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Cyanobacteria as bioindicators and bioreporters of environmental analysis in aquatic ecosystems

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Abstract

Knowledge of the incidence of anthropogenic pressure on water ecosystems is one of the main focus of integrated water resource management. The use of biological methods to assess water quality is of particular importance since organisms show an integrating response to their environment. Tolerances or ecological ranges of individual species can differ depending on the taxon, which leads to distinct bioindicator values of cyanobacterial taxa. In addition, a number of morphological and physiological features are known to relate with the environment in which they occur, which makes them excellent environmental indicators. Therefore, we review literature data of the main cyanobacterial methods used to obtain information about changes in running water quality, mainly related to eutrophication processes, which are found as the main cause of disturbance in rivers, with the focus on benthic cyanobacteria, as habitat recommended for monitoring studies. Further, their trophic independence and ease of cultivation make them very useful in the field of bioreporters of environmental monitoring and ecotoxicology. In fact, several cyanobacterial strains have been already genetically engineered to construct bioreporters which respond to different types of pollutants as well as limiting nutrients. The potential of cyanobacteria both as in situ bioindicators as well as bioreporters of environmental analysis in aquatic ecosystems will be discussed.

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Abbreviations

BMWPc:

Biological Monitoring Working Party adapted to Catalonian streams

IBD:

Biological Diatom Index (Indice Biologique Diatomées)

References

  • Aboal M (1988) Aportación al conocimiento de las algas epicontinentales del sudeste de España. III: Cianofíceas (Cyanophyceae Schaffner 1909). Anales Jardín Botánico de Madrid 45:3–46

    Google Scholar 

  • Aboal M, Puig MA, Mateo P, Perona E (2002) Implications of cyanophyte toxicity on biological monitoring of calcareous streams in north-east Spain. J Appl Phycol 14:49–56. doi:10.1023/a:1015298905510

    Google Scholar 

  • Aldehni MF, Forchhammer K (2006) Analysis of a non-canonical NtcA-dependent promoter in Synechococcus elongatus and its regulation by NtcA and P-II. Arch Microbiol 184:378–386. doi:10.1007/s00203-005-0056-6

    CAS  PubMed  Google Scholar 

  • Bachmann T (2003) Transforming cyanobacteria into bioreporters of biological relevance. Trends Biotechnol 21:247–249. doi:10.1016/S0167-7799(03)00114-8

    CAS  PubMed  Google Scholar 

  • Barinova S, Tavassi M (2009) Study of seasonal influences on algal biodiversity in the River Yarqon (central Israel) by bio-indication and canonical correspondence analysis (CCA). Turk J Bot 33:353–372

    Google Scholar 

  • Barinova S, Tavassi M, Nevo E (2006) Algal indicator system of environmental variables in the Hadera River basin, central Israel. Plant Biosyst 140:65–79

    Google Scholar 

  • Barinova S, Medvedeva L, Nevo E (2008) Regional influences on algal biodiversity in two polluted rivers of Eurasia (Rudnaya River, Russia, and Qishon River, Israel) by bioindication and canonical correspondence analysis. Appl Ecol Environ Res 6:29–59

    Google Scholar 

  • Barinova S, Kukhaleishvili L, Nevo E, Janelidze Z (2011) Diversity and ecology of algae in the Algeti National Park as a part of the Georgian system of protected areas. Turk J Bot 35:729–774

    Google Scholar 

  • Barran-Berdon AL, Rodea-Palomares I, Leganes F, Fernandez-Piñas F (2011) Free Ca2+ as an early intracellular biomarker of exposure of cyanobacteria to environmental pollution. Anal Bioanal Chem 400:1015–1029. doi:10.1007/s00216-010-4209-3

    CAS  PubMed  Google Scholar 

  • Belkin S (2003) Microbial whole-cell sensing systems of environmental pollutants. Curr Opin Microbiol 6:206–212

    CAS  PubMed  Google Scholar 

  • Berrendero E, Perona E, Mateo P (2008) Genetic and morphological characterization of Rivularia and Calothrix (Nostocales, Cyanobacteria) from running water. Int J Syst Evol Microbiol 58:447–460. doi:10.1099/ijs.0.65273-0

    CAS  PubMed  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21. doi:10.1038/35036035

    CAS  PubMed  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529. doi:10.1038/nrm1155

    CAS  PubMed  Google Scholar 

  • Bhaya D, Schwarz R, Grossman A (2000) Molecular responses to environmental stress. The ecology of cyanobacteria. Their diversity in time and space. Kluwer, Dordrecht, pp 397–442

    Google Scholar 

  • Bostrom B, Persson G, Broberg B (1988) Bioavailability of different phosphorous forms in fresh-water systems. Hydrobiologia 170:133–155. doi:10.1007/bf00024902

    Google Scholar 

  • Boyanapalli R, Bullerjahn GS, Pohl C, Croot PL, Boyd PW, McKay RML (2007) Luminescent whole-cell cyanobacterial bioreporter for measuring Fe availability in diverse marine environments. Appl Environ Microbiol 73:1019–1024. doi:10.1128/aem.01670-06

    PubMed Central  CAS  PubMed  Google Scholar 

  • Branchini BR, Southworth TL, Khattak NF, Michelini E, Roda A (2005) Red- and green-emitting firefly luciferase mutants for bioluminescent reporter applications. Anal Biochem 345:140–148. doi:10.1016/j.ab.2005.07.015

    CAS  PubMed  Google Scholar 

  • Branco LHZ, Pereira JL (2002) Evaluation of seasonal dynamics and bioindication potential of macroalgal communities in a polluted tropical stream. Arch Hydrobiol 155:147–161

    Google Scholar 

  • Branco LHZ, Necchi Júnior O, Branco CCZ (2001) Ecological distribution of Cyanophyceae in lotic ecosystems of São Paulo State. Braz J Bot 24:99–108

  • Bullerjahn GS, Boyanapalli R, Rozmarynowycz MJ, McKay RML (2010) Cyanobacterial bioreporters as sensors of nutrient availability. In: Belkin S, Gu MB (eds) Whole cell sensing systems II: applications, vol 118. Advances in biochemical engineering-biotechnology. Springer, Berlin, pp 165–188. doi:10.1007/10_2009_23

