Consideration of solar radiation as a relevant parameter associated with cyanobacteria in a tropical monomictic aquatic system

doi:10.21203/rs.3.rs-6156856/v1

Studies performed in Valle de Bravo (VB) reservoir in Mexico record the presence of cyanobacteria proliferation and microcystin LR (MC-LR), both from 1998 to 2022, related mainly to two environmental factors, nitrates (NO3) and temperature. We propose that these four parameters do not converge seasonally during stratification and mixing. We also suggest that solar radiation as a temperature effector could have a greater association between the parameters studied. We conducted laboratory tests to evaluate the intensity of light (rather than solar radiation) at different concentrations of NO3 to observe the growth of the model used, a wild-type cyanobacteria (M. aeruginosa) producer of MC-LR. The objectives of this study were to prove if there was a seasonal relationship between cyanobacteria and MC-LR with NO3 and temperature and to evaluate in vitro assay the association between light radiation and NO3 on the growth of the cyanobacterium Microcystis aeruginosa and MC-LR. Subsequently, wild-type microcystin-containing M. aeruginosa was cultured in different proportion of light radiation and NO3 (100, 50, 25 and 5%) to simulate the seasonal variation. The results showed that the algae did not proliferate due to the seasonal availability of NO3 but rather due to temperature. In vitro we observed that light radiation had a greater effect than NO3 on the growth of M. aeruginosa. The role of NO3 was inversely related to the presence of MC-LR but only with high light radiation. Therefore, we conclude that solar radiation governs the effect of NO3 for the proliferation of algae and cyanobacteria.

microcystin MC-LR

light radiation

M. aeruginosa

nitrates

tropical aquatic ecosystem

Cyanobacterial growth in aquatic systems has been associated with high nutrient loads, mainly phosphorus and nitrogen. These elements are responsible for the frequency, intensity and duration of blooms. Particularly inorganic forms of nitrogen as nitrates (NO3) are more directly related to cyanobacteria, since they play an important role in the production of several cyanotoxin (Rocha et al. 2024). However, field observations do not always agree that cyanobacteria proliferate under conditions abundant in NO3. Therefore, it has been proposed to extend the nutrient limitation competition model by incorporating light as a third resource. Fluctuations in solar radiation affect the phytoplankton community structure, making nutrient ratios secondary. Integrating this new nutrient-light approach helps predict species coexistence or dominance (Brauer et al. 2012, Harpole et al. 2016).

The environmental concordance between cyanobacteria, NO3 and temperature due to solar radiation is seasonally present during mixing (period when NO3 are abundant) in the most common aquatic systems such as cold monomictic and dimictic (Kramer et al. 2024). In the first case, refers to systems of cold temperate regions or at high elevations in subtropical latitudes, the mixing occurs twice a year, in spring and autumn, and are stratified directly in summer and inversely stratified under an ice sheet in winter. In the second case, these are arctic and mountain systems, covered with ice most of the year with a single mixing period in summer at 4 °C and stratification occurs during the winter (Alvarez 2023).

This generalization, primarily about the presence of cyanobacterial blooms associated with high levels of NO3, is transferred as a fact to warm monomictic systems in tropical environments, such as in central Mexico in the Valle de Bravo reservoir (VB). In VB cyanobacteria proliferate from spring to autumn, but they do so during stratification and not in the mixing season. Therefore, the environmental criterion that remains constant with respect to the other two aquatic systems mentioned is temperature. This leaves the effect of NO3 in second place, as they are scarce when cyanobacteria proliferate.

Valle de Bravo is classified as a high altitude epicontinental body of water with <2300 m above sea level. The VB is a very important system, since it supplies almost 40% of the drinking water to the Metropolitan Area of Mexico City. This reservoir is stratified for nine months from March to October, and with complete mixing from November to February. VB has been reported as eutrophic since 1989, condition that had promotes the presence of toxic and non-toxic cyanobacteria blooms (Olvera-Viascán et al. 1998, Merino-Ibarra et al. 2008). From the early 2000s to date, as diazotrophic as non-diazotrophic cyanobacteria have been dominant in VB during the stratification season. This period is characterized by a tendency to NO3 limitation due to thermocline. Blooms and presence of MC-LR during this season are explained to the fact there is a contribution of nutrients to the water column from the boundary mixing (which would correspond to the first mixing during spring in dimictic systems) or by winds, generate a vertical displacement of nutrients, including NO3. In the mixing season there is an increase in the concentration of NO3 caused by the circulation of water that allows a homogeneous distribution of this nutrient. Even with this increase in NO3, cyanobacteria do not proliferate; even decrease considerably (García et al. 2002, Nandini et al. 2008, Ramírez-Zierold et al. 2010). Based on this, we observed in VB an opposite trend between NO3 and cyanobacteria, unlike studies that establish a direct relationship between both parameters. It is important to delve into this current generalization, since the abundance of cyanobacteria, in turn, extends as an indicator of health risk by the presence of microcystin-LR (MC-LR) in the water of the reservoir.

