Abstract
Iron determines the abundance and diversity of life and controls primary production in numerous aqueous environments. Over the past decades, the availability of this metal in natural waters has decreased. Iron deficiency can apply a selective pressure on microbial aquatic communities. Each aquatic organism has their individual requirements for iron and pathways for metal acquisition, despite all having access to the common pool of iron. Cyanobacteria, a photosynthesizing bacterium that can accumulate and form so-called ‘algal blooms’, have evolved strategies to thrive in such iron-deficient aqueous environments where they can outcompete other organisms in iron acquisition in diverse microbial communities. Metabolic pathways for iron acquisition employed by cyanobacteria allow it to compete successfully for this essential nutrient. By competing more effectively for requisite iron, cyanobacteria can displace other species and grow to dominate the microbial population in a bloom. Aquatic resources are damaged by a diverse number of environmental pollutants that can further decrease metal availability and result in a functional deficiency of available iron. Pollutants can also increase iron demand. A pollutant-exposed microbe is compelled to acquire further metal critical to its survival. Even in pollutant-impacted waters, cyanobacteria enjoy a competitive advantage and cyanobacterial dominance can be the result. We propose that cyanobacteria have a distinct competitive advantage over many other aquatic microbes in polluted, iron-poor environments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbaspour N, Hurrell R, Kelishadi R (2014) Review on iorn and its importance for human health. J Res Med Sci 19:164–174
Ahmad S, Rao GS (1999) Complexation of 1,2,4-benzenetriol with inorganic and ferritin-released iron in vitro. Biochem Biophys Res Commun 259(1):169–171. https://doi.org/10.1006/bbrc.1999.0741
Alexova R, Fujii M, Birch D, Cheng J, Waite TD, Ferrari BC et al (2011) Iron uptake and toxin synthesis in the bloom-forming Microcystis aeruginosa under iron limitation. Environ Microbiol 13(4):1064–1077. https://doi.org/10.1111/j.1462-2920.2010.02412.x
Arstol E, Hohmann-Marriott MF (2019) Cyanobacterial siderophores-physiology, structure, biosynthesis, and applications. Mar Drugs. https://doi.org/10.3390/md17050281
Benner R (2011) Loose ligands and available iron in the ocean. Proc Natl Acad Sci U S A 108(3):893–894. https://doi.org/10.1073/pnas.1018163108
Berry JP, Gantar M, Perez MH, Berry G, Noriega FG (2008) Cyanobacterial toxins as allelochemicals with potential applications as algaecides, herbicides and insecticides. Mar Drugs 6:117–146. https://doi.org/10.3390/md20080007
Blanco-Ameijeiras S, Cabanes DJE, Cable RN, Trimborn S, Jacquet S, Wiegmann S et al (2020) Exopolymeric substances control microbial community structure and function by contributing to both C and Fe nutrition in Fe-limited southern ocean provinces. Microorganisms. https://doi.org/10.3390/microorganisms8121980
Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T, Murdoch R et al (2000) A mesoscale phytoplankton bloom in the polar southern ocean stimulated by iron fertilization. Nature 407(6805):695–702. https://doi.org/10.1038/35037500
Canini A, Leonardi D, Grilli Caiola M (2001) Superoxide dismutase activity in the cyanobacterium Microcystis aeruginosa after surface bloom formation. New Phytol 152:107–116
