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Physiological and thylakoid ultrastructural changes in cyanobacteria in response to toxic manganese concentrations

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Abstract

In this study, two cyanobacterial strains (morphologically identified as Microcystis novacekii BA005 and Nostoc paludosum BA033) were exposed to different Mn concentrations: 7.0, 10.5, 15.7, 23.6 and 35.4 mg L−1 for BA005; and 15.0, 22.5, 33.7, 50.6, and 76.0 mg L−1 for BA033. Manganese toxicity was assessed by growth rate inhibition (EC50), chlorophyll a content, quantification of Mn accumulation in biomass and monitoring morphological and ultrastructural effects. The Mn EC50 values were 16 mg L−1 for BA005 and 39 mg L−1 for BA033, respectively. Reduction of chlorophyll a contents and ultrastructural changes were observed in cells exposed to Mn concentrations greater than 23.6 and 33.7 mg L−1 for BA005 and BA033. Damage to intrathylakoid spaces, increased amounts of polyphosphate granules and an increased number of carboxysomes were observed in both strains. In the context of the potential application of these strains in bioremediation approaches, BA005 was able to remove Mn almost completely from aqueous medium after 96 h exposure to an initial concentration of 10.5 mg L−1, and BA033 was capable of removing 38% when exposed to initial Mn concentration of 22.5 mg L−1. Our data shed light on how these cyanobacterial strains respond to Mn stress, as well as supporting their utility as organisms for monitoring Mn toxicity in industrial wastes and potential bioremediation application.

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References

  • Allen MM, Stanier RY (1968) Growth and division of some unicellular blue-green algae. J Gen Microbiol 51:199–202

    Article  CAS  Google Scholar 

  • Andrade L, Keim CN, Farina M, Pfeiffer WC (2004) Zinc detoxification by a cyanobacterium from a metal contaminated bay in Brazil. Braz Arch Biol Technol 47:147–52

    Article  CAS  Google Scholar 

  • Arunakumara KKIU, Xuecheng Z (2009) Effects of heavy metals (Pb2+ and Cd2+) on the ultrastructure, growth and pigment contents of the unicellular cyanobacterium Synechocystis sp. PCC 6803*. Chin J Oceano Limn 27:383–8

    Article  CAS  Google Scholar 

  • Baulina OI (2012) Ultrastructural plasticity of cyanobacteria. Springer-Verlag, Berlin Heidelberg, London

    Book  Google Scholar 

  • Baxter M, Jensen T (1980) Uptake of magnesium, strontium, barium, and manganese by Plectonema boryanum (Cyanophyceae) with special reference to polyphosphate bodies. Protoplasma 104:81–9

    Article  CAS  Google Scholar 

  • Bender J, Gould JP, Vatcharapijarn Y, Young JS, Phillips P (1994) Removal of zinc and manganese from contaminated water with cyanobacteria mats. Water Environ Res 66:679–83

    Article  CAS  Google Scholar 

  • Bonaventura C, Johnson FM (1997) Healthy environments for healthy people: bioremediation today and tomorrow. Environ Health Persp 105:5–20

    CAS  Google Scholar 

  • Bouchard M, Laforest F, Vandelac L, Bellinger D, Mergler D (2007) Hair manganese and hyperactive behaviors: pilot study of school-age children exposed through tap water. Environ Health Persp 115:122–7

    Article  CAS  Google Scholar 

  • Brandenburg F, Schoffman H, Kurz S, Krämer U, Keren N, Weber AP, Eisenhut M (2017) The Synechocystis manganese exporter Mnx is essential for manganese homeostasis in cyanobacteria. Plant physiol 173:1798–810

    Article  CAS  Google Scholar 

  • BRAZIL, Resolução CONAMA no. 357 (2005). Classificação de águas, doces, salobras e salinas do Território Nacional. Diário Oficial da União, 18 de março de 2005, seção 1, p. 58.