  • Cai YP, Wolk CP (1997) Nitrogen deprivation of Anabaena sp strain PCC 7120 elicits rapid activation of a gene cluster that is essential for uptake and utilization of nitrate. J Bacteriol 179:258–266

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cantonati M (2008) Cyanoprokaryotes and algae other than diatoms in springs and streams of the Dolomiti Bellunesi National Park (Northern Italy). Arch Hydrobiol Algol Stud 126:113–136

    CAS  Google Scholar 

  • Cantonati M, Rott E, Pipp E (1996) Ecology of cyanophytes in mountain springs of the river Sarca catchment (Adamello-Brenta Regional Park, Trentino, Northern Italy). Arch Hydrobiol Algol Stud 83:145–162

    Google Scholar 

  • Cantonati M, Gerecke R, Bertuzzi E (2006) Springs of the Alps–sensitive ecosystems to environmental change: from biodiversity assessments to long-term studies. Hydrobiologia 562:59–96

    CAS  Google Scholar 

  • Carignan V, Villard MA (2002) Selecting indicator species to monitor ecological integrity: a review. Environ Monit Assess 78:45–61. doi:10.1023/a:1016136723584

    PubMed  Google Scholar 

  • Castenholz RW (2001) Phylum BX Cyanobacteria. Oxygenic photosynthetic bacteria. In: Bergey’s Manual® of Systematic Bacteriology, vol 1, 2nd edn. Springer, New York, pp 473–487

  • Charlton SED, Hickman M (1984) Seasonal physical, chemical and algal changes in 5 rivers flowing through the Oil Sands region of Alberta, Canada. Int Rev Ges Hydrobiol 69:297–332. doi:10.1002/iroh.19840690302

    Google Scholar 

  • Clapham DE (1995) Calcium signaling. Cell 80:259–268. doi:10.1016/0092-8674(95)90408-5

    CAS  PubMed  Google Scholar 

  • Collier JL, Grossman AR (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039–1047

    PubMed Central  CAS  PubMed  Google Scholar 

  • Conley DJ et al (2009) Eutrophication: time to adjust expectations response. Science 324:724–725

    CAS  Google Scholar 

  • Cox E (1991) What is the basis for using diatoms as monitors of river quality. Use of algae for monitoring rivers I. Universität Innsbruck, Innsbruck, Austria, Institut für Botanik, pp 33–40

    Google Scholar 

  • De Pauw N, Vanhooren G (1983) Method for biological quality assessment of watercourses in Belgium. Hydrobiologia 100:153–168

    Google Scholar 

  • Dell’Uomo A (1991) Use of benthic macroalgae for monitoring rivers in Italy. Use of algae for monitoring rivers I. Universität Innsbruck, Institut für Botanik, Innsbruck, pp 129–138

    Google Scholar 

  • Dodds WK (2006) Eutrophication and trophic state in rivers and streams. Limnol Oceanogr 51:671–680

    CAS  Google Scholar 

  • Dodds WK, Welch EB (2000) Establishing nutrient criteria in streams. J N Am Benthol Soc 19:186–196. doi:10.2307/1468291

    Google Scholar 

  • Dolman AM, Rucker J, Pick FR, Fastner J, Rohrlack T, Mischke U, Wiedner C (2012) Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLoS ONE. doi:10.1371/journal.pone.0038757

    PubMed Central  PubMed  Google Scholar 

  • Dominguez DC (2004) Calcium signalling in bacteria. Mol Microbiol 54:291–297. doi:10.1111/j.1365-2958.2004.04276.x

    CAS  PubMed  Google Scholar 

  • Dong YL, Xu XD (2009) Outer membrane proteins induced by iron deficiency in Anabaena sp PCC 7120. Prog Nat Sci 19:1477–1483. doi:10.1016/j.pnsc.2009.02.009

    CAS  Google Scholar 

  • Douterelo I, Perona E, Mateo P (2004) Use of cyanobacteria to assess water quality in running waters. Environ Pollut 127:377–384. doi:10.1016/j.envpol.2003.08.016

    CAS  PubMed  Google Scholar 

  • Durham KA, Porta D, Twiss MR, McKay RML, Bullerjahn GS (2002) Construction and initial characterization of a luminescent Synechococcus sp. PCC 7942 Fe-dependent bioreporter. FEMS Microbiol Lett 209:215–221. doi:10.1111/j.1574-6968.2002.tb11134.x

    CAS  PubMed  Google Scholar 

  • EC (2000) Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy. Off. J. Eur. Communities

  • Erbe JL, Adams AC, Taylor KB, Hall LM (1996) Cyanobacteria carrying an smt-lux transcriptional fusion as biosensors for the detection of heavy metal cations. J Ind Microbiol 17:80–83. doi:10.1007/bf01570047

    CAS  PubMed  Google Scholar 

  • Fernández-Piñas F, Wolk CP (1994) Expression of luxCD-E in Anabaena sp. can replace the use of exogenous aldehyde for in vivo localization of transcription by luxAB. Gene 150:169–174. doi:10.1016/0378-1119(94)90879-6

  • Fernandez-Piñas F, Leganes F, Wolk CP (2000) Bacterial lux genes as reporters in cyanobacteria. Methods Enzymol 305:513–527

    PubMed  Google Scholar 

  • Fetscher AE et al (2014) Development and comparison of stream indices of biotic integrity using diatoms vs. non-diatom algae vs. a combination. J Appl Phycol 26:433–450

    CAS  Google Scholar 

  • Fjerdingstad E (1964) Pollution of streams estimated by benthal phytomicro-organisms I. A saprobic system based on communities of organisms and ecological factors. Int Rev Ges Hydrobiol 49:63–131

    Google Scholar 

  • Fogg G, Stewart W, Fay P, Walsby A (1973) The blue-green algae. Academic Press, London

    Google Scholar 

  • Fromin N et al (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4:634–643. doi:10.1046/j.1462-2920.2002.00358.x