Cao HS, Kong FX, Tan JK, Zhang XF, Tao Y, Yang Z (2005) Recruitment of total phytoplankton, chlorophytes and cyanobacteria from lake sediments recorded by photosynthetic pigments in a large, shallow lake (Lake Taihu, China). Int Rev Hydrobiol 90(4):347–357. https://doi.org/10.1002/iroh.200410783
Ceballos-Laita L, Marcuello C, Lostao A, Calvo-Begueria L, Velazquez-Campoy A, Bes MT et al (2017) Microcystin-LR binds iron, and iron promotes self-assembly. Environ Sci Technol 51(9):4841–4850. https://doi.org/10.1021/acs.est.6b05939
Chen M, Wang WX, Guo LD (2004) Phase partitioning and solubility of iron in natural seawater controlled by dissolved organic matter. Glob Biogeochem Cycles. https://doi.org/10.1029/2003gb002160
Chobot V, Hadacek F (2010) Iron and its complexation by phenolic cellular metabolites: from oxidative stress to chemical weapons. Plant Signal Behav 5(1):4–8. https://doi.org/10.4161/psb.5.1.10197
Cornwall W (2023) Iron stress threatens southern ocean phytoplankton. Science 379(6634):741–742. https://doi.org/10.1126/science.adh2763
Dansie AP, Thomas DSG, Wiggs GFS, Baddock MC, Ashpole I (2022) Plumes and blooms-locally-sourced Fe-rich aeolian mineral dust drives phytoplankton growth off southwest Africa. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2022.154562
De Philippis R, Margheri MC, Materassi R, Vincenzini M (1998) Potential of unicellular cyanobacteria from saline environments as exopolysaccharide producers. Appl Environ Microbiol 64(3):1130–1132
Enzingmuller-Bleyl TC, Boden JS, Herrmann AJ, Ebel KW, Sanchez-Baracaldo P, Frankenberg-Dinkel N et al (2022) On the trail of iron uptake in ancestral Cyanobacteria on early Earth. Geobiology 20(6):776–789. https://doi.org/10.1111/gbi.12515
Fiorito F, Irace C, Di Pascale A, Colonna A, Iovane G, Pagnini U et al (2013) 2,3,7,8-Tetrachlorodibenzo-p-dioxin promotes BHV-1 infection in mammalian cells by interfering with iron homeostasis regulation. PLoS ONE 8(3):e58845. https://doi.org/10.1371/journal.pone.0058845
Fu QL, Fujii M, Natsuike M, Waite TD (2019) Iron uptake by bloom-forming freshwater cyanobacterium Microcystis aeruginosa in natural and effluent waters. Environ Pollut 247:392–400. https://doi.org/10.1016/j.envpol.2019.01.071
Galaris D, Barbouti A, Pantopoulos K (2019) Iron homeosatsis and oxidative stress: an intimate relationship. BBA—Mol Cell Res 1866:118
Ghio AJ, Stonehuerner J, Soukup JM, Dailey LA, Kesic MJ, Cohen MD (2015) Iron diminishes the in vitro biological effect of vanadium. J Inorg Biochem 147:126–133. https://doi.org/10.1016/j.jinorgbio.2015.03.008
Ghio AJ, Soukup JM, Dailey LA, Madden MC (2020) Air pollutants disrupt iron homeostasis to impact oxidant generation, biological effects, and tissue injury. Free Radic Biol Med 151:38–55. https://doi.org/10.1016/j.freeradbiomed.2020.02.007
Gillis B, Gavin IM, Arbieva Z, King ST, Jayaraman S, Prabhakar BS (2007) Identification of human cell responses to benzene and benzene metabolites. Genomics 90(3):324–333. https://doi.org/10.1016/j.ygeno.2007.05.003
Gledhill M, Buck KN (2012) The organic complexation of iron in the marine environment: a review. Front Microbiol 3:69. https://doi.org/10.3389/fmicb.2012.00069
Gonzalez A, Sevilla E, Bes MT, Peleato ML, Fillat MF (2016) Pivotal role of iron in the regulation of cyanobacterial electron transport. Adv Microb Physiol 68:169–217. https://doi.org/10.1016/bs.ampbs.2016.02.005
González A, Fillat MF, Bes MT, Peleato ML, Sevilla E (2018) The challenge of iron stress in cyanobacteria. In: Tiwari A (ed) Cyanobacteria. InTech, Houston, pp 1–31. https://doi.org/10.5772/intechopen.76720
