Marine phytoplankton produce and scavenge Reactive Oxygen Species, to support cellular processes, while limiting damaging reactions. Some prokaryotic picophytoplankton have, however, lost all genes encoding scavenging of hydrogen peroxide. Such losses of metabolic function can only apply to Reactive Oxygen Species which potentially traverse the cell membrane outwards, before provoking damaging intracellular reactions. We hypothesized that cell radius influences which elements of Reactive Oxygen Species metabolism are partially or fully dispensable from a cell. We therefore investigated genomes and transcriptomes from diverse marine eukaryotic phytoplankton, ranging from 0.4 to 44 μm radius, to analyze the genomic allocations encoding enzymes metabolizing Reactive Oxygen Species. Superoxide has high reactivity, short lifetimes and limited membrane permeability. Genes encoding superoxide scavenging are ubiquitous across phytoplankton, but the fractional gene allocation decreased with increasing cell radius, consistent with a nearly fixed set of core genes for scavenging superoxide pools. Hydrogen peroxide has lower reactivity, longer intracellular and extracellular lifetimes and readily crosses cell membranes. Genomic allocations to both hydrogen peroxide production and scavenging decrease with increasing cell radius. Nitric Oxide has low reactivity, long intracellular and extracellular lifetimes and readily crosses cell membranes. Neither Nitric Oxide production nor scavenging genomic allocations changed with increasing cell radius. Many taxa, however, lack the genomic capacity for nitric oxide production or scavenging. The probability of presence of capacity to produce nitric oxide decreases with increasing cell size, and is influenced by flagella and colony formation. In contrast, the probability of presence of capacity to scavenge nitric oxide increases with increasing cell size, and is again influenced by flagella and colony formation.

Department of Biology Mount Allison University Sackville NB Canada

Faculty of Computer Science Dalhousie University Halifax NS Canada

Faculty of Veterinary Medicine University of Calgary Calgary AB Canada

Institute of Microbiology Center Algatech Laboratory of Photosynthesis Trebon CZ Czech Republic

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Finkel ZV, Beardall J, Flynn KJ, Quigg A, Rees TAV, Raven JA. Phytoplankton in a changing world: Cell size and elemental stoichiometry. J Plankton Res. 2010;32: 119–137. doi: 10.1093/plankt/fbp098 DOI

Andersen KH, Aksnes DL, Berge T, Fiksen Ø, Visser A. Modelling emergent trophic strategies in plankton. J Plankton Res. 2015;37: 862–868. doi: 10.1093/plankt/fbv054 DOI

Finkel ZV. Light absorption and size scaling of light-limited metabolism in marine diatoms. Limnol Oceanogr. 2001;46: 86–94. doi: 10.4319/lo.2001.46.1.0086 DOI

Geider R, Piatt T, Raven J. Size dependence of growth and photosynthesis in diatoms: A synthesis. Mar Ecol Prog Ser. 1986;30: 93–104. doi: 10.3354/meps030093 DOI

Strom SL, Macri EL, Olson MB. Microzooplankton grazing in the coastal Gulf of Alaska: Variations in top-down control of phytoplankton. Limnol Oceanogr. 2007;52: 1480–1494. doi: 10.4319/lo.2007.52.4.1480 DOI

Litchman E, de Tezanos Pinto P, Klausmeier CA, Thomas MK, Yoshiyama K. Linking traits to species diversity and community structure in phytoplankton. In: Naselli-Flores L, Rossetti G, editors. Fifty years after the “Homage to Santa Rosalia”: Old and new paradigms on biodiversity in aquatic ecosystems. Dordrecht: Springer Netherlands; 2010. pp. 15–28. doi: 10.1007/978-90-481-9908-2_3 DOI

Diaz JM, Plummer S. Production of extracellular reactive oxygen species by phytoplankton: Past and future directions. J Plankton Res. 2018;40: 655–666. doi: 10.1093/plankt/fby039 PubMed DOI PMC

Schneider R. Kinetics of Biological Hydrogen Peroxide Production. Doctor of {{Philosophy}} ({{Geochemistry}}), Colorado School of Mines. 2015.

