Dynamics of toxic genotypes of Microcystis aeruginosa complex (MAC) through a wide freshwater to marine environmental gradient

Escalera, Gabriela Martínez de la; Kruk, Carla; Segura, Ángel M.; Nogueira, Lucía; Alcántara, Ignacio; Piccini, Claudia

doi:10.1016/j.hal.2016.11.012

Cited by 49 publications

(33 citation statements)

References 65 publications

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“…; Martínez de la Escalera et al . ). Nevertheless, the possible emergence of resistance of M. aeruginosa to salinity, based on selection of new genetic variants arising by spontaneous mutations, has not been previously addressed.…”

Section: Introductionmentioning

confidence: 97%

“…However, several strains of M. aeruginosa can tolerate salinities ≤10 g NaCl L −1 , up to 14 g NaCl L −1 (Preece et al 2017). It must be highlighted that previous studies on the effect of increased salinity on M. aeruginosa assessed the physiological or biochemical responses of cells after only a few generations under the experimental conditions (Otsuka et al 1999;Orr et al 2004;Verspagen et al 2006;Tonk et al 2007;Martínez de la Escalera et al 2017). Nevertheless, the possible emergence of resistance of M. aeruginosa to salinity, based on selection of new genetic variants arising by spontaneous mutations, has not been previously addressed.…”

Section: Introductionmentioning

confidence: 99%

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Adaptation of the toxic freshwater cyanobacterium Microcystis aeruginosa to salinity is achieved by the selection of spontaneous mutants

Melero‐Jiménez

Martín‐Clemente

García‐Sánchez

et al. 2019

Phycological Research

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SUMMARY The cyanobacterium Microcystis aeruginosa causes most of the harmful toxic blooms in freshwater ecosystems. Some strains of M. aeruginosa tolerate low‐medium levels of salinity, and because salinization of freshwater aquatic systems is increasing worldwide it is relevant to know what adaptive mechanisms allow tolerance to salinity. The mechanisms involved in the adaptation of M. aeruginosa to salinity (acclimation vs. genetic adaptation) were tested by a fluctuation analysis design, and then the maximum capacity of adaptation to salinity was studied by a ratchet protocol experiment. Whereas a dose of 10 g NaCl L−1 completely inhibited the growth of M. aeruginosa, salinity‐resistant genetic variants, capable of tolerating up to 14 g NaCl L−1, were isolated in the fluctuation analysis experiment. The salinity‐resistant cells arose by spontaneous mutations at a rate of 7.3 × 10−7 mutants per cell division. We observed with the ratchet protocol that three independent culture populations of M. aeruginosa were able to adapt to up to 15.1 g L−1 of NaCl, suggesting that successive mutation‐selection processes can enhance the highest salinity level to which M. aeruginosa cells can initially adapt. We propose that increasing salinity in water reservoirs could lead to the selection of salinity‐resistant mutants of M. aeruginosa.

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Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Adaptation of the toxic freshwater cyanobacterium Microcystis aeruginosa to salinity is achieved by the selection of spontaneous mutants

Melero‐Jiménez

Martín‐Clemente

García‐Sánchez

et al. 2019

Phycological Research

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“…The system presents strong temporal and spatial gradients in terms of temperature, conductivity (which was used as a proxy of salinity) and turbidity (Acha et al, 2008;Ferrari et al, 2011;García-Rodríguez et al, 2013;Kruk et al, 2015;Martínez de la Escalera et al, 2017). The highest surface water temperatures in Salto Grande reservoir are usually recorded during summer (January to March, 19-33 °C) while the lowest temperatures belong to the outer marine zone of the Río de la Plata during winter-early spring (June to October, 11-18 °C) Martínez de la Escalera et al, 2017). Conductivity was minimum in freshwater systems (0.023 mS cm -1 , Salto, Fray Bentos, Carmelo and Colonia) and maximum at the estuary (55 mS cm -1 , Montevideo and Punta del Este) Martínez de la Escalera et al, 2017).…”

Section: Study Sitementioning

confidence: 99%

“…The highest surface water temperatures in Salto Grande reservoir are usually recorded during summer (January to March, 19-33 °C) while the lowest temperatures belong to the outer marine zone of the Río de la Plata during winter-early spring (June to October, 11-18 °C) Martínez de la Escalera et al, 2017). Conductivity was minimum in freshwater systems (0.023 mS cm -1 , Salto, Fray Bentos, Carmelo and Colonia) and maximum at the estuary (55 mS cm -1 , Montevideo and Punta del Este) Martínez de la Escalera et al, 2017). Turbidity ranged from 0 to 187 NTU, with higher values at the middle of the gradient (Stns.…”

