct bromoperoxidase and iodoperoxidase activities. J Biol Chem, 2003, 278: 23545-23552

[15]

Colin C, Leblanc C, Michel G, Wagner E, Leize-Wagner E, van Dorsselaer A, Potin P. Vanadium-dependent iodoperoxidases in Laminaria digitata, a novel biochemical function diverging from brown algal bromoperoxidases. J Biol Inorg Chem, 2005, 10: 156-166

[16]

Cosse A, Potin P, Leblanc C. Patterns of gene expression induced by oligoguluronates reveal conserved and environment-specific molecular defense responses in the brown alga Laminaria digitata. New Phytol, 2009, 182: 239-250

[17]

Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol, 2008, 26: 1367-1372

[18]

Dittami SM, Scornet D, Petit J-L, Ségurens B, Da Silva C, Corre E, Dondrup M, Glatting K-H, König R, Sterck L, Rouzé P, van de Peer Y, Cock JM, Boyen C, Tonon T. Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. Genome Biol, 2009, 10 R66

[19]

Dummermuth A, Karsten U, Fisch K, König G, Wiencke C. Responses of marine macroalgae to hydrogen-peroxide stress. J Exp Mar Biol Ecol, 2003, 289: 103-121

[20]

Fournier J-B, Rebuffet E, Delage L, Grijol R, Meslet-Cladière L, Rzonca J, Potin P, Michel G, Czjzek M, Leblanc C. The vanadium iodoperoxidase from the marine flavobacteriaceae species Zobellia galactanivorans reveals novel molecular and evolutionary features of halide specificity in the vanadium haloperoxidase enzyme family. Appl Environ Microbiol, 2014, 80: 7561-7573

[21]

Green MR (2012) Molecular Cloning: a laboratory manual, 4th edn, Woodbury.

[22]

Gschloessl B, Guermeur Y, Cock JM. Hectar: a method to predict subcellular targeting in heterokonts. BMC Bioinformatics, 2008, 9: 393

[23]

Jensen T, Saleh L, Bents D, Krohn S, Wu Y-C, Mucke M, Boje AS, Veltel S, Hennig S, Piker L, Peipp M, Labes A. Optimised protocols for RNA extraction from a broad taxonomic range of algae. J Appl Phycol, 2023, 35: 1743-1753

[24]

Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong S-Y, Lopez R, Hunter S. InterProScan 5: genome-scale protein function classification. Bioinformatics, 2014, 30: 1236-1240

[25]

Jordan P, Kloareg B, Vilter H. Detection of vanadate-dependent bromoperoxidases in protoplasts from the brown algae Laminaria digitata and L. saccharina. J Plant Physiol, 1991, 137: 520-524

[26]

Kawano T. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep, 2003, 21: 829-837

[27]

Koyro H-W, Huchzermeyer BAhmad P, Ahanger MA, Singh VP, Tripathi DK, Alam P, Alyemeni MN. Coordinated regulation of photosynthesis in plants increases yield and resistance to different types of environmental stress. Plant metabolites and regulation under environmental stress, 2018, London. Academic press: 281-309

[28]

Kozlowski LP. IPC - isoelectric point calculator. Biol Direct, 2016, 11 55

[29]

Kraulis PJ. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr, 1991, 24: 946-950

[30]

Küpper FC, Schweigert N, Ar Gall E, Legendre J-M, Vilter H, Kloareg B. Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta, 1998, 207: 163-171

[31]

Küpper FC, Kloareg B, Guern J, Potin P. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol, 2001, 125: 278-291

[32]

Küpper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Waite TJ, Boneberg E-M, Woitsch S, Weiller M, Abela R, Grolimund D, Potin P, Butler A, Luther GW, Kroneck PMH, Meyer-Klaucke W, Feiters MC. Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc Natl Acad Sci U S A, 2008, 105: 6954-6958

[33]

Leblanc C, Colin C, Cosse A, Delage L, La Barre S, Morin P, Fiévet B, Voiseux C, Ambroise Y, Verhaeghe E, Amouroux D, Donard O, Tessier E, Potin P. Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie, 2006, 88: 1773-1785

[34]

Leblanc C, Vilter H, Fournier J-B, Delage L, Potin P, Rebuffet E, Michel G, Solari PL, Feiters MC, Czjzek M. Vanadium haloperoxidases: from the discovery 30 years ago to X-ray crystallographic and V K-edge absorption spectroscopic studies. Coord Chem Rev, 2015, 301–302: 134-146

[35]

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics, 2018, 34: 3094-3100

[36]

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 −ΔΔCT method. Methods, 2001, 25: 402-408

[37]

Manley SL. Phytogenesis of halomethanes: a product of selection or a metabolic accident?. Biogeochemistry, 2002, 60: 163-180

[38]

McKinnie SMK, Miles ZD, Moore BS. Characterization and biochemical assays of Streptomyces vanadium-dependent chloroperoxidases. Methods Enzymol, 2018, 604: 405-424

[39]

Merritt EA, Murphy ME. Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr D Biol Crystallogr, 1994, 50: 869-873

[40]

Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal, 2009, 2 ra45

[41]

Mittler R, Vanderauwera S, Gollery M, van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci, 2004, 9: 490-498

[42]

Murchie EH, Lawson T. Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot, 2013, 64: 3983-3998

[43]

Pandey VP, Awasthi M, Singh S, Tiwari S, Dwivedi UN. A comprehensive review on function and application of plant peroxidases. Biochem Anal Biochem, 2017, 6 01

[44]

Passardi F, Theiler G, Zamocky M, Cosio C, Rouhier N, Teixera F, Margis-Pinheiro M, Ioannidis V, Penel C, Falquet L, Dunand C. PeroxiBase: the peroxidase database. Phytochemistry, 2007, 68: 1605-1611

[45]

Petrov VD, van Breusegem F (2012) Hydrogen peroxide - a central hub for information flow in plant cells. AoB Plants 2012:pls014.