Lesser MP. Oxidative Stress in Marine Environments: Biochemistry and Physiological Ecology. Annu Rev Physiol. 2006;68: 253–278. doi: 10.1146/annurev.physiol.68.040104.110001 PubMed DOI

Bienert GP, Chaumont F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta. 2014;1840: 1596–1604. doi: 10.1016/j.bbagen.2013.09.017 PubMed DOI

Almasalmeh A, Krenc D, Wu B, Beitz E. Structural determinants of the hydrogen peroxide permeability of aquaporins. FEBS J. 2014;281: 647–656. doi: 10.1111/febs.12653 PubMed DOI

Wang H, Schoebel S, Schmitz F, Dong H, Hedfalk K. Characterization of aquaporin-driven hydrogen peroxide transport. Biochim Biophys Acta Biomembr BBA-BIOMEMBRANES. 2020;1862: 183065. doi: 10.1016/j.bbamem.2019.183065 PubMed DOI

Miller EW, Dickinson BC, Chang CJ. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. PNAS. 2010;107: 15681–15686. doi: 10.1073/pnas.1005776107 PubMed DOI PMC

Zinser ER. The microbial contribution to reactive oxygen species dynamics in marine ecosystems. Environ Microbiol Rep. 2018;10: 412–427. doi: 10.1111/1758-2229.12626 PubMed DOI

Tjell AØ, Almdal K. Diffusion rate of hydrogen peroxide through water-swelled polyurethane membranes. Sensing and Bio-Sensing Research. 2018;21: 35–39. doi: 10.1016/j.sbsr.2018.10.001 DOI

Adesina AO, Sakugawa H. Photochemically generated nitric oxide in seawater: The peroxynitrite sink and its implications for daytime air quality. Sci Total Environ. 2021;781: 146683. doi: 10.1016/j.scitotenv.2021.146683 PubMed DOI

Korshunov SS, Imlay JA. A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram-negative bacteria. Mol Microbiol. 2002;43: 95–106. doi: 10.1046/j.1365-2958.2002.02719.x PubMed DOI

Reinsberg PH, Koellisch A, Bawol PP, Baltruschat H. K 2 electrochemistry: Achieving highly reversible peroxide formation. Phys Chem Chem Phys. 2019;21: 4286–4294. doi: 10.1039/C8CP06362A PubMed DOI

Tian Y, Yang G-P, Liu C-Y, Li P-F, Chen H-T, Bange HW. Photoproduction of nitric oxide in seawater. Ocean Sci. 2020;16: 135–148. doi: 10.5194/os-16-135-2020 DOI

Olasehinde EF, Takeda K, Sakugawa H. Photochemical Production and Consumption Mechanisms of Nitric Oxide in Seawater. Environ Sci Technol. 2010;44: 8403–8408. doi: 10.1021/es101426x PubMed DOI

del Río LA, Puppo A, editors. Reactive oxygen species in plant signaling. Dordrecht; New York: Springer Verlag; 2009.

Zacharia IG, Deen WM. Diffusivity and Solubility of Nitric Oxide in Water and Saline. Ann Biomed Eng. 2005;33: 214–222. doi: 10.1007/s10439-005-8980-9 PubMed DOI

Möller MN, Cuevasanta E, Orrico F, Lopez AC, Thomson L, Denicola A. Diffusion and Transport of Reactive Species Across Cell Membranes. In: Trostchansky A, Rubbo H, editors. Bioactive Lipids in Health and Disease. Cham: Springer International Publishing; 2019. pp. 3–19. doi: 10.1007/978-3-030-11488-6_1 PubMed DOI

Mopper K, Zhou X. Hydroxyl Radical Photoproduction in the Sea and Its Potential Impact on Marine Processes. Science. 1990;250: 661–664. doi: 10.1126/science.250.4981.661 PubMed DOI

Sunday MO, Takeda K, Sakugawa H. Singlet Oxygen Photogeneration in Coastal Seawater: Prospect of Large-Scale Modeling in Seawater Surface and Its Environmental Significance. Environ Sci Technol. 2020;54: 6125–6133. doi: 10.1021/acs.est.0c00463 PubMed DOI

Dill KA, Bromberg S. Molecular driving forces: Statistical thermodynamics in biology, chemistry, physics, and nanoscience. 2nd ed. London; New York: Garland Science; 2011.

Zielonka J, Sikora A, Joseph J, Kalyanaraman B. Peroxynitrite Is the Major Species Formed from Different Flux Ratios of Co-generated Nitric Oxide and Superoxide: DIRECT REACTION WITH BORONATE-BASED FLUORESCENT PROBE. J Biol Chem. 2010;285: 14210–14216. doi: 10.1074/jbc.M110.110080 PubMed DOI PMC

Marla SS, Lee J, Groves JT. Peroxynitrite rapidly permeates phospholipid membranes. PNAS. 1997;94: 14243–14248. doi: 10.1073/pnas.94.26.14243 PubMed DOI PMC

Hayyan M, Hashim MA, AlNashef IM. Superoxide Ion: Generation and Chemical Implications. Chem Rev. 2016;116: 3029–3085. doi: 10.1021/acs.chemrev.5b00407 PubMed DOI