Guo W, Zhang J, Li W, Xu M, Liu S (2015) Disruption of iron homeostasis and resultant health effects upon exposure to various environmental pollutants: a critical review. J Environ Sci (china) 34:155–164. https://doi.org/10.1016/j.jes.2015.04.004
Hassler CS, Schoemann V, Nichols CM, Butler EC, Boyd PW (2011) Saccharides enhance iron bioavailability to southern ocean phytoplankton. Proc Natl Acad Sci USA 108(3):1076–1081
Honey S, O’Keefe P, Drahushuk AT, Olson JR, Kumar S, Sikka HC (2000) Metabolism of benzo(a)pyrene by duck liver microsomes. Comp Biochem Physiol C Toxicol Pharmacol 126(3):285–292. https://doi.org/10.1016/s0742-8413(00)00121-3
Hudson RJM, Morel FMM (1993) Trace-metal transport by marine microorganisms—implications of metal coordination kinetics. Deep-Sea Res Part I-Oceanogr Res Pap 40(1):129–150
Hunter KA, Boyd PW (2007) Iron-binding ligands and their role in the ocean biogeochemistry of iron. Environ Chem 4(4):221–232
Jang M-H, Kyong H, Takamura N (2007) Reciprocal allelopathic responses between toxic cyanobacteria (Microcystis aeruginosa) and duckweed (Lemna japonica). Toxicon 49:727–733. https://doi.org/10.1016/j.toxicon.2006.11.017
Juneau P, Dewez D, Matsui S, Kim SG, Popovic R (2001) Evaluation of different algal species sensitivity to mercury and metolachlor by PAM-fluorometry. Chemosphere 45(4–5):589
Klein AR, Baldwin DS, Silvester E (2013) Proton and iron binding by the cyanobacterial toxin microcystin-LR. Environ Sci Technol 47:5178–5184. https://doi.org/10.1021/es400464e
Kolachana P, Subrahmanyam VV, Meyer KB, Zhang L, Smith MT (1993) Benzene and its phenolic metabolites produce oxidative DNA damage in HL60 cells in vitro and in the bone marrow in vivo. Cancer Res 53(5):1023–1026
Kramer J, Ozkaya O, Kummerli R (2020) Bacterial siderophores in community and host interactions. Nat Rev Microbiol 18(3):152–163. https://doi.org/10.1038/s41579-019-0284-4
Kuwabara JS, Topping BR, Lynch DD, Carter JL, Essaid HI (2009) Benthic nutrient sources to hypereutrophic upper Klamath Lake, Oregon, USA. Environ Toxicol Chem 28(3):516–524
Lee N, Kim W, Chung J, Lee Y, Cho S, Jang KS et al (2020) Iron competition triggers antibiotic biosynthesis in Streptomyces coelicolor during coculture with Myxococcus xanthus. ISME J 14(5):1111–1124
Li PF, Cai YF, Shi LM, Geng LF, Xing P, Yu Y et al (2009) Microbial Degradation and Preliminary Chemical Characterization of Microcystis Exopolysaccharides from a Cyanobacterial Water Bloom of Lake Taihu. Int Rev Hydrobiol 94(6):645–655. https://doi.org/10.1002/iroh.200911149
Li ZK, Dai GZ, Juneau P, Qiu BS (2016) Capsular polysaccharides facilitate enhanced iron acquisition by the colonial cyanobacterium Microcystis sp. isolated from a freshwater lake. J Phycol 52(1):105–115. https://doi.org/10.1111/jpy.12372
Lis H, Shaked Y, Kranzler C, Keren N, Morel FMM (2015) Iron bioavailability to phytoplankton: an empirical approach. ISME J 9(4):1003–1013
Lyck S, Gjølme N, Utkilen H (1996) Iron starvation increases toxicity of Microcystis aeruginosa CYA 228/1 (Chroococcales, Cyanophyceae). Phycologia 35(sup6):120–124. https://doi.org/10.2216/i0031-8884-35-6S-120.1
Majsterek I, Sicinska P, Tarczynska M, Zalewski M, Walter Z (2004) Toxicity of microcystin from cyanobacteria growing in a source of drinking water. Comp Biochem Physiol C Toxicol Pharmacol 139(1–3):175–179. https://doi.org/10.1016/j.cca.2004.10.007
Manis J, Kim G (1979) Stimulation of iron absorption by polychlorinated aromatic hydrocarbons. Am J Physiol 236(6):E763-768
