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Ecofisiología, ciclos de vida anual y cianotoxinas de las cianobacterias planctónicas Anabaena, Aphanizomenon y Microcystis en embalses españoles

  • Autores: Samuel Cirés
  • Directores de la Tesis: Antonio Quesada (dir. tes.)
  • Lectura: En la Universidad Autónoma de Madrid ( España ) en 2012
  • Idioma: español
  • Tribunal Calificador de la Tesis: Francisca Fernández del Campo (presid.), Pilar Mateo Ortega (secret.), Claudia Wiedner (voc.), Vitor Manuel Oliveira Vasconcelos (voc.), Assaf Sukenik (voc.)
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  • Resumen
    • Summer blooms of potentially toxic cyanobacteria, like the Nostocalean Anabaena and Aphanizomenon or the Chroococcalean Microcystis, are frequent phenomena in Spanish freshwater reservoirs which pose a major concern for water management. In the last years, the cyanotoxins anatoxin-a (ATX), cylindrospermopsin (CYN), microcystins (MC) and paralytic shellfish toxins (PSP toxins) have been detected in a number of Spanish reservoirs. While CYN and MC production have been already confirmed in isolates of Aphanizomenon ovalisporum and Microcystis spp., respectively, no ATX or PSP-producer has been isolated in Spain yet. According to field data, Anabaena spp. and Aphanizomenon spp. are good candidates for ANA and PSP production in Spanish freshwaters.

      Predictive (e.g. mathematical modeling) and/or corrective (e.g. water flushing and/or sediment dredging) strategies aiming to prevent or delay blooms require a deep knowledge on the annual life-cycles of cyanobacteria. While summer blooms are well documented in Spain, the rest of the annual life-cycle of Microcystis and Nostocales remains poorly understood. Moreover, most studies on the annual life-cycle of cyanobacteria in Europe focused in lakes whereas reservoirs, which in Spain are more than 1000, have received less attention.

      In the last decade, it has been suggested that climate change has promoted a northwards spreading of certain Nostocales (e.g. the CYN-producer Cylindrospermopsis raciborskii). Recently, the CYN-producer Aphanizomenon ovalisporum has been added to the list of potentially invasive cyanobacteria in Europe. In this context, countries of Mediterranean Europe like Spain, as transition areas between the subtropical/tropical and the temperate regions, become a good opportunity to understand the spreading routes of these potentially invasive cyanobacteria.

      Taking all of this into account, the objectives of the present thesis are: to investigate the phylogeny and cyanotoxin production of potentially toxic Nostocales (Anabaena, Aphanizomenon and Cylindrospermopsis) isolated from Spanish freshwater reservoirs; to gain insight on the ecophysiology of the potentially invasive cyanobacterium Aphanizomenon ovalisporum; to describe the sedimentation dynamics of Microcystis during bloom (summer) and post-bloom (autumn) periods in three Spanish freshwater reservoirs; to investigate the overwintering strategies of Anabaena, Aphanizomenon and Microcystis in six Spanish freshwater reservoirs.

      The results of this thesis are organized in five chapters, whose main conclusions are: 1. The nostocalean genus Aphanizomenon was confirmed as a major producer of the cyanotoxins cylindrospermopsin (cytotoxin) and paralytic shellfish poisoning toxins (neurotoxins) in Spanish freshwaters. A high cylindrospermopsin production was observed in 6 strains of Aphanizomenon ovalisporum from different Spanish waterbodies, characterized by a low inter-strain variation and a remarkable share of extracellular CYN share of 19-40% during exponential growth. PSP-production (saxitoxin, neo-saxitoxin and decarbamoyl-saxitoxin) was confirmed in two Aphanizomenon gracile strains, lying below the quantification limit of our technique.

      2. Cylindrospermopsin production by Anabaena planctonica was confirmed for the first time worldwide in two strains of this species. In spite of the very low cylindrospermopsin production measured (in the range of ng CYN per mg dry weight), the possibility of an increased concentration in the field via scum formation and the cosmopolitan behavior of A. planctonica demand taking this species into account for future risk assessments. 3. The cyanotoxins anatoxin-a (neurotoxin) and microcystins (hepatotoxins) were not detected in any of the 33 Anabaena, Aphanizomenon and Cylindrospermopsis strains analyzed. This possibly reflects the low incidence of anatoxin-a in Spanish freshwaters and the close link of microcystin to the chroccocalean genus Microcystis in the Mediterranean region.