Fridovich I. Oxygen toxicity: A radical explanation. J Exp Biol. 1998;201: 1203–1209. doi: 10.1242/jeb.201.8.1203 PubMed DOI

Winterbourn CC, Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med. 2008;45: 549–561. doi: 10.1016/j.freeradbiomed.2008.05.004 PubMed DOI

Roe KL, Barbeau KA. Uptake mechanisms for inorganic iron and ferric citrate in Trichodesmium Erythraeum IMS101. Metallomics. 2014;6: 2042–2051. doi: 10.1039/c4mt00026a PubMed DOI

Rose A. The Influence of Extracellular Superoxide on Iron Redox Chemistry and Bioavailability to Aquatic Microorganisms. Front Microbiol. 2012;3: 124. doi: 10.3389/fmicb.2012.00124 PubMed DOI PMC

Kozuleva MA, Ivanov BN, Vetoshkina DV, Borisova-Mubarakshina MM. Minimizing an Electron Flow to Molecular Oxygen in Photosynthetic Electron Transfer Chain: An Evolutionary View. Front Plant Sci. 2020;11: 211. doi: 10.3389/fpls.2020.00211 PubMed DOI PMC

Blokhina O, Fagerstedt KV. Reactive oxygen species and nitric oxide in plant mitochondria: Origin and redundant regulatory systems. Physiologia Plantarum. 2010;138: 447–462. doi: 10.1111/j.1399-3054.2009.01340.x PubMed DOI

Asada K, Kiso K, Yoshikawa K. Univalent Reduction of Molecular Oxygen by Spinach Chloroplasts on Illumination. J Biol Chem. 1974;249: 2175–2181. doi: 10.1016/S0021-9258(19)42815-9 PubMed DOI

Kozuleva MA, Ivanov BN. Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids. Photosynth Res. 2010;105: 51–61. doi: 10.1007/s11120-010-9565-5 PubMed DOI

Pospíšil P. Production of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta (BBA)—Bioenergetics. 2009;1787: 1151–1160. doi: 10.1016/j.bbabio.2009.05.005 PubMed DOI

Pospíšil P. The Role of Metals in Production and Scavenging of Reactive Oxygen Species in Photosystem II. Plant Cell Physiol. 2014;55: 1224–1232. doi: 10.1093/pcp/pcu053 PubMed DOI

Solomon EI, Augustine AJ, Yoon J. O2 Reduction to H2O by the Multicopper Oxidases. Dalton Trans. 2008; 3921–3932. doi: 10.1039/b800799c PubMed DOI PMC

Messner KR, Imlay JA. Mechanism of Superoxide and Hydrogen Peroxide Formation by Fumarate Reductase, Succinate Dehydrogenase, and Aspartate Oxidase. J Biol Chem. 2002;277: 42563–42571. doi: 10.1074/jbc.M204958200 PubMed DOI

Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7: 405–410. doi: 10.1016/s1360-1385(02)02312-9 PubMed DOI

Zhang T, Hansel CM, Voelker BM, Lamborg CH. Extensive Dark Biological Production of Reactive Oxygen Species in Brackish and Freshwater Ponds. Environ Sci Technol. 2016;50: 2983–2993. doi: 10.1021/acs.est.5b03906 PubMed DOI

Diaz JM, Hansel CM, Voelker BM, Mendes CM, Andeer PF, Zhang T. Widespread Production of Extracellular Superoxide by Heterotrophic Bacteria. Science. 2013;340: 1223–1226. doi: 10.1126/science.1237331 PubMed DOI

Diaz JM, Plummer S, Tomas C, Alves-de-Souza C. Production of extracellular superoxide and hydrogen peroxide by five marine species of harmful bloom-forming algae. J Plankton Res. 2018;40: 667–677. doi: 10.1093/plankt/fby043 PubMed DOI PMC

Rose AL, Webb EA, Waite TD, Moffett JW. Measurement and Implications of Nonphotochemically Generated Superoxide in the Equatorial Pacific Ocean. Environ Sci Technol. 2008;42: 2387–2393. doi: 10.1021/es7024609 PubMed DOI

Schneider RJ, Roe KL, Hansel CM, Voelker BM. Species-Level Variability in Extracellular Production Rates of Reactive Oxygen Species by Diatoms. Frontiers in Chemistry. 2016;4. doi: 10.3389/fchem.2016.00005 PubMed DOI PMC

Sutherland KM, Coe A, Gast RJ, Plummer S, Suffridge CP, Diaz JM, et al.. Extracellular superoxide production by key microbes in the global ocean. Limnol Oceanogr. 2019;64: 2679–2693. doi: 10.1002/lno.11247 DOI