Martin JH, Gordon RM, Fitzwater SE (1991) The case for iron. Limnol Oceanogr 36(8):1793–1802
Melikian AA, Sun P, Prokopczyk B, El-Bayoumy K, Hoffmann D, Wang X et al (1999) Identification of benzo[a]pyrene metabolites in cervical mucus and DNA adducts in cervical tissues in humans by gas chromatography-mass spectrometry. Cancer Lett 146(2):127–134. https://doi.org/10.1016/s0304-3835(99)00203-7
Morel FMM, Kustka AB, Shaked Y (2008) The role of unchelated Fe in the iron nutrition of phytoplankton. Limnol Oceanogr 53(1):400–404
Murugappan R, Karthikeyan M, Aravinth A, Alamelu M (2012) Siderophore-mediated iron uptake promotes yeast-bacterial symbiosis. Appl Biochem Biotechnol 168(8):2170–2183. https://doi.org/10.1007/s12010-012-9926-y
Orihel DM, Schindler DW, Ballard NC, Wilson LR, Vinebrooke RD (2016) Experimental iron amendment suppresses toxic cyanobacteria in a hypereutrophic lake. Ecol Appl 26(5):1517–1534. https://doi.org/10.1890/15-1928
Paerl HW, Fulton RS 3rd, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci World J 1:76–113. https://doi.org/10.1100/tsw.2001.16
Perron NR, Brumaghim JL (2009) A review of the antioxidant mechanisms of polyphenol compounds related to iron binding. Cell Biochem Biophys 53(2):75–100. https://doi.org/10.1007/s12013-009-9043-x
Qiu GW, Lou WJ, Sun CY, Yang N, Li ZK, Li DL et al (2018) Outer membrane iron uptake pathways in the model cyanobacterium synechocystis sp strain PCC 6803. Appl Environ Microbiol 84(19):e01512–e01518. https://doi.org/10.1128/AEM.01512-18
Raghuvanshi R, Singh S, Bisen PS (2007) Iron mediated regulation of growth and siderophore production in a diazotrophic cyanobacterium Anabaena cylindrica. Indian J Exp Biol 45(6):563–567
Řezanka T, Palyzová A, Sigler K (2018) Isolation and identification of siderophores produced by cyanobacteria. Folia Microbiol (praha) 63(5):569–579. https://doi.org/10.1007/s12223-018-0626-z
Ryan-Keogh TJ, Thomalla SJ, Monteiro PMS, Tagliabue A (2023) Multidecadal trend of increasing iron stress in southern ocean phytoplankton. Science 379(6634):834–840. https://doi.org/10.1126/science.abl5237
Sachan N, Tiwari N, Patel DK, Katiyar D, Srikrishna S, Singh MP (2023) Dyshomeostasis of iron and its transporter proteins in cypermethri-induced Parkinson’s disease. Mol Neurobiol. https://doi.org/10.1007/s12035-023-03436-2
Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int 23:3984–3999. https://doi.org/10.1007/s11356-015-4294-0
Sakaki T, Yamamoto K, Ikushiro S (2013) Possibility of application of cytochrome P450 to bioremediation of dioxins. Biotechnol Appl Biochem 60(1):65–70
Santamaria R, Fiorito F, Irace C, De Martino L, Maffettone C, Granato GE et al (2011) 2,3,7,8-Tetrachlorodibenzo-p-dioxin impairs iron homeostasis by modulating iron-related proteins expression and increasing the labile iron pool in mammalian cells. Biochim Biophys Acta 1813(5):704–712. https://doi.org/10.1016/j.bbamcr.2011.02.003
Schreinemachers DM, Ghio AJ (2016) Effects of environmental pollutants on cellular iron homeostasis and ultimate links to human disease. Environ Health Insights 10:35–43. https://doi.org/10.4137/EHI.S36225
Schröder I, Johnson E, de Vries S (2003) Microbial ferric iron reductases. FEMS Microbiol Rev 27:427–447. https://doi.org/10.1016/S0168-6445(03)00043-3
Shaked Y, Lis H (2012) Disassembling iron availability to phytoplankton. Front Microbiol 3:123. https://doi.org/10.3389/fmicb.2012.00123
Sunda WG, Huntsman SA (1997) Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390(6658):389–392