    CAS  PubMed  Google Scholar 

  • Galmozzi CV, Saelices L, Florencio FJ, Muro-Pastor MI (2010) Posttranscriptional regulation of glutamine synthetase in the filamentous Cyanobacterium Anabaena sp PCC 7120: differential expression between vegetative cells and heterocysts. J Bacteriol 192:4701–4711. doi:10.1128/jb.00222-10

    PubMed Central  CAS  PubMed  Google Scholar 

  • García ME, Aboal M (2014) Environmental gradients and macroalgae in Mediterranean marshes: the case of Pego-Oliva marsh (East Iberian Peninsula). Sci Total Environ 475:216–224. doi:10.1016/j.scitotenv.2013.10.014

    PubMed  Google Scholar 

  • Garcia JAL, Grijalbo L, Ramos B, Fernandez-Piñas F, Rodea-Palomares I, Gutierrez-Manero FJ (2013) Combined phytoremediation of metal-working fluids with maize plants inoculated with different microorganisms and toxicity assessment of the phytoremediated waste. Chemosphere 90:2654–2661. doi:10.1016/j.chemosphere.2012.11.042

    Google Scholar 

  • Gillor O, Hadas O, Post AF, Belkin S (2002) Phosphorus bioavailability monitoring by a bioluminescent cyaniobacterial sensor strain. J Phycol 38:107–115. doi:10.1046/j.1529-8817.2002.01069.x

    Google Scholar 

  • Gillor O, Harush A, Hadas O, Post AF, Belkin S (2003) A Synechococcus Pgln: AluxAB fusion for estimation of nitrogen bioavailability to freshwater cyanobacteria. Appl Environ Microbiol 69:1465–1474. doi:10.1128/aem.69.3.1465-1474.2003

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gillor O, Hadas O, Post AF, Belkin S (2010) Phosphorus and nitrogen in a monomictic freshwater lake: employing cyanobacterial bioreporters to gain new insights into nutrient bioavailability. Freshw Biol 55:1182–1190. doi:10.1111/j.1365-2427.2009.02342.x

    CAS  Google Scholar 

  • Goericke R, Welschmeyer NA (1993) The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep Sea Res Part I 40:2283–2294. doi:10.1016/0967-0637(93)90104-b

    Google Scholar 

  • González-Pleiter M et al (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064. doi:10.1016/j.watres.2013.01.020

    PubMed  Google Scholar 

  • Grimm NB, Petrone KC (1997) Nitrogen fixation in a desert stream ecosystem. Biogeochemistry 37:33–61. doi:10.1023/a:1005798410819

    CAS  Google Scholar 

  • Gutowski A, Foerster J (2009) Benthische Algen ohne Diatomeen und Characeen: Bestimmungshilfe. LANUV, Recklinghausen

  • Gutowski A, Foerster J, Schaumburg J (2004) Use of benthic algae excluding diatoms and charales for the assessment of the ecological status of running freshwaters: a case history from Germany. Oceanol Hydrobiol Stud 33:3–15

    CAS  Google Scholar 

  • Hajibabaei M, Shokralla S, Zhou X, Singer GAC, Baird DJ (2011) Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS ONE. doi:10.1371/journal.pone.0017497

    Google Scholar 

  • Hassler CS, Twiss MR, Simon DF, Wilkinson KJ (2008) Porous underwater chamber (PUC) for in situ determination of nutrient and pollutant bioavailability to microorganisms. Limnol Oceanogr 6:277–287

    CAS  Google Scholar 

  • Hassler CS, Havens SM, Bullerjahn GS, McKay RML, Twiss MR (2009) An evaluation of iron bioavailability and speciation in western Lake Superior with the use of combined physical, chemical, and biological assessment. Limnol Oceanogr 54:987–1001. doi:10.4319/lo.2009.54.3.0987

    CAS  Google Scholar 

  • Heim R, Tsien RY (1996) Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6:178–182

    CAS  PubMed  Google Scholar 

  • Heim R, Cubitt AB, Tsien RY (1995) Improved green fluorescence. Nature 373:663–664. doi:10.1038/373663b0

    CAS  PubMed  Google Scholar 

  • Hoppe HG (2003) Phosphatase activity in the sea. Hydrobiologia 493:187–200. doi:10.1023/a:1025453918247

    CAS  Google Scholar 

  • Horne AJ, Carnmiggelt C (1975) Algal nitrogen fixation in California streams: seasonal cycles. Freshw Biol 5:461–470

    Google Scholar 

  • Huckle JW, Morby AP, Turner JS, Robinson NJ (1993) Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace-metal ions. Mol Microbiol 7:177–187. doi:10.1111/j.1365-2958.1993.tb01109.x

    CAS  PubMed  Google Scholar 

  • Hynninen A, Tonismann K, Virta M (2010) Improving the sensitivity of bacterial bioreporters for heavy metals. Bioeng Bugs 1:132–138. doi:10.4161/bbug.1.2.10902

    PubMed Central  PubMed  Google Scholar 

  • Iliopoulou-Georgudaki J, Kantzaris V, Katharios P, Kaspiris P, Georgiadis T, Montesantou B (2003) An application of different bioindicators for assessing water quality: a case study in the rivers Alfeios and Pineios (Peloponnisos, Greece). Ecol Indic 2:345–360

    CAS  Google Scholar 

  • Ivanikova NV, McKay RML, Bullerjahn GS (2005) Construction and characterization of a cyanobacterial bioreporter capable of assessing nitrate assimilatory capacity in freshwaters. Limnol Oceanogr 3:86–93

    CAS  Google Scholar 

  • Ivanikova NV, McKay RML, Bullerjahn GS, Sterner RW (2007) Nitrate utilization by phytoplankton in Lake Superior is impaired by low nutrient (P, Fe) availability and seasonal light limitation—a cyanobacterial bioreporter study. J Phycol 43:475–484. doi:10.1111/j.1529-8817.2007.00348.x

