{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,20]],"date-time":"2026-02-20T07:41:14Z","timestamp":1771573274246,"version":"3.50.1"},"reference-count":55,"publisher":"Microbiology Society","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2011,2,1]]},"abstract":"<jats:p>Many cyanobacteria produce extracellular polymeric substances (EPS) mainly of polysaccharidic nature. These EPS can remain associated to the cell surface as sheaths, capsules and\/or slimes, or be liberated into the surrounding environment as released polysaccharides (RPS). The ability of EPS-producing cyanobacteria to remove heavy metals from aqueous solutions has been widely reported in the literature, focusing mainly on the biotechnological potential. However, the knowledge of the effects of the metals in the cell's survival\/growth is still scarce, particularly when they are simultaneously exposed to more than one metal. This work evaluated the effects of different concentrations of Cu<jats:sup>2+<\/jats:sup>and\/or Pb<jats:sup>2+<\/jats:sup>in the growth\/survival of<jats:italic>Gloeothece<\/jats:italic>sp. PCC 6909 and its sheathless mutant<jats:italic>Gloeothece<\/jats:italic>sp. CCY 9612. The results obtained clearly showed that both phenotypes are more severely affected by Cu<jats:sup>2+<\/jats:sup>than Pb<jats:sup>2+<\/jats:sup>, and that the mutant is more sensitive to the former metal than the wild-type. Evident ultrastructural changes were also observed in the wild-type and mutant cells exposed to high levels (10\u2005mg l<jats:sup>\u22121<\/jats:sup>) of Cu<jats:sup>2+<\/jats:sup>. Moreover, in bi-metal systems, Pb<jats:sup>2+<\/jats:sup>was preferentially removed compared with Cu<jats:sup>2+<\/jats:sup>, being the RPS of the mutant that is the most efficient polysaccharide fraction in metal removal. In these systems, the simultaneous presence of Cu<jats:sup>2+<\/jats:sup>and Pb<jats:sup>2+<\/jats:sup>caused a mutual inhibition in the adsorption of each metal.<\/jats:p>","DOI":"10.1099\/mic.0.041038-0","type":"journal-article","created":{"date-parts":[[2010,10,22]],"date-time":"2010-10-22T04:45:17Z","timestamp":1287722717000},"page":"451-458","source":"Crossref","is-referenced-by-count":124,"title":["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?"],"prefix":"10.1099","volume":"157","author":[{"given":"Sara","family":"Pereira","sequence":"first","affiliation":[{"name":"Faculdade de Ci\u00eancias, Universidade do Porto, Departamento de Biologia, Rua do Campo Alegre, Edif\u00edcio FC4, 4169-007 Porto, Portugal"},{"name":"IBMC \u2013 Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal"}]},{"given":"Ernesto","family":"Micheletti","sequence":"additional","affiliation":[{"name":"Department of Agricultural Biotechnology, University of Florence, Piazzale delle Cascine 24, I-50144, Florence, Italy"}]},{"given":"Andrea","family":"Zille","sequence":"additional","affiliation":[{"name":"IBMC \u2013 Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal"}]},{"given":"Arlete","family":"Santos","sequence":"additional","affiliation":[{"name":"Faculdade de Ci\u00eancias, Universidade do Porto, Departamento de Biologia, Rua do Campo Alegre, Edif\u00edcio FC4, 4169-007 Porto, Portugal"},{"name":"IBMC \u2013 Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal"}]},{"given":"Pedro","family":"Moradas-Ferreira","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biom\u00e9dicas Abel Salazar (ICBAS), Universidade do Porto, Largo Abel Salazar 2, 4099-003 Porto, Portugal"},{"name":"IBMC \u2013 Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal"}]},{"given":"Paula","family":"Tamagnini","sequence":"additional","affiliation":[{"name":"Faculdade de Ci\u00eancias, Universidade do Porto, Departamento de Biologia, Rua do Campo Alegre, Edif\u00edcio FC4, 4169-007 Porto, Portugal"},{"name":"IBMC \u2013 Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre 823, 4150-180 Porto, Portugal"}]},{"given":"Roberto","family":"De Philippis","sequence":"additional","affiliation":[{"name":"Department of Agricultural Biotechnology, University of