      4. The phylogenetic analyses based on cpcBA-IGS and 16S rRNA-gene sequences demonstrated the high genetic homogeneity of Aphanizomenon ovalisporum and the high similitude of Aphanizomenon gracile strains from Spain with those from other European countries. In contrast, cpcBA-IGS based phylogeny suggested that Cylindrospermopsis raciborskii from Spain might form a group separated from the rest of European strains analyzed so far, a hypothesis that needs further confirmation with more genetic markers. Also, the phylogenetic trees based on cpcBA-IGS and 16S rRNA-gene sequences showed an intermixing of toxin-producing (CYN-producing and PSP-producing) and non-producing Nostocales strains.

      5. The gene sxtA, potentially involved in the biosynthesis of saxitoxin (paralytic shellfish toxin), was detected in two saxitoxin-producing strains and one non-saxitoxin producing strain of Aphanizomenon gracile, as well as, for the first time worldwide, in six non-saxitoxin producing Aphanizomenon ovalisporum strains. This reinforces the idea of a complex history of insertions, deletions and horizontal gene transfers building up the toxin-synthesis clusters in cyanobacteria.

      6. Cylindrospermopsin was produced by Aphanizomenon ovalisporum UAM 290 from Spain over a wide range of temperatures and light irradiances in a laboratory experiment performed under batch and semi-continuous growth-regimes. Light induced 4-fold variations in CYN production, whereas this production varied only 2-fold within the 15-30 °C range and decreased 25-fold at 35 °C. Extracellular CYN represented a conspicuous 20-63% of the total CYN produced, with values above 50% coinciding with extreme temperatures and/or growth rates. These results confirm Aphanizomenon ovalisporum as a strong and stable CYN-producer under field realistic gradients of light and temperature, and thus become a predictive tool for waterbodies potentially affected by this ecologically plastic cyanobacterium.

      7. This is the first study establishing a threshold temperature for akinete differentiation in Aphanizomenon ovalisporum and confirming the filament fragmentation in this species, as revealed by a laboratory study performed in the strain Aphanizomenon ovalisporum UAM 290. The maximum akinete production took place at 20 °C, with 15% of the cells being akinetes unlike the low proportion found for the range of 25-35 °C. Temperatures also correlated negatively with filament width, with filaments being 2-fold wider at 20 ºC than at 35 °C. The process of filament fragmentation was confirmed in Aphanizomenon ovalisporum at temperatures above 25 °C, thus becoming a potential dispersal strategy of this species during summer months.

      8. Microcystis sedimentation occurring in three reservoirs of Central Spain represented a "biomass rain" both during bloom (summer) and post-bloom (autumn) periods, accounting for a 0.1-7.6% of the organic matter settled. The detailed study in Valmayor allowed estimating a high Microcystis settling rate of 0.04 d-1 equivalent to 0.7 m d-1 for the whole watercolumn studied, without a global influence of temperature and/or inorganic matter in the settling rates obtained.

      9. A clear decrease of the microcystin cell quota in settling Microcystis was observed in three reservoirs of Central Spain. Although no specific cause for such trend was determined in the present study, three hypotheses were herein proposed: (i) differential settling of Microcystis chemotypes; (ii) internal consumption of microcystins during descent; and (iii) increase of protein-bound microcystins in senescent settling populations. The novelty of these results and their implications on understanding the regulation of the Microcystis annual life-cycle and/or the physiological role of microcystins demand further studies confirming such trend in other waterbodies and determining its physiological causes.

      10. Anabaena, Aphanizomenon and Microcystis may overwinter both in the benthos and in the pelagial of Spanish freshwater reservoirs, as confirmed by a study in six reservoirs in Northwestern Spain. Large benthic populations in the order of 1000-100000 Anabaena spp. akinetes mL-1 sediment and 100-10000 Microcystis colonies mL-1 sediment were found in the surface sediments of the different reservoirs, representing circa 1% of the organic matter in those sediments. Most of the resting stages accumulated in the deepest points near to the dam. Overwintering pelagic-populations of 10000-10000 cells mL-1 of Anabaena flos-aquae, Aphanizomenon gracile and Microcystis aeruginosa were observed in three of the reservoirs at water temperatures between 7.5 and 9.2 °C.

      11. A low proportion (< 1%) of the sediment pool of akinetes and Microcystis was re-suspended into the hypolimnetic water in winter. However, these apparently small benthic inocula, combined with overwintering pelagic populations, seemed sufficient to build up the summer maxima observed in the reservoirs studied according to the in situ growth rates estimated for these cyanobacteria in previous scientific literature.


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