  • Campos MMC, Faria VHF, Teodoro TS, Barbosa FA, Magalhães SM (2013) Evaluation of the capacity of the cyanobacterium Microcystis novacekii to remove atrazine from a culture medium. J Environ Sci Heal B 48:101–7

    Article  CAS  Google Scholar 

  • Carrasco-Gil S, Rios JJ, Álvarez-Fernández A, Abadía A, García-Mina JM, Abadía J (2015) Effects of individual and combined metal foliar fertilisers on iron- and manganese-deficient Solanum lycopersicum plants. Plant Soil 402:27–45

    Article  CAS  Google Scholar 

  • Chojnacka K, Noworyta A (2004) Evaluation of Spirulina sp. growth in photoautotrophic, heterotrophic and mixotrophic cultures. Enzym Micro Tech 34:461–5

    Article  CAS  Google Scholar 

  • CICAD (2004) Manganese and its compounds: environmental aspects. Concise international chemical assessment document 63. WHO, Geneva, Switzerland, http://www.who.int/ipcs/publications/cicad/cicad63_rev_1.pdf, Accessed 19 Sept 2018

  • Csatorday K, Gombos Z, Szalontai B (1984) Mn2+ and Co2+ toxicity in chlorophyll biosynthesis. P Natl Acad Sci 81:476–8

    Article  CAS  Google Scholar 

  • Dohnalkova A, Bilskis C, Kennedy D (2006) TEM study of manganese biosorption by Cyanobacterium Synechocystis 6803. Microsc Micro 12:444–5

    Article  Google Scholar 

  • Duan N, Fan W, Changbo Z, Chunlei Z, Hongbing Y (2010) Analysis of pollution materials generated from electrolytic manganese industries in China. Resour Conserv Recy 54:506–11

    Article  Google Scholar 

  • El-Sheekh MM, El-Shouny WA, Osman MEH, El-Gammal EWE (2005) Growth and heavy metals removal efficiency of Nostoc muscorum and Anabaena subcylindrica in sewage and industrial wastewater effluents. Environ Toxicol Phar 19:357–65

    Article  CAS  Google Scholar 

  • Farag AM, Woodward DF, Goldstein JN, Brumbaugh W, Meyer JS (1998) Concentrations of metals associated with mining waste in sediments, biofilm, benthic macroinvertebrates, and fish from the Coeur d’Alene river basin, Idaho. Arch Environ Con Tox 34:119–27

    Article  CAS  Google Scholar 

  • Fiore MF, Moon DH, Tsai SM, Lee H, Trevors JT (2000) Miniprep DNA isolation from unicellular and filamentous cyanobacteria. J Microbiol Meth 39:159–69

    Article  CAS  Google Scholar 

  • Fischer WW, Hemp J, Johnson JE (2015) Manganese and the evolution of photosynthesis. Orig Life Evol B 45:351–7

    Article  CAS  Google Scholar 

  • Frisbie SH, Mitchell EJ, Dustin H, Maynard DM, Sarkar B (2012) World health organization discontinues its drinking-water guideline for manganese. Environ Health Perspect 120:775–8

    Article  CAS  Google Scholar 

  • Franco MW, Ferreira FAG, Vasconcelos IF, Batista BL, Pujoni DGF, Magalhães SMS, Barbosa Jr F, Barbosa FAR (2015) Arsenic biotransformation by cyanobacteria from mining areas: evidences from culture experiments. Environ Sci Pollut R 22:18607–15

    Article  CAS  Google Scholar 

  • Genuário DB, Lorenzi AS, Agujaro LF, Isaac RL, Azevedo MTP, Neto RC, Fiore MF (2016) Cyanobacterial community and microcystin production in a recreational reservoir with constant Microcystis blooms. Hydrobiologia 779:105–25

    Article  CAS  Google Scholar 

  • Genuário DB, Vaz MGMV, Hentschke GS, Sant’Anna CL, Fiore MF (2015) Halotia gen. nov., a phylogenetically and physiologically coherent cyanobacterial genus isolated from marine coastal environments. Int J Syst Evol Micr 65:663–75

    Article  CAS  Google Scholar 

  • Genuário DB, Corrêa DM, Komárek J, Fiore MF (2013) Characterization of freshwater benthic biofilm-forming Hydrocoryne (Cyanobacteria) isolates from Antarctica. J Phycol 49:1142–53