    Google Scholar 

  • Jarvie HP, Sharpley AN, Withers PJA, Scott JT, Haggard BE, Neal C (2013) Phosphorus mitigation to control river eutrophication: murky waters, inconvenient truths, and “postnormal” science. J Environ Qual 42:295–304. doi:10.2134/jeq2012.0085

    CAS  PubMed  Google Scholar 

  • Kann E (1978) Typification of Austrian streams concerning algae. In: Proceedings-International association of theoretical and applied limnology

  • Kann E (1982) Qualitative Veränderungen der litoralen Algenbiocönose österreichischer Seen. Arch Hydrobiol Suppl 62:440–490

  • Kelly M (2013) Data rich, information poor? Phytobenthos assessment and the Water Framework Directive. Eur J Phycol 48:437–450. doi:10.1080/09670262.2013.852694

    Google Scholar 

  • Kelly MG, Whitton BA (1998) Biological monitoring of eutrophication in rivers. Hydrobiologia 384:55–67. doi:10.1023/a:1003400910730

    Google Scholar 

  • Kelly M et al (1998) Recommendations for the routine sampling of diatoms for water quality assessments in Europe. J Appl Phycol 10:215–224

    Google Scholar 

  • Kolkwitz R, Marsson M (1908) Ökologie der pflanzlichen Saprobien. Ber Deutschen Botanischen Gesellschaft 26A:505–519

    Google Scholar 

  • Komárek J (1994) Current trends and species delimitation in the cyanoprokaryote taxonomy. Arch Hydrobiol Algol Stud 75:11–29

    Google Scholar 

  • Komárek J (2013) Cyanoprocaryota 3. Teil: Heterocytous Genera In: Sußwasserflora Von mitteleuropa 19/3. Gustav Fischer, Berlin, p 1130

  • Komárek J, Anagnostidis K (1999) Cyanoprocaryota 1. Teil: Chroococcales. In: Sußwasserflora Von mitteleuropa 19/1. Gustav Fischer, Jena-Stuttgart-Lübeck-Ulm, Germany, p 548

  • Komárek J, Anagnostidis K (2005) Cyanoprocaryota 2. Teil: Oscillatoriales. In: Sußwasserflora Von mitteleuropa 19/2. Elsevier Spektrum, Heidelberg, p 759

  • Kozlova O, Zwinderman M, Christofi N (2005) A new short-term toxicity assay using Aspergillus awamori with recombinant aequorin gene. BMC Microbiol. doi:10.1186/1471-2180-5-40

    PubMed Central  PubMed  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563. doi:10.1105/tpc.109.072686

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kunert A, Hagemann M, Erdmann N (2000) Construction of promoter probe vectors for Synechocystis sp PCC 6803 using the light-emitting reporter systems Gfp and LuxAB. J Microbiol Methods 41:185–194. doi:10.1016/s0167-7012(00)00162-7

    CAS  PubMed  Google Scholar 

  • Leganes F, Forchhammer K, Fernandez-Piñas F (2009) Role of calcium in acclimation of the cyanobacterium Synechococcus elongatus PCC 7942 to nitrogen starvation. Microbiology 155:25–34. doi:10.1099/mic.0.022251-0

    CAS  PubMed  Google Scholar 

  • Lewis WM, Wurtsbaugh WA, Paerl HW (2011) Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environ Sci Technol 45:10300–10305. doi:10.1021/es202401p

    CAS  PubMed  Google Scholar 

  • Liebmann H (1962) Handbuch der Frischwasser und Abwasser-biologie, vol I. München, Germany

    Google Scholar 

  • Lindstrøm E (1999) Attempts to assess biodiversity of epilithic algae in running water in Norway. In: Use of algae for monitoring European Rivers IV. Agence de l´Eau Artois-Picardie, France, pp 253–260

  • Lindstrøm EA, Traaen TS (1984) Influence of current velocity on periphyton distribution and succession in a Norwegian soft water river. Verhandlung Internationale Vereinigung Limnologie 22:1965–1972

    Google Scholar 

  • Lindstrøm EA, Johansen SW, Saloranta T (2004) Periphyton in running waters—long-term studies of natural variation. Hydrobiologia 521:63–86. doi:10.1023/B:HYDR.0000026351.68927.ee

  • Liu HB, Nolla HA, Campbell L (1997) Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat Microb Ecol 12:39–47. doi:10.3354/ame012039

    Google Scholar 

  • Loza V, Berrendero E, Perona E, Mateo P (2013a) Polyphasic characterization of benthic cyanobacterial diversity from biofilms of the Guadarrama River (Spain): morphological, molecular, and ecological approaches. J Phycol 49:282–297. doi:10.1111/jpy.12036

    Google Scholar 

  • Loza V, Perona E, Carmona J, Mateo P (2013b) Phenotypic and genotypic characteristics of Phormidium-like cyanobacteria inhabiting microbial mats are correlated with the trophic status of running waters. Eur J Phycol 48:235–252. doi:10.1080/09670262.2013.799715

    Google Scholar 

  • Loza V, Perona E, Mateo P (2013c) Molecular fingerprinting of cyanobacteria from river biofilms as a water quality monitoring tool. Appl Environ Microbiol 79:1459–1472. doi:10.1128/aem.03351-12

    PubMed Central  CAS  PubMed  Google Scholar 

  • Loza V, Perona E, Mateo P (2014) Specific responses to nitrogen and phosphorus enrichment in cyanobacteria: factors influencing changes in species dominance along eutrophic gradients. Water Res 48:622–631. doi:10.1016/j.watres.2013.10.014

    CAS  PubMed  Google Scholar 

  • Malik S, Beer M, Megharaj M, Naidu R (2008) The use of molecular techniques to characterize the microbial communities in contaminated soil and water. Environ Int 34:265–276. doi:10.1016/j.envint.2007.09.001

    CAS  PubMed  Google Scholar 

  • Mateo P, Douterelo I, Berrendero E, Perona E (2006) Physiological differences between two species of cyanobacteria in relation to phosphorus limitation. J Phycol 42:61–66. doi:10.1111/j.1529-8817.2006.00180.x