Sutak R, Camadro JM, Lesuisse E (2020) Iron uptake mechanisms in marine phytoplankton. Front Microbiol. https://doi.org/10.3389/fmicb.2020.566691
Tapia JM, Munoz JA, Gonzalez F, Blazquez ML, Ballester A (2011) Mechanism of adsorption of ferric iron by extracellular polymeric substances (EPS) from a bacterium Acidiphilium sp. Water Sci Technol 64(8):1716–1722. https://doi.org/10.2166/wst.2011.649
Tease BE, Walker RW (1987) Comparative composition of the sheath of the cyanobacterium gloeothece Atcc-27152 cultured with and without combined nitrogen. J Gen Microbiol 133:3331–3339
Theil EC, Goss DJ (2009) Living with iron (and oxygen): questions and answers about iron homeostasis. Chem Rev 109:4568–4579. https://doi.org/10.1021/cr900052g
Tronnet S, Garcie C, Rehm N, Dobrindt U, Oswald E, Martin P (2016) Iron homeostasis regulates the genotoxicity of Escherichia coli that produces colibactin. Infect Immun 84(12):3358–3368. https://doi.org/10.1128/Iai.00659-16
Utkilen H, Gjolme N (1995) Iron-stimulated toxin production in Microcystis aeruginosa. Appl Environ Microbiol 61(2):797–800. https://doi.org/10.1128/aem.61.2.797-800.1995
Vepritskii AA, Gromov BV, Titota NN, Mamkaeva KA (1991) Production of the antibiotic algicide cyanobacterin LU-2 by a filamentous cyanobacterium Nostoc sp. Mikrobiologia 60:21–25
Vraspir JM, Butler A (2009) Chemistry of marine ligands and siderophores. Ann Rev Mar Sci 1:43–63. https://doi.org/10.1146/annurev.marine.010908.163712
Wahba ZZ, Al-Bayati ZA, Stohs SJ (1988) Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the hepatic distribution of iron, copper, zinc, and magnesium in rats. J Biochem Toxicol 3:121–129. https://doi.org/10.1002/jbt.2570030206
Wang X, Wu Y, Stonehuerner JG, Dailey LA, Richards JD, Jaspers I, Piantadosi CA, Ghio AJ (2006) Oxidant generation promotes iron sequestration in BEAS-2B cells exposed to asbestos. Am J Respir Cell Mol Biol 34(3):286–292. https://doi.org/10.1165/rcmb.2004-0275OC
Wang C, Wang X, Wang P, Chen B, Hou J, Qian J et al (2016) Effects of iron on growth, antioxidant enzyme activity, bound extracellular polymeric substances and microcystin production of Microcystis aeruginosa FACHB-905. Ecotoxicol Environ Saf 132:231–239. https://doi.org/10.1016/j.ecoenv.2016.06.010
Wang J, Wang ZK, Chen XX, Wang WX, Huang HQ, Chen YC et al (2023) Transcriptomic analysis of the effect of deferoxamine exposure on the growth, photosynthetic activity and iron transfer of Microcystis aeruginosa. Chemosphere. https://doi.org/10.1016/j.chemosphere.2023.138506
Yeung ACY, D’Agostino PM, Poljak A, McDonald J, Bligh MW, Waite TD et al (2016) Physiological and proteomic responses of continuous cultures of Microcystis aeruginosa PCC 7806 to changes in iron bioavailability and growth rate. Appl Environ Microbiol 82(19):5918–5929. https://doi.org/10.1128/Aem.01207-16
Zhang M, Shi XL, Yu Y, Kong FX (2011) The acclimative changes in photochemistry after colony formation of the cyanobacteria Microcystis aeruginosa. J Phycol 47(3):524–532. https://doi.org/10.1111/j.1529-8817.2011.00987.x
Funding
This work was supported in part by the US Environmental Protection Agency (internal funding).
Author information
Authors and Affiliations
Contributions
AG and EH wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ghio, A.J., Hilborn, E.D. Cyanobacterial blooms, iron, and environmental pollutants. Biometals 37, 577–586 (2024). https://doi.org/10.1007/s10534-023-00553-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-023-00553-2