OpenLB
Open Library of Bioscience
Advanced Search
Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine
Jun, 2024;37 (3): 577-586.

Cyanobacterial blooms, iron, and environmental pollutants.

Andrew J Ghio, Elizabeth D Hilborn
Author Information
  1. Andrew J Ghio: US Environmental Protection Agency, Chapel Hill, NC, USA. ghio.andy@epa.gov.
  2. Elizabeth D Hilborn: US Environmental Protection Agency, Chapel Hill, NC, USA.
PMID: 37910342 DOI: 10.1007/s10534-023-00553-2

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.

Keywords

Aqueous environments and iron Environmental pollution Harmful algal blooms Iron Polysaccharides Siderophores Toxins

References

  1. Abbaspour N, Hurrell R, Kelishadi R (2014) Review on iorn and its importance for human health. J Res Med Sci 19:164���174 [PMID: 24778671]
  2. 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 [DOI: 10.1006/bbrc.1999.0741]
  3. 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 [DOI: 10.1111/j.1462-2920.2010.02412.x]
  4. Arstol E, Hohmann-Marriott MF (2019) Cyanobacterial siderophores-physiology, structure, biosynthesis, and applications. Mar Drugs. https://doi.org/10.3390/md17050281 [DOI: 10.3390/md17050281]
  5. 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 [DOI: 10.1073/pnas.1018163108]
  6. 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 [DOI: 10.3390/md20080007]
  7. 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 [DOI: 10.3390/microorganisms8121980]
  8. 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 [DOI: 10.1038/35037500]
  9. 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 [DOI: 10.1046/j.0028-646x.2001.00244.x]
  10. 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 [DOI: 10.1002/iroh.200410783]
  11. 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 [DOI: 10.1021/acs.est.6b05939]
  12. 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 [DOI: 10.1029/2003gb002160]
  13. 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 [DOI: 10.4161/psb.5.1.10197]
  14. Cornwall W (2023) Iron stress threatens southern ocean phytoplankton. Science 379(6634):741���742. https://doi.org/10.1126/science.adh2763 [DOI: 10.1126/science.adh2763]
  15. 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 [DOI: 10.1016/j.scitotenv.2022.154562]
  16. 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 [DOI: 10.1128/AEM.64.3.1130-1132.1998]
  17. 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 [DOI: 10.1111/gbi.12515]
  18. 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 [DOI: 10.1371/journal.pone.0058845]
  19. 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 [DOI: 10.1016/j.envpol.2019.01.071]
  20. Galaris D, Barbouti A, Pantopoulos K (2019) Iron homeosatsis and oxidative stress: an intimate relationship. BBA���Mol Cell Res 1866:118
  21. 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 [DOI: 10.1016/j.jinorgbio.2015.03.008]
  22. 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 [DOI: 10.1016/j.freeradbiomed.2020.02.007]
  23. 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 [DOI: 10.1016/j.ygeno.2007.05.003]
  24. 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 [DOI: 10.3389/fmicb.2012.00069]
  25. 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 [DOI: 10.1016/bs.ampbs.2016.02.005]
  26. Gonz��lez 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 [DOI: 10.5772/intechopen.76720]
  27. 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 [DOI: 10.1016/j.jes.2015.04.004]
  28. 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 [DOI: 10.1073/pnas.1010963108]
  29. 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 [DOI: 10.1016/s0742-8413(00)00121-3]
  30. 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 [DOI: 10.1016/0967-0637(93)90057-A]
  31. Hunter KA, Boyd PW (2007) Iron-binding ligands and their role in the ocean biogeochemistry of iron. Environ Chem 4(4):221���232 [DOI: 10.1071/EN07012]
  32. 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 [DOI: 10.1016/j.toxicon.2006.11.017]
  33. 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 [DOI: 10.1016/S0045-6535(01)00034-0]
  34. 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 [DOI: 10.1021/es400464e]
  35. 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 [PMID: 8439949]
  36. 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 [DOI: 10.1038/s41579-019-0284-4]
  37. 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 [DOI: 10.1897/08-207.1]
  38. 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 [DOI: 10.1038/s41396-020-0594-6]
  39. 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 [DOI: 10.1002/iroh.200911149]
  40. 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 [DOI: 10.1111/jpy.12372]
  41. Lis H, Shaked Y, Kranzler C, Keren N, Morel FMM (2015) Iron bioavailability to phytoplankton: an empirical approach. ISME J 9(4):1003���1013 [DOI: 10.1038/ismej.2014.199]
  42. Lyck S, Gj��lme 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 [DOI: 10.2216/i0031-8884-35-6S-120.1]
  43. 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 [DOI: 10.1016/j.cca.2004.10.007]
  44. Manis J, Kim G (1979) Stimulation of iron absorption by polychlorinated aromatic hydrocarbons. Am J Physiol 236(6):E763-768 [PMID: 443429]
  45. Martin JH, Gordon RM, Fitzwater SE (1991) The case for iron. Limnol Oceanogr 36(8):1793���1802 [DOI: 10.4319/lo.1991.36.8.1793]
  46. 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 [DOI: 10.1016/s0304-3835(99)00203-7]
  47. Morel FMM, Kustka AB, Shaked Y (2008) The role of unchelated Fe in the iron nutrition of phytoplankton. Limnol Oceanogr 53(1):400���404 [DOI: 10.4319/lo.2008.53.1.0400]
  48. 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 [DOI: 10.1007/s12010-012-9926-y]
  49. 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 [DOI: 10.1890/15-1928]
  50. 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 [DOI: 10.1100/tsw.2001.16]
  51. 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 [DOI: 10.1007/s12013-009-9043-x]
  52. 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 [DOI: 10.1128/AEM.01512-18]
  53. 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 [PMID: 17585693]
  54. ��ezanka T, Palyzov�� 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 [DOI: 10.1007/s12223-018-0626-z]
  55. 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 [DOI: 10.1126/science.abl5237]
  56. 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 [DOI: 10.1007/s12035-023-03436-2]
  57. 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 [DOI: 10.1007/s11356-015-4294-0]
  58. Sakaki T, Yamamoto K, Ikushiro S (2013) Possibility of application of cytochrome P450 to bioremediation of dioxins. Biotechnol Appl Biochem 60(1):65���70 [DOI: 10.1002/bab.1067]
  59. 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 [DOI: 10.1016/j.bbamcr.2011.02.003]
  60. 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 [DOI: 10.4137/EHI.S36225]
  61. Schr��der 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 [DOI: 10.1016/S0168-6445(03)00043-3]
  62. Shaked Y, Lis H (2012) Disassembling iron availability to phytoplankton. Front Microbiol 3:123. https://doi.org/10.3389/fmicb.2012.00123 [DOI: 10.3389/fmicb.2012.00123]
  63. Sunda WG, Huntsman SA (1997) Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390(6658):389���392 [DOI: 10.1038/37093]
  64. Sutak R, Camadro JM, Lesuisse E (2020) Iron uptake mechanisms in marine phytoplankton. Front Microbiol. https://doi.org/10.3389/fmicb.2020.566691 [DOI: 10.3389/fmicb.2020.566691]
  65. 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 [DOI: 10.2166/wst.2011.649]
  66. 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
  67. 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
  68. 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 [DOI: 10.1128/Iai.00659-16]
  69. 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 [DOI: 10.1128/aem.61.2.797-800.1995]
  70. 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
  71. 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 [DOI: 10.1146/annurev.marine.010908.163712]
  72. 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 [DOI: 10.1002/jbt.2570030206]
  73. 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 [DOI: 10.1165/rcmb.2004-0275OC]
  74. 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 [DOI: 10.1016/j.ecoenv.2016.06.010]
  75. 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 [DOI: 10.1016/j.chemosphere.2023.138506]
  76. 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 [DOI: 10.1128/Aem.01207-16]
  77. 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 [DOI: 10.1111/j.1529-8817.2011.00987.x]