    Article  CAS  Google Scholar 

  • Gorelova OA, Baulina OI (2009) Ultrastructure of cyanobacterium Nostoc sp. f. Blasia cell forms in persisting populations. Microbiology 78:609–17

    Article  CAS  Google Scholar 

  • Gorham PR, Mclachlan J, Hammer U, Kim WK (1964) Isolation and culture of toxic strains of Anabaena flos-aquae (Lyng) de Breb. Int Ver für Theor und Angew Limnol: Verh 15:796–804

    Google Scholar 

  • Groschen GE, Arnold TL, Morrow WS, Warner KL (2008) Occurrence and distribution of iron, manganese, and selected trace elements in ground water in the glacial aquifer system of the Northern United States. Sci Investig Rep 2009–5006:89

    Google Scholar 

  • Hardie LP, Balkwill DL, Stevens SE (1983) Effects of iron starvation on the ultrastructure of the cyanobacterium Agmenellum quadruplicatum. Appl Environ Microbiol 45:1007–17

    CAS  Google Scholar 

  • Hazarika J, Pakshirajan K, Sinharoy A, Syiem MB (2014) Bioremoval of Cu(II), Zn(II), Pb(II) and Cd(II) by Nostoc muscorum isolated from a coal mining site. J Appl Phycol 27:1525–34

    Article  CAS  Google Scholar 

  • Hrouzek P, Lukešová A, Mareš J, Ventura S (2013) Description of the cyanobacterial genus Desmonostoc gen. nov. including D. muscorum comb. nov. as a distinct, phylogenetically coherent taxon related to the genus Nostoc. Fottea 13:201–13

    Article  Google Scholar 

  • Hudek L, Rai S, Michalczyk A, Rai LC, Neilan BA, Ackland ML (2012) Physiological metal uptake by Nostoc punctiforme. Biometals 25:893–903

    Article  CAS  Google Scholar 

  • IGAM (2017) Instituto Mineiro de Gestão das águas. Encarte especial sobre a qualidade das águas do rio Doce após 2 anos do rompimento de barragem de Fundão 2015–2017, Belo Horizonte, Brazil, http://www3.ana.gov.br/portal/ANA/sala-de-situacao/rio-doce/documentos-relacionados/encarte-qualidade-da-gua-do-rio-doce-dois-anos-apos-rompimento-de-barragem-de-fundao-1.pdf, Accessed 19 Sept 2018

  • Jensen TE, Baxter M, Rachlin JW, Jani V (1982) Uptake of heavy metals by plectonema into cellular components, especially polyphosphate bodies: an x-ray energy dispersive study. Environ Pollut A 27:119–27

    Article  CAS  Google Scholar 

  • Ji L, Xie S, Feng J, Li Y, Chen L (2012) Heavy metal uptake capacities by the common freshwater green alga Cladophora fracta. J Appl Phycol 24:979–83

    Article  CAS  Google Scholar 

  • Keren N, Kidd MJ, Penner-Hahn JE, Pakrasi HB (2002) A light-dependent mechanism for massive accumulation of manganese in the photosynthetic bacterium Synechocystis sp. PCC 6803. Biochem-US 41:15085–92

    Article  CAS  Google Scholar 

  • Komárek J, Anagnostidis K (1989) Modern approach to the classification system of cyanophytes 4 –Nostocales. Algological Studies. 56:247–345

    Google Scholar 

  • Komárek J, Anagnostidis K (1998) Cyanoprokaryota 1. Teil: Chroococcales. Gustav Fischer Verlang Jena, Jena

    Google Scholar 

  • Komárek J, Anagnostidis K (2013) Cyanoprokaryota 3. Teil/ 3nd Part: Heterocytous Genera. Springer Spektrum, Berlim

    Google Scholar 

  • Komárek J, Kaštovský J, Mareš J, Johansen JR (2014) Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86:295–335

    Google Scholar 

  • Komárek J (2016) Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia 764:259–70

    Article  Google Scholar 

  • Kumar D, Rai J, Gaur JP (2012) Removal of metal ions by Phormidium bigranulatum (Cyanobacteria)-dominated mat in batch and continuous flow systems. Bioresour Technol 104:202–7