    CAS  Google Scholar 

  • Mateo P, Berrendero E, Perona E, Loza V, Whitton BA (2010) Phosphatase activities of cyanobacteria as indicators of nutrient status in a Pyrenees river. Hydrobiologia 652:255–268. doi:10.1007/s10750-010-0338-0

    CAS  Google Scholar 

  • Mbeunkui F, Richaud C, Etienne AL, Schmid RD, Bachmann TT (2002) Bioavailable nitrate detection in water by an immobilized luminescent cyanobacterial reporter strain. Appl Microbiol Biotechnol 60:306–312. doi:10.1007/s00253-002-1139-9

    CAS  PubMed  Google Scholar 

  • McKay RML et al (2005) Bioavailable iron in oligotrophic Lake Superior assessed using biological reporters. J Plankton Res 27:1033–1044. doi:10.1093/plankt/fbi070

    CAS  Google Scholar 

  • Meighen EA (1991) Molecular biology of bacterial bioluminescence. Microbiol Rev 55:123–142

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mischke U, Venohr M, Behrendt H (2011) Using phytoplankton to assess the trophic status of German Rivers. Int Rev Hydrobiol 96:578–598. doi:10.1002/iroh.201111304

    CAS  Google Scholar 

  • Mollenhauer D, Bengtsson R, Lindstrøm EA (1999) Macroscopic cyanobacteria of the genus Nostoc: a neglected and endangered constituent of European inland aquatic biodiversity. Eur J Phycol 34:349–360. doi:10.1017/s0967026299002358

  • Morby AP, Turner JS, Huckle JW, Robinson NJ (1993) SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA: identification of a Zn inhibited DNA–protein complex. Nucleic Acids Res 21:921–925. doi:10.1093/nar/21.4.921

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mulholland PJ, Rosemond AD (1992) Periphyton response to longitudinal nutrient depletion in a woodland stream: evidence of upstream downstream linkage. J N Am Benthol Soc 11:405–419. doi:10.2307/1467561

  • Muñoz-Martín MA, Mateo P, Leganes F, Fernandez-Piñas F (2011) Novel cyanobacterial bioreporters of phosphorus bioavailability based on alkaline phosphatase and phosphate transporter genes of Anabaena sp PCC 7120. Anal Bioanal Chem 400:3573–3584. doi:10.1007/s00216-011-5017-0

    PubMed  Google Scholar 

  • Muñoz-Martín MA, Martínez-Rosell A, Perona E, Fernandez-Piñas F, Mateo P (2014a) Monitoring bioavailable phosphorus in lotic systems: a polyphasic approach based on cyanobacteria. Sci Total Environ 475:158–168. doi:10.1016/j.scitotenv.2013.06.076

    PubMed  Google Scholar 

  • Muñoz-Martín MA, Mateo P, Leganes F, Fernandez-Piñas F (2014b) A battery of bioreporters of nitrogen bioavailability in aquatic ecosystems based on cyanobacteria. Sci Total Environ 475:169–179. doi:10.1016/j.scitotenv.2013.07.015

    PubMed  Google Scholar 

  • Nakajima Y, Ohmiya Y (2010) Bioluminescence assays: multicolor luciferase assay, secreted luciferase assay and imaging luciferase assay. Expert Opin Drug Discov 5:835–849. doi:10.1517/17460441.2010.506213

    CAS  PubMed  Google Scholar 

  • Neal C, Jarvie HP, Withers PJA, Whitton BA, Neal M (2010) The strategic significance of wastewater sources to pollutant phosphorus levels in English rivers and to environmental management for rural, agricultural and urban catchments. Sci Total Environ 408:1485–1500. doi:10.1016/j.scitotenv.2009.12.020

    CAS  PubMed  Google Scholar 

  • Norris RH, Thoms MC (1999) What is river health? Freshw Biol 41:197–209. doi:10.1046/j.1365-2427.1999.00425.x

    Google Scholar 

  • Ogunbayo OA, Lai PF, Connolly TJ, Michelangeli F (2008) Tetrabromobisphenol A (TBBPA), induces cell death in TM4 Sertoli cells by modulating Ca(2+) transport proteins and causing dysregulation of Ca(2+) homeostasis. Toxicol In Vitro 22:943–952. doi:10.1016/j.tiv.2008.01.015

    CAS  PubMed  Google Scholar 

  • Ohta M, Suzuki T (2007) Participation of the inositol phospholipid signaling pathway in the increase in cytosolic calcium induced by tributyltin chloride intoxication of chlorophyllous protozoa Euglena gracilis Z and its achlorophyllous mutant SM-ZK. Comp Biochem Physiol C 146:525–530. doi:10.1016/j.cbpc.2007.06.005

    Google Scholar 

  • Osman D, Cavet JS (2010) Bacterial metal-sensing proteins exemplified by ArsR-SmtB family repressors. Nat Prod Rep 27:668–680. doi:10.1039/b906682a

    CAS  PubMed  Google Scholar 

  • Paerl HW, Xu H, McCarthy MJ, Zhu G, Qin B, Li Y, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45:1973–1983. doi:10.1016/j.watres.2010.09.018

    CAS  PubMed  Google Scholar 

  • Palmer CM (1969) A composite rating of algae tolerating organic pollution. J Phycol 5:78–82. doi:10.1111/j.1529-8817.1969.tb02581.x

    Google Scholar 

  • Peca L, Kos PB, Mate Z, Farsang A, Vass I (2008) Construction of bioluminescent cyanobacterial reporter strains for detection of nickel, cobalt and zinc. FEMS Microbiol Lett 289:258–264. doi:10.1111/j.1574-6968.2008.01393.x

    CAS  PubMed  Google Scholar 

  • Perona E, Mateo P (2006) Benthic cyanobacterial assemblages as indicators of nutrient enrichment regimes in a Spanish river. Acta Hydrochim Hydrobiol 34:67–72. doi:10.1002/aheh.200500611

    CAS  Google Scholar 

  • Perona E, Bonilla I, Mateo P (1998) Epilithic cyanobacterial communities and water quality: an alternative tool for monitoring eutrophication in the Alberche River (Spain). J Appl Phycol 10:183–191. doi:10.1023/a:1008051327689