Grants

  1. EPA999999/Intramural EPA
  2. Internal funds/U.S. Environmental Protection Agency

MeSH Term

Cyanobacteria
Iron
Environmental Pollutants
Eutrophication
Journal Article Review
Article has an altmetric score of 2

Word Cloud

Created with Highcharts 10.0.0ironcanenvironmentsmetalcyanobacteriaIronmicrobialaquaticacquisitionaqueousavailabilitywatersdeficiencycommunitiespathwaysdiverseenvironmentalpollutantsresultcompetitiveadvantagebloomsdeterminesabundancediversitylifecontrolsprimaryproductionnumerouspastdecadesnaturaldecreasedapplyselectivepressureorganismindividualrequirementsdespiteaccesscommonpoolCyanobacteriaphotosynthesizingbacteriumaccumulateformso-called'algalblooms'evolvedstrategiesthriveiron-deficientoutcompeteorganismsMetabolicemployedallowcompetesuccessfullyessentialnutrientcompetingeffectivelyrequisitedisplacespeciesgrowdominatepopulationbloomAquaticresourcesdamagednumberdecreasefunctionalavailablePollutantsalsoincreasedemandpollutant-exposedmicrobecompelledacquirecriticalsurvivalEvenpollutant-impactedenjoycyanobacterialdominanceproposedistinctmanymicrobespollutediron-poorCyanobacterialAqueousEnvironmentalpollutionHarmfulalgalPolysaccharidesSiderophoresToxins

Similar Articles

Cited By