[46]

Potin P, Bouarab K, Salaün J-P, Pohnert G, Kloareg B. Biotic interactions of marine algae. Curr Opin Plant Biol, 2002, 5: 308-317

[47]

Renirie R, Dewilde A, Pierlot C, Wever R, Hober D, Aubry J-M. Bactericidal and virucidal activity of the alkalophilic P395D/L241V/T343A mutant of vanadium chloroperoxidase. J Appl Microbiol, 2008, 105: 264-270

[48]

Ritter A, Goulitquer S, Salaün J-P, Tonon T, Correa JA, Potin P. Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol, 2008, 180: 809-821

[49]

Ritter A, Ubertini M, Romac S, Gaillard F, Delage L, Mann A, Cock JM, Tonon T, Correa JA, Potin P. Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpus siliculosus. Proteomics, 2010, 10: 2074-2088

[50]

Ritter A, Dittami SM, Goulitquer S, Correa JA, Boyen C, Potin P, Tonon T. Transcriptomic and metabolomic analysis of copper stress acclimation in Ectocarpus siliculosus highlights signaling and tolerance mechanisms in brown algae. BMC Plant Biol, 2014, 14 116

[51]

Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. Integrative genomics viewer. Nat Biotechnol, 2011, 29: 24-26

[52]

Roeder V, Collén J, Rousvoal S, Corre E, Leblanc C, Boyen C. Identification of stress gene transcripts in Laminaria digitata (Phaeophyceae) protoplast cultures by expressed sequence tag analysis. J Phycol, 2005, 41: 1227-1235

[53]

Salgado LT, Cinelli LP, Viana NB, Tomazetto de Carvalho R, Souza Mourão PA, Teixeira VL, Farina M, Filho AGMA. A vanadium bromoperoxidase catalyzes the formation of high-molecular-weight complexes between brown algal phenolic substances and alginates. J Phycol, 2009, 45: 193-202

[54]

Schiel DR, Foster MS. The population biology of large brown seaweeds: ecological consequences of multiphase life histories in dynamic coastal environments. Annu Rev Ecol Evol Syst, 2006, 37: 343-372

[55]

Schiener P, Black KD, Stanley MS, Green DH. The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol, 2015, 27: 363-373

[56]

Schomburg D, Reichelt J. Bragi: a comprehensive protein modeling program system. J Mol Graph, 1988, 6: 161-165

[57]

Schreiber U. Chlorophyll fluorescence yield changes as a tool in plant physiology I. The measuring system. Photosynth Res, 1983, 4: 361-373

[58]

Sewelam N, Kazan K, Schenk PM. Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci, 2016, 7 187

[59]

Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc, 2006, 1: 2856-2860

[60]

Sies H. Oxidative stress: from basic research to clinical application. Am J Med, 1991, 91: 31S-38S

[61]

Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol, 2011, 7 539

[62]

Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition?. Trends Plant Sci, 2008, 13: 178-182

[63]

Verhaeghe E, Buisson D, Zekri E, Leblanc C, Potin P, Ambroise Y. A colorimetric assay for steady-state analyses of iodo- and bromoperoxidase activities. Anal Biochem, 2008, 379: 60-65

[64]

Verhaeghe EF, Fraysse A, Guerquin-Kern J-L, Wu T-D, Devès G, Mioskowski C, Leblanc C, Ortega R, Ambroise Y, Potin P. Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. J Biol Inorg Chem, 2008, 13: 257-269

[65]

Verma S, Nizam S, Verma PKSarwat M, Ahmad A, Abdin MZ. Biotic and abiotic stress signaling in plants. Stress signaling in plants: genomics and proteomics perspective, 2013, New York. Springer: 25-49 1

[66]

Wever R, Krenn BE, Renirie R. Marine vanadium-dependent haloperoxidases, their isolation, characterization, and application. Methods Enzymol, 2018, 605: 141-201

[67]

Wojtaszek P. Oxidative burst: an early plant response to pathogen infection. Biochem J, 1997, 322: 681-692

[68]

Xing Q, Rousvoal S, Leblanc C. Transcriptome-wide identification and evaluation of optimal reference genes for RT-qPCR expression analysis of Saccharina latissima responses to biotic and abiotic stress. J Appl Phycol, 2021, 33: 617-627

[69]

Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform, 2012, 13 134

[70]

Zhang Y, Wang X, Shan T, Pang S, Xu N. Transcriptome profiling of the meristem tissue of Saccharina japonica (Phaeophyceae, Laminariales) under severe stress of copper. Mar Genomics, 2019, 47 100671

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Hochschule Flensburg University of Applied Sciences (3320)

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