Florence, Piazzale delle Cascine 24, I-50144, Florence, Italy"}]}],"member":"345","reference":[{"key":"R1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev.mi.38.100184.000245","article-title":"Cyanobacterial cell inclusions","volume":"38","author":"Allen","year":"1984","journal-title":"Annu Rev Microbiol"},{"key":"R2","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1007\/s11802-008-0397-2","article-title":"Bioaccumulation of Pb2+ and its effects on growth, morphology and pigment contents of Spirulina Arthrospira ) platensis","volume":"7","author":"Arunakumara","year":"2008","journal-title":"J Ocean Univ China"},{"key":"R3","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1080\/10408410600822934","article-title":"Cyanobacteria metal interactions: requirements, toxicity, and ecological implications","volume":"32","author":"Baptista","year":"2006","journal-title":"Crit Rev Microbiol"},{"key":"R4","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1111\/j.1399-3054.1995.tb00799.x","article-title":"Copper and photosystem II: a controversial relationship","volume":"94","author":"Baron","year":"1995","journal-title":"Physiol Plant"},{"key":"R5","doi-asserted-by":"crossref","first-page":"e6204","DOI":"10.1371\/journal.pone.0006204","article-title":"In situ determination of the effects of lead and copper on cyanobacterial populations in microcosms","volume":"4","author":"Burnat","year":"2009","journal-title":"PLoS ONE"},{"key":"R6","doi-asserted-by":"crossref","first-page":"1610","DOI":"10.1016\/j.chemosphere.2007.05.043","article-title":"Correlating metal ionic characteristics with biosorption capacity using QSAR model","volume":"69","author":"Can","year":"2007","journal-title":"Chemosphere"},{"key":"R7","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/S0168-6445(03)00050-0","article-title":"Zn, Cu and Co in cyanobacteria: selective control of metal availability","volume":"27","author":"Cavet","year":"2003","journal-title":"FEMS Microbiol Rev"},{"key":"R8","doi-asserted-by":"crossref","first-page":"1162","DOI":"10.1111\/j.1529-8817.2005.00143.x","article-title":"Early toxic effects of zinc on PSII of Synechocystis aquatilis f aquatilis (Cyanophyceae)","volume":"41","author":"Chaloub","year":"2005","journal-title":"J Phycol"},{"key":"R9","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1093\/bfgp\/elm030","article-title":"A proteomic approach to iron and copper homeostasis in cyanobacteria","volume":"6","author":"De la Cerda","year":"2007","journal-title":"Brief Funct Genomic Proteomic"},{"key":"R10","first-page":"89","article-title":"Heavy metal removal with exopolysaccharide-producing cyanobacteria","volume-title":"In Heavy Metals in the Environment","author":"De Philippis","year":"2009"},{"key":"R11","first-page":"13","article-title":"Outermost polysaccharidic investments of cyanobacteria: nature, significance and possible applications","volume":"7","author":"De Philippis","year":"2003","journal-title":"Recent Res Dev Microbiology"},{"key":"R12","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1023\/A:1017590425924","article-title":"Exopolysaccharide-producing cyanobacteria and their possible exploitation: a review","volume":"13","author":"De Philippis","year":"2001","journal-title":"J Appl Phycol"},{"key":"R13","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1007\/s10532-006-9053-y","article-title":"Heavy metal sorption by released polysaccharides and whole cultures of two exopolysaccharide-producing cyanobacteria","volume":"18","author":"De Philippis","year":"2007","journal-title":"Biodegradation"},{"key":"R14","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1021\/ac60111a017","article-title":"Colorimetric method for determination of sugars and related substances","volume":"28","author":"Dubois","year":"1956","journal-title":"Anal Chem"},{"key":"R15","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/BF00140478","article-title":"Cell composition and metal tolerance in cyanobacteria","volume":"7","author":"Fiore","year":"1994","journal-title":"Biometals"},{"key":"R16","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/S0300-483X(03)00159-8","article-title":"Copper