    Google Scholar 

  • Perona E, Aboal M, Bonilla I, Mateo P (2003) Cyanobacterial diversity in a Spanish river determined by means of isolation of cultures. Morphological variability of isolates in relation to natural populations. Arch Hydrobiol Algol Stud 109:475–486

    Google Scholar 

  • Persoone G, De Pauw N (1979) Systems of biological indicators for water quality assessment. In: Ravera O (ed) Biological aspects of freshwater pollution. Pergamon Press, Oxford, pp 39–75

  • Porta D, Bullerjahn GS, Durham KA, Wilhelm SW, Twiss MR, McKay RML (2003) Physiological characterization of a Synechococcus sp (Cyanophyceae) strain PCC 7942 iron-dependent bioreporter for freshwater environments. J Phycol 39:64–73. doi:10.1046/j.1529-8817.2003.02068.x

    CAS  Google Scholar 

  • Porta D, Bullerjahn GS, Twiss MR, Wilhelm SW, Poorvin L, McKay RML (2005) Determination of bioavailable Fe in Lake Erie using a luminescent cyanobacterial bioreporter. J Great Lakes Res 31:180–194

    CAS  Google Scholar 

  • Porter SD, Mueller DK, Spahr NE, Munn MD, Dubrovsky NM (2008) Efficacy of algal metrics for assessing nutrient and organic enrichment in flowing waters. Freshw Biol 53:1036–1054. doi:10.1111/j.1365-2427.2007.01951.x

    Google Scholar 

  • Richaud C, Zabulon G, Joder A, Thomas JC (2001) Nitrogen or sulfur starvation differentially affects phycobilisome degradation and expression of the nblA gene in Synechocystis strain PCC 6803. J Bacteriol 183:2989–2994. doi:10.1128/jb.183.10.2989-2994.2001

    PubMed Central  CAS  PubMed  Google Scholar 

  • Roda A, Guardigli M (2012) Analytical chemiluminescence and bioluminescence: latest achievements and new horizons. Anal Bioanal Chem 402:69–76. doi:10.1007/s00216-011-5455-8

    CAS  PubMed  Google Scholar 

  • Rodea-Palomares I, González-García C, Leganes F, Fernéndez-Piñas F (2009) Effect of pH, EDTA, and anions on heavy metal toxicity toward a bioluminescent cyanobacterial bioreporter. Arch Environ Cont Toxicol 57:477–487. doi:10.1007/s00244-008-9280-9

    CAS  Google Scholar 

  • Rodea-Palomares I, Petre AL, Boltes K, Leganes F, Perdigon-Melon JA, Rosal R, Fernandez-Piñas F (2010) Application of the combination index (CI)-isobologram equation to study the toxicological interactions of lipid regulators in two aquatic bioluminescent organisms. Water Res 44:427–438. doi:10.1016/j.watres.2009.07.026

    CAS  PubMed  Google Scholar 

  • Rodea-Palomares I, Boltes K, Fernandez-Piñas F, Leganes F, García-Calvo E, Santiago J, Rosal R (2011) Physicochemical characterization and ecotoxicological assessment of CeO2 nanoparticles using two aquatic microorganisms. Toxicol Sci 119:135–145. doi:10.1093/toxsci/kfq311

    CAS  PubMed  Google Scholar 

  • Rodea-Palomares I, Leganes F, Rosal R, Fernandez-Piñas F (2012) Toxicological interactions of perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) with selected pollutants. J Hazard Mater 201:209–218. doi:10.1016/j.jhazmat.2011.11.061

    PubMed  Google Scholar 

  • Rodriguez V, Aguirre de Cárcer D, Loza V, Perona E, Mateo P (2007) A molecular fingerprint technique to detect pollution-related changes in river cyanobacterial diversity. J Environ Qual 36:464–468. doi:10.2134/jeq2006.0190SC

    CAS  PubMed  Google Scholar 

  • Rosal R, Rodea-Palomares I, Boltes K, Fernandez-Piñas F, Leganes F, Gonzalo S, Petre A (2010a) Ecotoxicity assessment of lipid regulators in water and biologically treated wastewater using three aquatic organisms. Environ Sci Pollut Res 17:135–144. doi:10.1007/s11356-009-0137-1

    CAS  Google Scholar 

  • Rosal R, Rodea-Palomares I, Boltes K, Fernandez-Piñas F, Leganes F, Petre A (2010b) Ecotoxicological assessment of surfactants in the aquatic environment: combined toxicity of docusate sodium with chlorinated pollutants. Chemosphere 81:288–293. doi:10.1016/j.chemosphere.2010.05.050

    CAS  PubMed  Google Scholar 

  • Rott E, Pfister P (1988) Natural epilithic algal communities in fast-flowing mountain streams and rivers and some man-induced changes. Internationale Vereinigung fuer Theoretische und Angewandte Limnologie Verhandlungen IVTLAP 23

  • Rott E, Schneider S (2014) A comparison of ecological optima of soft-bodied benthic algae in Norwegian and Austrian rivers and consequences for river monitoring in Europe. Sci Total Environ 475:180–186

    CAS  PubMed  Google Scholar 

  • Rott E, Hofmann G, Pall K, Pfister P, Pipp E (1997) Indikationslisten für Aufwuchsalgen in Österreichischen Fliessgewässern. Teil 1: Saprobielle Indikation Wasserwirtschaftskataster, Bundeministerium f. Land- u. Forstwirtschaft, Wien

  • Rott E, Pipp E, Pfister P, Van Dam H, Ortler K, Binder N, Pall K (1999) Indikationslisten für Aufwuchsalgen in österreichischen Fliessgewässern. Teil 2: Trophieindikation (sowie geochemische Präferenzen, taxonomische und toxikologische Anmerkungen). Wasserwirtschaftskataster, Bundesministerium f. Land- u. Forstwirtschaft, Wien

  • Rott E, Walser L, Kegele M (2000) Ecophysiological aspects of macroalgal seasonality in a gravel stream in the Alps (River Isar, Austria). Verhandlungen der Internationalen Vereinigung für Limnologie 27:1622–1625