Kustka AB, Shaked Y, Milligan AJ, King DW, Morel FMM. Extracellular production of superoxide by marine diatoms: Contrasting effects on iron redox chemistry and bioavailability. Limnol Oceanogr. 2005;50: 1172–1180. doi: 10.4319/lo.2005.50.4.1172 DOI

Hansel CM, Buchwald C, Diaz JM, Ossolinski JE, Dyhrman ST, Mooy BASV, et al.. Dynamics of extracellular superoxide production by Trichodesmium Colonies from the Sargasso Sea. Limnol Oceanogr. 2016;61: 1188–1200. doi: 10.1002/lno.10266 DOI

Marshall J-A, de Salas M, Oda T, Hallegraeff G. Superoxide production by marine microalgae. Mar Biol. 2005;147: 533–540. doi: 10.1007/s00227-005-1596-7 DOI

Sutherland KM, Grabb KC, Karolewski JS, Plummer S, Farfan GA, Wankel SD, et al.. Spatial Heterogeneity in Particle-Associated, Light-Independent Superoxide Production Within Productive Coastal Waters. J Geophys Res Oceans. 2020;125: e2020JC016747. doi: 10.1029/2020JC016747 PubMed DOI PMC

Hansel CM, Diaz JM, Plummer S. Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant Roseobacter Clade. mBio. 2019;10: e02668–18. doi: 10.1128/mBio.02668-18 PubMed DOI PMC

Zafiriou OC. Chemistry of superoxide ion-radical (O2-) in seawater. I. (HOO) and uncatalyzed dismutation kinetics studied by pulse radiolysis. Mar Chem. 1990;30: 31–43. doi: 10.1016/0304-4203(90)90060-P DOI

Sutherland KM, Wankel SD, Hansel CM. Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. PNAS. 2020;117: 3433–3439. doi: 10.1073/pnas.1912313117 PubMed DOI PMC

Wuttig K, Heller MI, Croot PL. Pathways of Superoxide (O2) Decay in the Eastern Tropical North Atlantic. Environ Sci Technol. 2013; 130826150409004. doi: 10.1021/es401658t PubMed DOI

Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, et al.. Ecological Genomics of Marine Picocyanobacteria. Microbiol Mol Biol Rev. 2009;73: 249–299. doi: 10.1128/MMBR.00035-08 PubMed DOI PMC

Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. 3rd ed. Oxford: New York: Clarendon Press; Oxford University Press; 1999.

Seaver LC, Imlay JA. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia Coli. J Bacteriol. 2001;183: 7182–7189. doi: 10.1128/JB.183.24.7182-7189.2001 PubMed DOI PMC

Fedurayev PV, Mironov KS, Gabrielyan DA, Bedbenov VS, Zorina AA, Shumskaya M, et al.. Hydrogen Peroxide Participates in Perception and Transduction of Cold Stress Signal in Synechocystis. Plant Cell Physiol. 2018;59: 1255–1264. doi: 10.1093/pcp/pcy067 PubMed DOI

Avery GB, Cooper WJ, Kieber RJ, Willey JD. Hydrogen peroxide at the Bermuda Atlantic Time Series Station: Temporal variability of seawater hydrogen peroxide. Mar Chem. 2005;97: 236–244. doi: 10.1016/j.marchem.2005.03.006 DOI

Kelly TJ, Daum PH, Schwartz SE. Measurements of peroxides in cloudwater and rain. Journal of Geophysical Research: Atmospheres. 1985;90: 7861–7871. doi: 10.1029/JD090iD05p07861 DOI

Willey JD, Kieber RJ, Lancaster RD. Coastal rainwater hydrogen peroxide: Concentration and deposition. J Atmos Chem. 1996;25: 149–165. doi: 10.1007/BF00053789 DOI

Morris JJ, Johnson ZI, Wilhelm SW, Zinser ER. Diel regulation of hydrogen peroxide defenses by open ocean microbial communities. J Plankton Res. 2016;38: 1103–1114. doi: 10.1093/plankt/fbw016 DOI

Yuan J, Shiller AM. The distribution of hydrogen peroxide in the southern and central Atlantic ocean. Deep Sea Research Part II: Topical Studies in Oceanography. 2001;48: 2947–2970. doi: 10.1016/S0967-0645(01)00026-1 DOI

Bond RJ, Hansel CM, Voelker BM. Heterotrophic Bacteria Exhibit a Wide Range of Rates of Extracellular Production and Decay of Hydrogen Peroxide. Front Mar Sci. 2020;7: 72. doi: 10.3389/fmars.2020.00072 DOI