toxicity, oxidative stress, and antioxidant nutrients","volume":"189","author":"Gaetke","year":"2003","journal-title":"Toxicology"},{"key":"R17","doi-asserted-by":"crossref","first-page":"1546","DOI":"10.1016\/j.procbio.2007.08.009","article-title":"Effect of the presence of lead on the biosorption of copper, cadmium and nickel by anaerobic biomass","volume":"42","author":"Hawari","year":"2007","journal-title":"Process Biochem"},{"key":"R18","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1007\/s00128-003-8923-9","article-title":"Toxicity of single and combinations of lead and cadmium to the cyanobacteria Anabaena flos-aquae","volume":"72","author":"Heng","year":"2004","journal-title":"Bull Environ Contam Toxicol"},{"key":"R19","first-page":"118","article-title":"Assessment of individual and combined toxicities of four non-essential metals (As. Cd Hg. Pb.) and in the microtox assay","volume-title":"Int J Environ Res Public Health","volume":"3","author":"Ishaque","year":"2006"},{"key":"R20","first-page":"144","article-title":"Electron microscopy of polyphosphate bodies in a blue-green alga, Nostoc pruniforme","volume":"62","author":"Jensen","year":"1968","journal-title":"Arch Microbiol"},{"key":"R21","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1508\/cytologia.42.357","article-title":"Phosphate metabolism in blue-green algae. III. The effect of fixation and post-staining on the morphology of polyphosphate bodies in Plectonema boryanum","volume":"42","author":"Jensen","year":"1977","journal-title":"Cytologia (Tokyo"},{"key":"R22","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/0143-1471(82)90104-0","article-title":"Uptake of heavy metals by Plectonema boryanum (Cyanophyceae) into cellular components, especially polyphosphate bodies: an X-ray energy dispersive study","volume":"27","author":"Jensen","year":"1982","journal-title":"Environ Pollut"},{"key":"R23","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1016\/j.procbio.2008.01.019","article-title":"Metal-salt co-tolerance and metal removal by indigenous cyanobacterial strains","volume":"43","author":"Kiran","year":"2008","journal-title":"Process Biochem"},{"key":"R24","doi-asserted-by":"crossref","first-page":"4567","DOI":"10.1128\/AEM.71.8.4567-4576.2005","article-title":"Analysis of the hupSL operon of the nonheterocystous cyanobacterium Lyngbya majuscula CCAP 1446\/4: regulation of transcription and expression under a light\u2013dark regime","volume":"71","author":"Leita\u0303o","year":"2005","journal-title":"Appl Environ Microbiol"},{"key":"R25","doi-asserted-by":"crossref","first-page":"4677","DOI":"10.1073\/pnas.0900666106","article-title":"A P-type ATPase importer that discriminates between essential and toxic transition metals","volume":"106","author":"Lewinson","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R26","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1080\/02648725.2001.10648020","article-title":"Cyanobacterial exopolysaccharides: their nature and potential biotechnological applications","volume":"18","author":"Li","year":"2001","journal-title":"Biotechnol Genet Eng Rev"},{"key":"R27","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1111\/j.1365-2672.2008.03728.x","article-title":"Selectivity in the heavy metal removal by exopolysaccharide-producing cyanobacteria","volume":"105","author":"Micheletti","year":"2008a","journal-title":"J Appl Microbiol"},{"key":"R28","doi-asserted-by":"crossref","first-page":"2797","DOI":"10.1128\/AEM.02212-07","article-title":"Sheathless mutant of the cyanobacterium Gloeothece sp. strain PCC 6909 with increased capacity to remove copper ions from aqueous solutions","volume":"74","author":"Micheletti","year":"2008b","journal-title":"Appl Environ Microbiol"},{"key":"R29","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/0143-148X(80)90017-8","article-title":"The replacement of the nondescript term \u201cheavy metals\u201d by a biologically and chemically significant classification of metal