    CAS  Google Scholar 

  • Rott E, Cantonati M, Füreder L, Pfister P (2006) Benthic algae in high altitude streams of the Alps—a neglected component of the aquatic biota. Hydrobiologia 562:195–216

    Google Scholar 

  • Round FE (1991) Diatoms in river water—monitoring studies. J Appl Phycol 3:129–145. doi:10.1007/bf00003695

    Google Scholar 

  • Sabater S (1983) Distribución espacio-temporal de las poblaciones de algas del arroyo de l’Avencó (Barcelona). In: I Congreso Español de Limnología, Barcelona, Spain, pp 159–166

  • Sabater S (1989) Encrusting algal assemblages in a mediterranean river basin. Arch Hydrobiol 114:555–573

    Google Scholar 

  • Sabater S, Armengol J, Comas E, Sabater F, Urrizalqui I, Urrutia I (2000) Algal biomass in a disturbed Atlantic river: water quality relationships and environmental implications. Sci Total Environ 263:185–195. doi:10.1016/s0048-9697(00)00702-6

    CAS  PubMed  Google Scholar 

  • Sabater S, Vilalta E, Gaudes A, Guasch H, Muñoz I, Romaní A (2003) Ecological implications of mass growth of benthic cyanobacteria in rivers. Aquat Microb Ecol 32:175–184. doi:10.3354/ame032175

  • Schaumburg J, Schranz C, Foerster J, Gutowski A, Hofmann G, Meilinger P, Schneider S, Schmedtje U (2004) Ecological classification of macrophytes and phytobenthos for rivers in Germany according to the Water Framework Directive. Limnologica 34:283–301. doi:10.1016/s0075-9511(04)80002-1

  • Schneider SC, Lindstrøm E-A (2011) The periphyton index of trophic status PIT: a new eutrophication metric based on non-diatomaceous benthic algae in Nordic rivers. Hydrobiologia 665:143–155

    CAS  Google Scholar 

  • Schreiter PPY, Gillor O, Post A, Belkin S, Schmid RD, Bachmann TT (2001) Monitoring of phosphorus bioavailability in water by an immobilized luminescent cyanobacterial reporter strain. Biosens Bioelectron 16:811–818. doi:10.1016/s0956-5663(01)00224-x

    CAS  PubMed  Google Scholar 

  • Schultz GE Jr, Kovatch JJ, Anneken EM (2013) Bacterial diversity in a large, temperate, heavily modified river, as determined by pyrosequencing. Aquat Microb Ecol 70:169–179. doi:10.3354/ame01646

    Google Scholar 

  • Serrano A, Mateo P, Perona E (2004) Estructura y composición de la comunidad de cianobacterias bentónicas de un arroyo de montaña mediterráneo, el arroyo Mediano (Madrid). Limnetica 23:83–94

  • Shao CY, Howe CJ, Porter AJR, Glover LA (2002) Novel cyanobacterial biosensor for detection of herbicides. Appl Environ Microbiol 68:5026–5033. doi:10.1128/aem.68.10.5026-5033.2002

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shih PM et al (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 110:1053–1058. doi:10.1073/pnas.1217107110

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shokralla S, Spall JL, Gibson JF, Hajibabaei M (2012) Next-generation sequencing technologies for environmental DNA research. Mol Ecol 21:1794–1805. doi:10.1111/j.1365-294X.2012.05538.x

    CAS  PubMed  Google Scholar 

  • Sierra MV, Gómez N (2007) Structural characteristics and oxygen consumption of the epipelic biofilm in three lowland streams exposed to different land uses. Water Air Soil Pollut 186:115–127. doi:10.1007/s11270-007-9469-y

    CAS  Google Scholar 

  • Sládecek V (1973) System of water quality from the biological point of view. Ergeb Limnol (Germany, FR) 7:1-18

  • Soltani N, Khodaei K, Alnajar N, Shahsavari A, Ashja Ardalan A (2012) Cyanobacterial community patterns as water quality Bioindicators. Iran J Fish Sci 11:876–891

    Google Scholar 

  • Sorensen SJ, Burmolle M, Hansen LH (2006) Making bio-sense of toxicity: new developments in whole-cell biosensors. Curr Opin Biotechnol 17:11–16. doi:10.1016/j.copbio.2005.12.007

    CAS  PubMed  Google Scholar 

  • Stancheva R, Fetscher AE, Sheath RG (2012) A novel quantification method for stream-inhabiting, non-diatom benthic algae, and its application in bioassessment. Hydrobiologia 684:225–239

    CAS  Google Scholar 

  • Stancheva R, Sheath RG, Read BA, McArthur KD, Schroepfer C, Kociolek JP, Fetscher AE (2013) Nitrogen-fixing cyanobacteria (free-living and diatom endosymbionts): their use in southern California stream bioassessment. Hydrobiologia 720:111–127. doi:10.1007/s10750-013-1630-6

    CAS  Google Scholar 

  • Stevenson RJ, Smol JP (2003) Use of algae in environmental assessments. Academic Press, San Diego

    Google Scholar 

  • Stevenson R, Pan Y, van Dam H (2010) Assessing environmental conditions in rivers and streams with diatoms. The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge, pp 57–85

    Google Scholar 

  • Su ZC, Olman V, Xu Y (2007) Computational prediction of Pho regulons in cyanobacteria. BMC Genom. doi:10.1186/1471-2164-8-156

    Google Scholar 

  • Torrecilla I, Leganes F, Bonilla I, Fernandez-Piñas F (2000) Use of recombinant aequorin to study calcium homeostasis and monitor calcium transients in response to heat and cold shock in cyanobacterial. Plant Physiol 123:161–175. doi:10.1104/pp.123.1.161

    PubMed Central  CAS  PubMed  Google Scholar 

  • Torrecilla I, Leganes F, Bonilla I, Fernandez-Piñas F (2004a) A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp PCC7120. Microbiology 150:3731–3739. doi:10.1099/mic.0.27403-0