Sengupta D, Mazumder S, Cole JV, Lowry S. Controlling Non-Catalytic Decomposition of High Concentration Hydrogen Peroxide: Fort Belvoir, VA: Defense Technical Information Center; 2004. Feb. doi: 10.21236/ADA426795 DOI

Millero FJ, Sharma VK, Karn B. The rate of reduction of copper(II) with hydrogen peroxide in seawater. Mar Chem. 1991;36: 71–83. doi: 10.1016/S0304-4203(09)90055-X DOI

Moffett JW, Zika RG. Reaction kinetics of hydrogen peroxide with copper and iron in seawater. Environ Sci Technol. 1987;21: 804–810. doi: 10.1021/es00162a012 PubMed DOI

Vardi A, Formiggini F, Casotti R, De Martino A, Ribalet F, Miralto A, et al.. A Stress Surveillance System Based on Calcium and Nitric Oxide in Marine Diatoms. PLoS Biol. 2006;4: e60. doi: 10.1371/journal.pbio.0040060 PubMed DOI PMC

Thomson PG. Ecophysiology of the brine dinoflagellate, Polarella Glacialis, and Antarctic fast ice brine communities. PhD thesis, University of Tasmania. 2000.

Vardi A, Bidle KD, Kwityn C, Hirsh DJ, Thompson SM, Callow JA, et al.. A Diatom Gene Regulating Nitric-Oxide Signaling and Susceptibility to Diatom-Derived Aldehydes. Current Biology. 2008;18: 895–899. doi: 10.1016/j.cub.2008.05.037 PubMed DOI

Vardi A. Cell signaling in marine diatoms. Commun Integr Biol. 2008;1: 134–136. doi: 10.4161/cib.1.2.6867 PubMed DOI PMC

Zafiriou OC, McFarland M, Bromund RH. Nitric Oxide in Seawater. Science. 1980;207: 637–639. Available: https://www.jstor.org/stable/1683488 doi: 10.1126/science.207.4431.637 PubMed DOI

Fujiwara T, Fukumori Y. Cytochrome cb-type nitric oxide reductase with cytochrome c oxidase activity from Paracoccus denitrificans ATCC 35512. J Bacteriol. 1996;178: 1866–1871. doi: 10.1128/jb.178.7.1866-1871.1996 PubMed DOI PMC

Jahnová J, Luhová L, Petřivalský M. S-Nitrosoglutathione Reductase of Protein S-Nitrosation in Plant NO Signaling. Plants (Basel). 2019;8: 48. doi: 10.3390/plants8020048 PubMed DOI PMC

Collin F. Chemical Basis of Reactive Oxygen Species Reactivity and Involvement in Neurodegenerative Diseases. Int J Mol Sci. 2019;20. doi: 10.3390/ijms20102407 PubMed DOI PMC

Marusawa H, Ichikawa K, Narita N, Murakami H, Ito K, Tezuka T. Hydroxyl radical as a strong electrophilic species. Bioorganic & Medicinal Chemistry. 2002;10: 2283–2290. doi: 10.1016/S0968-0896(02)00048-2 PubMed DOI

Gutteridge JM. Reactivity of hydroxyl and hydroxyl-like radicals discriminated by release of thiobarbituric acid-reactive material from deoxy sugars, nucleosides and benzoate. Biochem J. 1984;224: 761–767. doi: 10.1042/bj2240761 PubMed DOI PMC

McGill MR, Jaeschke H. Chapter 4—Oxidant Stress, Antioxidant Defense, and Liver Injury. In: Kaplowitz N, DeLeve LD, editors. Drug-Induced Liver Disease (Third Edition). Boston: Academic Press; 2013. pp. 71–84. doi: 10.1016/B978-0-12-387817-5.00004–2 DOI

Davies KJ, Goldberg AL. Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells. J Biol Chem. 1987;262: 8227–8234. doi: 10.1016/S0021-9258(18)47553-9 PubMed DOI

Brezonik PL, Fulkerson-Brekken J. Nitrate-Induced Photolysis in Natural Waters:  Controls on Concentrations of Hydroxyl Radical Photo-Intermediates by Natural Scavenging Agents. Environ Sci Technol. 1998;32: 3004–3010. doi: 10.1021/es9802908 DOI

Morris JJ, Lenski RE, Zinser ER. The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss. mBio. 2012;3: e00036-12–e00036-12. doi: 10.1128/mBio.00036-12 PubMed DOI PMC

Morris JJ, Johnson ZI, Szul MJ, Keller M, Zinser ER. Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean’s Surface. Rodriguez-Valera F, editor. PLoS ONE. 2011;6: e16805. doi: 10.1371/journal.pone.0016805 PubMed DOI PMC