ions","volume":"1","author":"Nieboer","year":"1980","journal-title":"Environ Pollut Ser"},{"key":"R30","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1007\/s002530051457","article-title":"Microbial heavy-metal resistance","volume":"51","author":"Nies","year":"1999","journal-title":"Appl Microbiol Biotechnol"},{"key":"R31","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/S0168-6445(03)00048-2","article-title":"Eflux-mediated heavy metal resistance in prokaryotes","volume":"27","author":"Nies","year":"2003","journal-title":"FEMS Microbiol Rev"},{"key":"R32","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1023\/A:1008195312218","article-title":"Sorption of metals by extracellular polymers from the cyanobacterium Microcystis aeruginosa f. flos-aquae strain C3\u201340","volume":"12","author":"Parker","year":"2000","journal-title":"J Appl Phycol"},{"key":"R33","doi-asserted-by":"crossref","first-page":"3533","DOI":"10.1021\/ja00905a001","article-title":"Hard and soft acids and bases","volume":"85","author":"Pearson","year":"1963","journal-title":"J Am Chem Soc"},{"key":"R34","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1021\/ed045p581","article-title":"Hard and soft acids and bases, HSAB, part 1: fundamental principles","volume":"45","author":"Pearson","year":"1968","journal-title":"J Chem Educ"},{"key":"R35","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1111\/j.1574-6976.2009.00183.x","article-title":"Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors, and putative genes involved in their biosynthesis and assembly","volume":"33","author":"Pereira","year":"2009","journal-title":"FEMS Microbiol Rev"},{"key":"R36","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s11270-006-9116-z","article-title":"The effect of lead on photosynthesis, as determined by photoacoustics in Synechococcus leopoliensis (Cyanobacteria","volume":"175","author":"Pinchasov","year":"2006","journal-title":"Water Air Soil Pollut"},{"key":"R37","doi-asserted-by":"crossref","first-page":"1008","DOI":"10.1111\/j.0022-3646.2003.02-193.x","article-title":"Heavy metal-induced oxidative stress in algae","volume":"39","author":"Pinto","year":"2003","journal-title":"J Phycol"},{"key":"R38","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/BF01055209","article-title":"Utilization of morphometric analysis in evaluating response of Plectonema boryanum (Cyanophyceae) to exposure to eight heavy metals","volume":"11","author":"Rachlin","year":"1982","journal-title":"Arch Environ Contam Toxicol"},{"key":"R39","doi-asserted-by":"crossref","first-page":"5891","DOI":"10.1128\/JB.181.19.5891-5897.1999","article-title":"Families of soft-metal-ion-transporting ATPases","volume":"181","author":"Rensing","year":"1999","journal-title":"J Bacteriol"},{"key":"R40","first-page":"1","article-title":"Generic assignments, strain histories and properties of pure cultures of cyanobacteria","volume":"111","author":"Rippka","year":"1979","journal-title":"J Gen Microbiol"},{"key":"R41","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1016\/S1095-6433(02)00201-5","article-title":"Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes","volume":"133","author":"Rosen","year":"2002","journal-title":"Comp Biochem Physiol A Mol Integr Physiol"},{"key":"R42","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1007\/s10534-008-9138-7","article-title":"Uptake of Pb2+ by a cyanobacterium belonging to the genus Synechocystis , isolated from East Kolkata Wetlands","volume":"21","author":"Roy","year":"2008","journal-title":"Biometals"},{"key":"R43","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1111\/j.1574-6968.2008.01471.x","article-title":"Immunolocalization of the uptake hydrogenase in the marine cyanobacterium Lyngbya majuscula CCAP 1446\/4 and two Nostoc strains","volume":"292","author":"Seabra","year":"2009","journal-title":"FEMS Microbiol Lett"},{"key":"R44","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1104\/pp.106.079251","article-title":"Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus","volume":"141","author":"Shcolnick","year":"2006","journal-title":"Plant