Section: Study Sitementioning

confidence: 99%

“…Microcystis is one of the most common bloom-forming cyanobacterial genus worldwide, capable of successful growth in a variety of freshwater and brackish ecosystems (De Leon and Yunes, 2001;González-Piana et al, 2017, 2011O'Neil et al, 2012;Srivastava et al, 2013). It harbours a number of species defined according to their morphology and ecology that are aggregated in the Microcystis aeruginosa Complex (MAC), whose diversity and bloom formation capacity varied along environmental gradients from headwaters to marine waters Martínez de la Escalera et al, 2017;Sabart et al, 2009;Segura et al, 2017;Tanabe et al, 2018). Most of MAC organisms are able to produce microcystin, a toxin known to cause of serious liver diseases in humans (Azevedo et al, 2002;Dittmann and Wiegand, 2006;Milutinović et al, 2003;Vidal et al, 2017) with more than 250 variants (Meriluoto et al, 2017;Puddick et al, 2014), which are produced via non-ribosomal peptide synthesis (NRPS) and polyketide synthase (PKS) (Dittmann et al, 1997;Tillett et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

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Genotyping and functional regression trees reveals environmental preferences of toxic cyanobacteria (Microcystis aeruginosacomplex) along a wide spatial gradient

Escalera

Segura

Kruk

et al. 2019

Preprint

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Addressing ecological and evolutionary processes explaining biodiversity patterns is essential to identify the mechanisms driving community assembly. In the case of bacteria, the formation of new ecologically distinct populations or ecotypes is proposed as one of the main drivers of diversification. New ecotypes arise when mutation in key functional genes or acquisition of new metabolic pathways by horizontal gene transfer allow the population to exploit new resources, making possible their coexistence with parental population. Recently, we have reported the presence of toxic, microcystin-producing organisms from the Microcystis aeruginosa complex (MAC) through a wide environmental gradient (800 km) in South America, ranging from freshwater to estuarine-marine waters. In order to explain this finding, we hypothesize that the success of toxic organisms of MAC in such array of environmental conditions is due to the existence of ecotypes having different environmental preferences. So, we analysed the genetic diversity of microcystin-producing populations of Microcystis aeruginosa complex (MAC) by qPCR and high resolution melting analysis (HRMA) of a functional gene (mcyJ, involved in microcystin synthesis) and explored its relationship with the environmental conditions through the gradient by functional classification and regression trees (fCART). Six groups of mcyJ genotypes were distinguished and selected by different combinations of water temperature, conductivity and turbidity, determining the environmental preferences of each group. Since these groups were based on the basis of similar sequence and ecological characteristics they were defined as ecotypes of toxic MAC. Taking into account that the role of microcystins in MAC biology and ecology has not yet been elucidated, we propose that the toxin might have a role in MAC fitness that would be mainly controlled by the physical environment in a way such that the ecotypes that thrive in the riverine zone of the gradient would be more stable and less influenced by salinity fluctuations than those living at the marine limit of the estuary. These would periodically disappear or being eliminated by salinity increases, depending on the estuary dynamics. Thus, ecotypes generation would be an important mechanism allowing toxic MAC adapting to and succeed in a wide array of environmental conditions.

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The limit of resistance to salinity in the freshwater cyanobacterium Microcystis aeruginosa is modulated by the rate of salinity increase

Melero‐Jiménez

Martín‐Clemente

García‐Sánchez

et al. 2020

Ecology and Evolution

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The overall mean levels of different environmental variables are changing rapidly in the present Anthropocene, in some cases creating lethal conditions for organisms. Under this new scenario, it is crucial to know whether the adaptive potential of organisms allows their survival under different rates of environmental change. Here, we used an eco‐evolutionary approach, based on a ratchet protocol, to investigate the effect of environmental change rate on the limit of resistance to salinity of three strains of the toxic cyanobacterium Microcystis aeruginosa. Specifically, we performed two ratchet experiments in order to simulate two scenarios of environmental change. In the first scenario, the salinity increase rate was slow (1.5‐fold increase), while in the second scenario, the rate was faster (threefold increase). Salinity concentrations ranging 7–10 gL‐1 NaCl (depending on the strain) inhibited growth completely. However, when performing the ratchet experiment, an increase in salinity resistance (9.1–13.6 gL‐1 NaCl) was observed in certain populations. The results showed that the limit of resistance to salinity that M. aeruginosa strains were able to reach depended on the strain and on the rate of environmental change. In particular, a higher number of populations were able to grow under their initial lethal salinity levels when the rate of salinity increment was slow. In future scenarios of increased salinity in natural freshwater bodies, this could have toxicological implications due to the production of microcystin by this species.

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Dynamics of toxic genotypes of Microcystis aeruginosa complex (MAC) through a wide freshwater to marine environmental gradient

Cited by 49 publications

References 65 publications

Adaptation of the toxic freshwater cyanobacterium Microcystis aeruginosa to salinity is achieved by the selection of spontaneous mutants

Adaptation of the toxic freshwater cyanobacterium Microcystis aeruginosa to salinity is achieved by the selection of spontaneous mutants

Genotyping and functional regression trees reveals environmental preferences of toxic cyanobacteria (Microcystis aeruginosacomplex) along a wide spatial gradient

The limit of resistance to salinity in the freshwater cyanobacterium Microcystis aeruginosa is modulated by the rate of salinity increase

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