Zinser ER. Cross-protection from hydrogen peroxide by helper microbes: The impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities. Environ Microbiol Rep. 2018;0. doi: 10.1111/1758-2229.12625 PubMed DOI

Morris JJ, Kirkegaard R, Szul MJ, Johnson ZI, Zinser ER. Facilitation of Robust Growth of Prochlorococcus Colonies and Dilute Liquid Cultures by "Helper" Heterotrophic Bacteria. Appl Environ Microbiol. 2008;74: 4530–4534. doi: 10.1128/AEM.02479-07 PubMed DOI PMC

Coe A, Ghizzoni J, LeGault K, Biller S, Roggensack SE, Chisholm SW. Survival of Prochlorococcus in extended darkness. Limnol Oceanogr. 2016;61: 1375–1388. doi: 10.1002/lno.10302 DOI

Omar NM, Prášil O, McCain JSP, Campbell DA. Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H2O2 as a Case Study. Microorganisms. 2022;10: 821. doi: 10.3390/microorganisms10040821 PubMed DOI PMC

Mitchell JG, Seuront L, Doubell MJ, Losic D, Voelcker NH, Seymour J, et al.. The Role of Diatom Nanostructures in Biasing Diffusion to Improve Uptake in a Patchy Nutrient Environment. PLoS One. 2013;8: e59548. doi: 10.1371/journal.pone.0059548 PubMed DOI PMC

DellaPenna D, Pogson BJ. VITAMIN SYNTHESIS IN PLANTS: Tocopherols and Carotenoids. Annual Review of Plant Biology. 2006;57: 711–738. doi: 10.1146/annurev.arplant.56.032604.144301 PubMed DOI

Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive Oxygen Species, Oxidative Damage, and Antioxidative Defense Mechanism in Plants under Stressful Conditions. Journal of Botany. 2012;2012: e217037. doi: 10.1155/2012/217037 DOI

Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2016;44: D7–D19. doi: 10.1093/nar/gkv1290 PubMed DOI PMC

Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, et al.. The Genome Portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res. 2012;40: D26–D32. doi: 10.1093/nar/gkr947 PubMed DOI PMC

Nordberg H, Cantor M, Dusheyko S, Hua S, Poliakov A, Shabalov I, et al.. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res. 2014;42: D26–31. doi: 10.1093/nar/gkt1069 PubMed DOI PMC

Youens-Clark K, Bomhoff M, Ponsero AJ, Wood-Charlson EM, Lynch J, Choi I, et al.. iMicrobe: Tools and data-driven discovery platform for the microbiome sciences. GigaScience. 2019;8. doi: 10.1093/gigascience/giz083 PubMed DOI PMC

Leinonen R, Akhtar R, Birney E, Bower L, Cerdeno-Tárraga A, Cheng Y, et al.. The European Nucleotide Archive. Nucleic Acids Res. 2011;39: D28–D31. doi: 10.1093/nar/gkq967 PubMed DOI PMC

Vandepoele K, Van Bel M, Richard G, Van Landeghem S, Verhelst B, Moreau H, et al.. Pico-PLAZA, a genome database of microbial photosynthetic eukaryotes. Environ Microbiol. 2013;15: 2147–2153. doi: 10.1111/1462-2920.12174 PubMed DOI

Matasci N, Hung L-H, Yan Z, Carpenter EJ, Wickett NJ, Mirarab S, et al.. Data access for the 1,000 Plants (1KP) project. Gigascience. 2014;3: 17. doi: 10.1186/2047-217X-3-17 PubMed DOI PMC

Liew YJ, Aranda M, Voolstra CR. Reefgenomics.Org—a repository for marine genomics data. Database (Oxford). 2016;2016. doi: 10.1093/database/baw152 PubMed DOI PMC

Mölder F, Jablonski KP, Letcher B, Hall MB, Tomkins-Tinch CH, Sochat V, et al.. Sustainable data analysis with Snakemake. F1000Research; 2021. doi: 10.12688/f1000research.29032.2 PubMed DOI PMC

Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, et al.. Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper. Mol Biol Evol. 2017;34: 2115–2122. doi: 10.1093/molbev/msx148 PubMed DOI PMC

Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale. Bioinformatics; 2021. Jun. doi: 10.1093/molbev/msab293 PubMed DOI PMC

Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12: 59–60. doi: 10.1038/nmeth.3176 PubMed DOI

Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, et al.. eggNOG 5.0: A hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research. 2019;47: D309–D314. doi: 10.1093/nar/gky1085 PubMed DOI PMC

Team RC. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2019.

RStudio Team. RStudio: Integrated Development Environment for R. Boston, MA: RStudio, Inc.; 2015.

Wickham H. Tidyverse: Easily Install and Load the ‘Tidyverse’. 2017.