    Article  CAS  Google Scholar 

  • Kupriyanova EV, Sinetova MA, Cho SM, Park YI, Los DA, Pronina NA (2013) CO2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role, and evolutionary origin. Photosynth Res 117:133–46

    Article  CAS  Google Scholar 

  • Lindon FC, Barreiro MG, Ramalho JC (2004) Manganese accumulation in rice: implications for photosynthetic functioning. J Plant Physiol 161:1235–44

    Article  CAS  Google Scholar 

  • Lizieri C, Kuki KN, Aguiar R (2012) The morphophysiological responses of free-floating aquatic macrophytes to a supra-optimal supply of manganese. Water Air Soil Poll 223:2807–20

    Article  CAS  Google Scholar 

  • Mateo P, Perona E, Berrendero E, Leganés F, Martín M, Golubic S (2011) Life cycle as a stable trait in the evaluation of diversity of Nostoc from biofilms in rivers. FEMS Microbiol Ecol 76:185–98

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London, p 889

    Google Scholar 

  • Meeks JC, Castenholz RW (1971) Growth and photosyntehsis in na extreme thermophile Synechococus lividus–I. Effect of temperature on fluorescence and enhancemente of CO2 assimilation. J Therm Biol 3:11–8

    Article  Google Scholar 

  • Mohamed ZA (2001) Removal of cadmium and manganese by a non-toxic strain of the freshwater cyanobacterium Gloeothece magna. Water Res 35:4405–9

    Article  CAS  Google Scholar 

  • Neilan BA, Jacobs D, Del DT, Blackall LL, Hawkins PR, Cox PT, Goodman AE (1997) rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int J Syst Evol Micr 47:693–7

    CAS  Google Scholar 

  • OECD-The Organisation for Economic Co-operation and Development (2011) Test No. 201: Freshwater alga and cyanobacteria, growth inhibition test, OECD Guidelines for the Testing of Chemicals. OECD Publishing, Paris

    Google Scholar 

  • Pandey S, Rai R, Rai LC (2012) Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J Proteom 75:921–37

    Article  CAS  Google Scholar 

  • Papaefthimiou D, Hrouzek P, Mugnai MA, Lukesova A, Turicchia S, Rasmussen U, Ventura S (2008) Differential patterns of evolution and distribution of the symbiotic behaviour in Nostocacean cyanobacteria. Int J Syst Evol Micr 58:553–64

    Article  CAS  Google Scholar 

  • Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10

    Article  CAS  Google Scholar 

  • Pereira S, Micheletti E, Zille A, Santos A, Moradas-Ferreira P, Tamagnini P, Philippis R (2011) Using extracellular polymeric substances (EPS)-producing cyanobacteria for the bioremediation of heavy metals: do cations compete for the EPS functional groups and also accumulate inside the cell? Microbiology 157:451–58

    Article  CAS  Google Scholar 

  • Pinsino A, Matranga V, Roccheri MC (2012) Manganese: a new emerging contaminant in the environment. In: Srivastava J (ed) Environmental contamination. In Tech Open Access Publisher, Rijeka, Croatia, pp. 17–36.

  • Pokrovsky OS, Martinez RE, Golubev SV, Kompantseva EI, Shirokova LS (2008) Adsorption of metals and protons on Gloeocapsa sp. cyanobacteria: A surface speciation approach. Appl Geochem 23:2574–88

    Article  CAS  Google Scholar 

  • Rachlin JW, Jensen TE, Warkentine BE (1985) Morphometric analysis of the response of Anabaena flos-aquae and Anabaena variabilis (Cyanophyceae) to selected concentrations of zinc. Arch Environ Con Tox 402:395–402

    Article  Google Scholar 

  • Rangsayatorn N, Upatham ES, Kruatrachue M, Pokethitiyooka P, Lanzac GR (2002) Phytoremediation potential of Spirulina (Arthrospira) platensis: Biosorption and toxicity studies of cadmium. Environ Pollut 119:45–53

    Article  CAS  Google Scholar 

  • Reichman SM (2002) The responses of plants to metal toxicity: a review focusing on copper, manganese and zinc. Australian Minerals and Energy Environment Foundation, Melbourne, Australia, p 54