Physiol"},{"key":"R45","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0032-9592(00)00211-9","article-title":"Metal removal from single and multimetallic systems by different biosorbent materials as evaluated by differential pulse anodic stripping voltammetry","volume":"36","author":"Singh","year":"2000","journal-title":"Process Biochem"},{"key":"R46","doi-asserted-by":"crossref","first-page":"3622","DOI":"10.1016\/j.biortech.2006.11.041","article-title":"Copper(II) and lead(II) sorption from aqueous solution by non-living Spirogyra neglecta","volume":"98","author":"Singh","year":"2007","journal-title":"Bioresour Technol"},{"key":"R47","doi-asserted-by":"crossref","first-page":"5047","DOI":"10.1128\/AEM.00271-09","article-title":"Coastal strains of marine Synechococcus species exhibit increased tolerance to copper shock and a distinctive transcriptional response relative to those of open-ocean strains","volume":"75","author":"Stuart","year":"2009","journal-title":"Appl Environ Microbiol"},{"key":"R48","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.4319\/lo.1998.43.6.1055","article-title":"Interactions among Cu2+, Zn2+, and Mn2+ in controlling cellular Mn, Zn, and growth rate in the coastal alga Chlamydomonas","volume":"43","author":"Sunda","year":"1998","journal-title":"Limnol Oceanogr"},{"key":"R49","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1007\/s00244-004-0163-4","article-title":"Effects of heavy-metal stress on cyanobacterium Anabaena flos-aquae","volume":"48","author":"Surosz","year":"2005","journal-title":"Arch Environ Contam Toxicol"},{"key":"R50","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/S0168-6445(02)00114-6","article-title":"Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution","volume":"26","author":"Valls","year":"2002","journal-title":"FEMS Microbiol Rev"},{"key":"R51","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1007\/BF00171964","article-title":"Biosorption of heavy metals by Saccharomyces cerevisiae","volume":"42","author":"Volesky","year":"1995","journal-title":"Appl Microbiol Biotechnol"},{"key":"R52","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1007\/s001289900623","article-title":"Lead uptake and effects on seed germination and plant growth in a Pb hyperaccumulator Brassica pekinensis Rupr","volume":"60","author":"Xiong","year":"1998","journal-title":"Bull Environ Contam Toxicol"},{"key":"R53","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1007\/s10811-008-9341-5","article-title":"Growth characteristics of the cyanobacterium Nostoc flagelliforme in photoautotrophic, mixotrophic and heterotrophic cultivation","volume":"21","author":"Yu","year":"2009","journal-title":"J Appl Phycol"},{"key":"R54","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1007\/s12010-008-8428-4","article-title":"Accumulation of exopolysaccharides in liquid suspension culture of Nostoc flagelliforme cells","volume":"160","author":"Yu","year":"2010","journal-title":"Appl Biochem Biotechnol"},{"key":"R55","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1016\/j.watres.2005.12.011","article-title":"A comparison of the properties of polyurethane immobilised Sphagnum moss, seaweed, sunflower waste and maize for the biosorption of Cu, Pb, Zn and Ni in continuous flow packed columns","volume":"40","author":"Zhang","year":"2006","journal-title":"Water Res"}],"container-title":["Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.041038-0?crawler=true","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,3]],"date-time":"2023-06-03T23:05:18Z","timestamp":1685833518000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.041038-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2011,2,1]]},"references-count":55,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2011,2,1]]}},"URL":"https:\/\/doi.org\/10.1099\/mic.0.041038-0","relation":{},"ISSN":["1350-0872","1465-2080"],"issn-type":[{"value":"1350-0872","type":"print"},{"value":"1465-2080","type":"electronic"}],"subject":[],"published":{"date-parts":[[2011,2,1]]}}}