Robinson D, Hayes A. Broom: Convert Statistical Analysis Objects into Tidy Tibbles. 2019.

Bache SM, Wickham H. Magrittr: A Forward-Pipe Operator for R. 2014.

Wickham H, François R, Henry L, Müller K. Dplyr: A Grammar of Data Manipulation. 2018.

Mangiafico S. Rcompanion: Functions to Support Extension Education Program Evaluation. 2020.

Warnes GR, Bolker B, Lumley T, Johnson R. Gmodels: Various R Programming Tools for Model Fitting. 2018.

Kleiber C, Zeileis A. AER: Applied Econometrics with R. 2020.

Warton DI, Duursma RA, Falster DS, Taskinen S. Smatr 3—an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution. 2012;3: 257–259.

Sauer S. Convert logit to probability. 2017.

Wickham H. Ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag; New York; 2016.

Wilke CO. Cowplot: Streamlined Plot Theme and Plot Annotations for ‘Ggplot2’. 2019.

Hester J. Glue: Interpreted String Literals. 2018.

Zhu H. kableExtra: Construct Complex Table with ‘kable’ and Pipe Syntax. 2019.

Wei T, Simko V. R package "corrplot": Visualization of a Correlation Matrix. 2017.

Tang Y, Horikoshi M, Li W. Ggfortify: Unified Interface to Visualize Statistical Result of Popular R Packages. The R Journal. 2016;8: 478–489.

Horikoshi M, Tang Y. Ggfortify: Data Visualization Tools for Statistical Analysis Results. 2018.

Pedersen TL, RStudio. Ggforce: Accelerating ‘Ggplot2’. 2021.

Xie Y. Knitr A Comprehensive Tool for Reproducible Research in R. Implementing Reproducible Research. Chapman and Hall/CRC; 2014.

Xie Y. Dynamic Documents with R and knitr. Second. Boca Raton, Florida: Chapman and Hall/CRC; 2015.

Xie Y. Knitr: A General-Purpose Package for Dynamic Report Generation in R. 2018.

Xie Y. Bookdown: Authoring books and technical documents with R markdown. 2019.

Aust F. Citr: ‘RStudio’ Add-in to Insert Markdown Citations. 2018.

Chang A, Jeske L, Ulbrich S, Hofmann J, Koblitz J, Schomburg I, et al.. BRENDA, the ELIXIR core data resource in 2021: New developments and updates. Nucleic Acids Research. 2021;49: D498–D508. doi: 10.1093/nar/gkaa1025 PubMed DOI PMC

Lundgren CAK, Sjöstrand D, Biner O, Bennett M, Rudling A, Johansson A-L, et al.. Scavenging of superoxide by a membrane-bound superoxide oxidase. Nat Chem Biol. 2018;14: 788–793. doi: 10.1038/s41589-018-0072-x PubMed DOI PMC

Matlashov ME, Belousov VV, Enikolopov G. How Much H2O2 Is Produced by Recombinant D-Amino Acid Oxidase in Mammalian Cells? Antioxid Redox Signal. 2014;20: 1039–1044. doi: 10.1089/ars.2013.5618 PubMed DOI PMC

Bou-Abdallah F, Yang H, Awomolo A, Cooper B, Woodhall MR, Andrews SC, et al.. Functionality of the Three-Site Ferroxidase Center of Escherichia Coli Bacterial Ferritin (EcFtnA). Biochemistry. 2014;53: 483–495. doi: 10.1021/bi401517f PubMed DOI PMC

Fleury K. Reactive Oxygen Detoxification Genes in Phytoplankton. Bachelor of {{Science}}, {{Honors}} Thesis, Mount Allison University. 2019.

Omar N. Reactive Oxygen Production and Scavenging in Marine Phytoplankton. Bachelor of {{Science}}, {{Honors}} Thesis, Mount Allison University. 2020.

Shapiro SS, Wilk MB. An Analysis of Variance Test for Normality (Complete Samples). Biometrika. 1965;52: 591. doi: 10.2307/2333709 DOI

Anova.glm function—RDocumentation.

McFadden D. Quantitative Methods for Analyzing Travel Behaviour of Individuals: Some Recent Developments. Cowles Foundation Discussion Papers. 1977.

Kassambara A. Ggpubr: ‘ggplot2’ Based Publication Ready Plots. 2018.