    CAS  PubMed  Google Scholar 

  • Torrecilla I, Leganes F, Bonilla I, Fernandez-Piñas F (2004b) Light-to-dark transitions trigger a transient increase in intracellular Ca2+ modulated by the redox state of the photosynthetic electron transport chain in the cyanobacterium Anabaena sp PCC7120. Plant Cell Environ 27:810–819. doi:10.1111/j.1365-3040.2004.01187.x

    CAS  Google Scholar 

  • Tseng IC, Wang SYC (1982) The taxonomy and ecology of genus Oscillatoria in Tainan area. Biol Bull NTNU 17:25–38

  • Turner BL, Baxter R, Whitton BA (2003) Nitrogen and phosphorus in soil solutions and drainage streams in Upper Teesdale, northern England: implications of organic compounds for biological nutrient limitation. Sci Total Environ 314:153–170. doi:10.1016/s0048-9697(03)00101-3

  • Tytgat B et al (2014) Bacterial diversity assessment in Antarctic terrestrial and aquatic microbial mats: a comparison between bidirectional pyrosequencing and cultivation. PLoS ONE 9:e97564. doi:10.1371/journal.pone.0097564

  • USEPA (2000) Nutrient Criteria. Technical guidance manual. Rivers and streams. EPA-822-B-00-002. United States Environmental Protection Agency, Washington, DC

  • Van Bogelen RA, Olson ER, Wanner BL, Neidhardt FC (1996) Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli. J Bacteriol 178:4344–4366

    Google Scholar 

  • Van der Meer JR, Belkin S (2010) Where microbiology meets microengineering: design and applications of reporter bacteria. Nat Rev Microbiol 8:511–522. doi:10.1038/nrmicro2392

    PubMed  Google Scholar 

  • Walley WJ, Grbović J, Džeroski S (2001) A reappraisal of saprobic values and indicator weights based on Slovenian river quality data. Water Res 35:4285–4292

    CAS  PubMed  Google Scholar 

  • Wang SS, Chen L, Xia SK (2007) Cadmium is acutely toxic for murine hepatocytes: effects on intracellular free Ca2+ homeostasis. Physiol Res 56:193–201

    CAS  PubMed  Google Scholar 

  • Whalley HJ, Knight MR (2013) Calcium signatures are decoded by plants to give specific gene responses. New Phytol 197:690–693. doi:10.1111/nph.12087

    CAS  PubMed  Google Scholar 

  • Whitton B (1987) The biology of Rivulariaceae. The Cyanobacteria. Elsevier, Amsterdam, pp 513–534

    Google Scholar 

  • Whitton BA (1999) Perspective on the use of phototrophs to monitor nutrients in running waters. Aquat Conserv 9:545–549. doi:10.1002/(sici)1099-0755(199911/12)9:6<545:aid-aqc385>3.0.co;2-9

    Google Scholar 

  • Whitton BA (2002) Phylum Cyanophyta (Cyanobacteria). The freshwater algal flora of the British Isles. Cambridge University Press, Cambridge, pp 25–122

    Google Scholar 

  • Whitton BA (2008) Cyanobacterial diversity in relation to the environment. In: Evangelista V, Barsanti L, Frassanito AM, Passarelli V, Gualtieri P (eds) Algal toxins: nature, occurrence, effect and detection. NATO Science for peace and security series A—chemistry and biology. Springer, Dordrecht, pp 17–43. doi:10.1007/978-1-4020-8480-5_2

  • Whitton BA (2012) Changing approaches to monitoring during the period of the ‘Use of algae for monitoring rivers’ symposia. Hydrobiologia 695:7–16. doi:10.1007/s10750-012-1121-1

    CAS  Google Scholar 

  • Whitton BA (2013) Use of benthic algae and bryophytes for monitoring rivers. J Ecol Environ 36:95–100. doi:10.5141/ecoenv.2013.012

    Google Scholar 

  • Whitton BA, Mateo P (2012) Rivulariaceae. In: Whitton B (ed) Ecology of Cyanobacteria II. Their diversity in space and time. Springer, London, pp 561–591

    Google Scholar 

  • Whitton BA, Neal C (2011) Organic phosphate in UK rivers and its relevance to algal and bryophyte surveys. Ann Limnol 47:3–10. doi:10.1051/limn/2010102

    Google Scholar 

  • Whitton BA, Potts M (2000) Introduction to the cyanobacteria. In: Ecology of cyanobacteria: their diversity in time and space. Kluwer, Dordrecht, pp 1–10

  • Whitton BA, Potts M (2012) Introduction to the cyanobacteria. In: Ecology of cyanobacteria II. Springer, Dordrecht, pp 1–13

  • Whitton BA, Yelloly JM, Christmas M, Hernandez I (1998) Surface phosphatase activity of benthic algae in a stream with highly variable ambient phosphate concentrations. In: Williams WD, Sladeckova A (eds) International association of theoretical and applied limnology—proceedings, vol 26, Pt 3. E Schweizerbart’sche, Stuttgart, pp 967–972

  • Zha SH, Xu XD, Hu HH (2012) A high sensitivity iron-dependent bioreporter used to measure iron bioavailability in freshwaters. FEMS Microbiol Lett 334:135–142. doi:10.1111/j.1574-6968.2012.02629.x

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was funded by MINECO grants CTM2013-45775-C2-2-R and CGL2013-44870-R.

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  1. Departamento de Biología, Universidad Autónoma de Madrid, Cantoblanco, 28049, Madrid, Spain

    Pilar Mateo, Francisco Leganés, Elvira Perona, Virginia Loza & Francisca Fernández-Piñas

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  1. Pilar Mateo
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  2. Francisco Leganés
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  3. Elvira Perona
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Correspondence to Francisca Fernández-Piñas.

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Communicated by Anurag chaurasia.

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Mateo, P., Leganés, F., Perona, E. et al. Cyanobacteria as bioindicators and bioreporters of environmental analysis in aquatic ecosystems. Biodivers Conserv 24, 909–948 (2015). https://doi.org/10.1007/s10531-015-0903-y

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