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate stain at high pH in electron microscopy. J Cell Biol 17:208–12

    Article  CAS  Google Scholar 

  • Roy S (1997) Genetic diversity of manganese deposition in the terrestrial geological record. Geol Soc Spec Publ 119:5–27

    Article  CAS  Google Scholar 

  • Siqueira MEPB (1985) Aspectos toxicológicos da exposição ao manganês. Rev Bras Saude Ocup 13:28–36

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultra Mol Struct R 26:31–43

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–9

    Article  CAS  Google Scholar 

  • Taton A, Grubisic S, Brambilla E, Wit RD, Wilmotte A (2003) Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl Environ Micro 69:5157–69

    Article  CAS  Google Scholar 

  • Teixeira IR, Borém A, Andrade MJB, Giúdice MPD, Cecon PR (2004) Chlorophyll levels in common bean plants as influence by manganese and zinc fertilization. Acta Sci Agron 26:147–52

    Article  CAS  Google Scholar 

  • Truus K, Viitak A, Vaher M, Muinasmaa U, Paasrand K, Tuvikene R, Levandi T (2007) Comparative determination of microelements in Baltic seawater and brown algae samples by atomic absorption spectrometric and inductively coupled plasma methods. Proc Estonian Acad Sci Chem 56:122–33

    CAS  Google Scholar 

  • Vaz MGMV, Genuário DB, Andreote APD, Malone CFS, Sant’Anna CL, Barbiero L, Fiore MF (2015) Pantanalinema gen. nov. and Alkalinema gen. nov.: novel Pseudanabaenacean genera (Cyanobacteria) isolated from saline–alkaline lakes. Int J Syst Evol Micr 65:298–308

    Article  CAS  Google Scholar 

  • Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73:1163–72

    Article  CAS  Google Scholar 

  • Yee N, Benning LG, Phoenix VR, Ferris FG (2004) Characterization of metal-cyanobacteria sorption reactions: a combined macroscopic and infrared spectroscopic investigation. Envir Sci Tech Lib 38:775–82

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship granted to KAFM, and the National Institute for Research and Technology on Mineral Resources, Water and Biodiversity—INCT-Acqua—for financial support. We acknowledge the Center of Microscopy of UFMG (http://www.microscopia.ufmg.br) for the TEM images and the Laboratory of Chemical Analysis of the Departamento de Engenharia Metalúrgica e de Materiais of the Engineering School/UFMG for the quantitative analysis of Mn. Funding from the Max Planck Society, the National Council for Scientific and Technological Development (CNPq-Brazil) and the Foundation for Research Assistance of the Minas Gerais State, Brazil (FAPEMIG, Grants APQ-01106-13 and APQ-01357-14) to WLA, and scholarships and a research fellowship granted by CAPES/FAPEMIG (BPD-00514-14) and CAPES (PNPD-1638006) to MGMVV are gratefully acknowledged. PC is supported by NERC core funding to the British Antarctic Survey’s ‘Biodiversity, Evolution and Adaptation’ Team.

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Authors and Affiliations

  1. Laboratório de Limnologia, Ecotoxicologia e Ecologia Aquática, Instituto de Ciências Biológicas, B. I3, 163, Universidade Federal de Minas Gerais, Avenida Antonio Carlos, 6627, Belo Horizonte, Minas Gerais, 31270-901, Brazil

    Karen Ann Ferreira Moura, Claudineia Lizieri, Maione Wittig Franco & Francisco Antônio Rodrigues Barbosa

  2. Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil

    Marcelo Gomes Marçal Vieira Vaz & Wagner L. Araújo

  3. Max Planck Partner Group at the Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil

    Marcelo Gomes Marçal Vieira Vaz & Wagner L. Araújo

  4. British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge, CB3 0ET, UK

    Peter Convey

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  1. Karen Ann Ferreira Moura
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Moura, K.A.F., Lizieri, C., Wittig Franco, M. et al. Physiological and thylakoid ultrastructural changes in cyanobacteria in response to toxic manganese concentrations. Ecotoxicology 28, 1009–1021 (2019). https://doi.org/10.1007/s10646-019-02098-y

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