Diaz JM, Plummer S, Hansel CM, Andeer PF, Saito MA, McIlvin MR. NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira Oceanica. PNAS. 2019;116: 16448–16453. doi: 10.1073/pnas.1821233116 PubMed DOI PMC

Mella-Flores D, Six C, Ratin M, Partensky F, Boutte C, Le Corguillé G, et al.. Prochlorococcus and Synechococcus have Evolved Different Adaptive Mechanisms to Cope with Light and UV Stress. Front Microbiol. 2012;3: 285. doi: 10.3389/fmicb.2012.00285 PubMed DOI PMC

Pospíšil P. Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta (BBA)—Bioenergetics. 2012;1817: 218–231. doi: 10.1016/j.bbabio.2011.05.017 PubMed DOI

Pospíšil P. Production of Reactive Oxygen Species by Photosystem II as a Response to Light and Temperature Stress. Frontiers in Plant Science. 2016;7. doi: 10.3389/fpls.2016.01950 PubMed DOI PMC

Bergamini C, Gambetti S, Dondi A, Cervellati C. Oxygen, Reactive Oxygen Species and Tissue Damage. CPD. 2004;10: 1611–1626. doi: 10.2174/1381612043384664 PubMed DOI

Miller A-F. Superoxide dismutases: Ancient enzymes and new insights. FEBS Lett. 2012;586: 585–595. doi: 10.1016/j.febslet.2011.10.048 PubMed DOI PMC

Groussman RD, Parker MS, Armbrust EV. Diversity and Evolutionary History of Iron Metabolism Genes in Diatoms. PLOS ONE. 2015;10: e0129081. doi: 10.1371/journal.pone.0129081 PubMed DOI PMC

Bernroitner M, Zamocky M, Furtmüller PG, Peschek GA, Obinger C. Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteria. J Exp Bot. 2009;60: 423–440. doi: 10.1093/jxb/ern309 PubMed DOI

Pandey P, Singh J, Achary VMM, Reddy MK. Redox homeostasis via gene families of ascorbate-glutathione pathway. Front Environ Sci. 2015;3. doi: 10.3389/fenvs.2015.00025 DOI

Randhawa V, Thakkar M, Wei L. Applicability of Hydrogen Peroxide in Brown Tide Control Culture and Microcosm Studies. PLOS ONE. 2012;7: e47844. doi: 10.1371/journal.pone.0047844 PubMed DOI PMC

Picciano AL, Crane BR. A nitric oxide synthaselike protein from Synechococcus produces NO/NO3- from l-arginine and NAPDH in a tetrahydrobiopterin- and Ca2+-dependent manner. J Biol Chem. 2019;294: 10708–10719. doi: 10.1074/jbc.RA119.008399 PubMed DOI PMC

Zweier JL, Samouilov A, Kuppusamy P. Non-enzymatic nitric oxide synthesis in biological systems. Biochim Biophys Acta. 1999;1411: 250–262. doi: 10.1016/s0005-2728(99)00018-3 PubMed DOI

Chen Y-C, Chen Y-H, Chiu H, Ko Y-H, Wang R-T, Wang W-P, et al.. Cell-Penetrating Delivery of Nitric Oxide by Biocompatible Dinitrosyl Iron Complex and Its Dermato-Physiological Implications. Int J Mol Sci. 2021;22: 10101. doi: 10.3390/ijms221810101 PubMed DOI PMC

Lampe RH, Wang S, Cassar N, Marchetti A. Strategies among phytoplankton in response to alleviation of nutrient stress in a subtropical gyre. ISME J. 2019;13: 2984–2997. doi: 10.1038/s41396-019-0489-6 PubMed DOI PMC

Peifeng L, Min Z, Chunying L, Guipeng Y. Effects of Nitric Oxide On The Growth of The Marine Microalgae And The Parameters of Carbonate Chemistry. In Review; 2021. May. doi: 10.21203/rs.3.rs-521371/v1 DOI

Thompson SEM, Taylor AR, Brownlee C, Callow ME, Callow JA. The Role of Nitric Oxide in Diatom Adhesion in Relation to Substratum Properties. J Phycol. 2008;44: 967–976. doi: 10.1111/j.1529-8817.2008.00531.x PubMed DOI

Hunsucker KZ, Swain GW. In situ measurements of diatom adhesion to silicone-based ship hull coatings. J Appl Phycol. 2016;28: 269–277. doi: 10.1007/s10811-015-0584-7 DOI

Di Dato V, Musacchia F, Petrosino G, Patil S, Montresor M, Sanges R, et al.. Transcriptome sequencing of three Pseudo-nitzschia species reveals comparable gene sets and the presence of Nitric Oxide Synthase genes in diatoms. Scientific Reports. 2015;5: 1–14. doi: 10.1038/srep12329 PubMed DOI PMC

Vihtakari M. ggOceanMaps: Plot Data on Oceanographic Maps using ‘Ggplot2’. Zenodo; 2021. doi: 10.5281/zenodo.4554715 DOI