On the other hand, VB records during stratification and when cyanobacteria proliferation does not conform to low levels of NO3, temperature is incorporated as a secondary environmental criterion that acts as a growth enhancer (). We postulate that this could only happen in part and as far as temperature is concerned, but not for NO3. For example, in the warm months of March and April, the temperature is around 23 °C, while NO3 hovers around low levels of (). Under these environmental conditions the density of cyanobacteria and MC-LR records the highest values of the year, in range of 1 to 5 μg L^-1. Later during the winter in the months of November to February, the temperature drops around 17 °C, but there is a greater amount of NO3, approximately 0.05. During this season the density of cyanobacteria decreases by about 0.5. , and MC-LR concentration shows values even below 1 μg L^-1 (Gaytan-Herrera et al. 2011, Figueroa-Sanchez et al. 2014, Valeriano-Riveros et al. 2014, Alillo-Sánchez et al. 2015, Nandini et al. 2019, Arias-Rodriguez et al. 2020). With these first observations to the data in VB, temperature is placed before NO3 in cyanobacterial proliferation.

We consider the effect of temperature on cyanobacteria growth to be an expression of solar radiation that would complement current parameters related to cyanobacteria. In VB the information of effect of solar irradiation on phytoplankton has been recorded in a punctual and non-recurrent way throughout the annual cycle. For example, in monthly records at VB during the mixing, an unusual decrement of cyanobacteria due to a low light radiation of 2mM photon is reported (Valeriano-Riveros et al. 2014, Arias-Rodriguez et al. 2020). Similarly, in the reservoir the association of solar radiation with the amount of MC-LR toxin has not been considered. Therefore, we wonder if in the studies carried out in VB the proposed association pattern between cyanobacteria, NO3 and temperature is an environmental constant. On the other hand, what would be the response of growth and production of MC-LR from a model cyanobacterium when exposed to different levels of light radiation and NO3.

We hypothesized that the data in VB on the abundance of cyanobacteria are not related to levels of NO3, but with temperature during stratification and mixing seasons. By checking whether these association patterns are present in VB, we could establish the quantitative relationships between them. We also propose that the incidence of light radiation could complement the dynamics between cyanobacteria, MC-LR and NO3. Therefore, the first objective of this study was to statistically know the association between the presence of cyanobacteria, MC-LR, NO3 and temperature at the stratification stations and mixing in the reservoir of VB. The second objective was to evaluate in vitro the effect of light intensity and NO3 availability on the growth of the cyanobacteria Microcystis aeruginosa and its production of MC-LR. In doing this we consider establishing the importance of constantly monitoring light irradiation in VB to analyze, understand and predict the seasonal dynamics of cyanobacteria blooms and MC-LR with respect to the availability of NO3.

Data collection

Scopus, Springer and Web of Science databases were reviewed using search terms such as: reservoir, Valle de Bravo, stratification, mixing, monthly monitoring, cyanobacteria, microcystin-LR, NO3, and temperature. Initially 95 results were obtained, of which 28 were repeated work between the databases. Out of 67 jobs, 58 posts were removed where at least five of the search criteria did not appear in each job. Nine publications were selected for the VB reservoir covering 1998-2022. Each study had monthly records in the stratification and mixing seasons of the cell density of cyanobacteria or the presence of MC-LR together with related parameters such as NO3 or temperature.

Experimental test

Organisms

The cyanobacterium Microcystis aeruginosa was isolated randomly from VB reservoir, 1780 m a. s. l. (19°11´ N; 100°09´ W,), State of Mexico, Mexico. The taxonomic keys used for determining the cyanobacterium was Komárek and Anagnostidis (1999) and Cronberg and Annadotter (2006). M. aeruginosa was maintained in monocultures using Z8 medium (Staub 1961, NIVA 1972), the cultures were in suspension by means of an orbital shaker (Orbit 1900, Labnet) at room temperature of 26 ± 2 °C, pH 6.8 and light irradiation of photons of 100 μmol m² s^-1, emitted by a cold white fluorescent light (T8 Power Light 30w, Azoo) with a photoperiod in light-dark cycles 14:10 h. The irradiance of the light was measured through a quantum sensor equipped with a hemispherical sensor (MQ-200, Apogee Instruments).

Before experimental phase, the cyanobacteria monoculture strain in exponential growth phase was centrifuged and resuspended to be cultured in nitrogen-free Z8 medium for 12 hours in order to avoid the accumulation of nitrogen from the stock culture. This was made to reduce the presence of extracellular MC-LR in the culture medium. This process was carried out once more, and after 24 hours the cells were concentrated by centrifugation at 3000 rpm for 3 minutes and inoculated into the experimental cultures.

Growth conditions

The nitrogen source used in the tests was NaNO₃ and mentioned as NO₃ in the text. Its availability of 100% corresponded to a concentration of 4.67 g L^-1, which contains the formulation of the culture medium Z8. From the NaNO₃ concentration of the Z8 medium, a lower concentration gradient was established, reducing the nitrogen source by 50, 25 and 5%, so that the evaluated concentrations remained at 2.34, 1.17 and 0.47 NaNO₃ g L^-1. In the case of photon irradiation an availability of 100% corresponded to 100 µmol photons m^-2 s^-1, this based on the range of best light intensity that favors growth for Microcystis genus in laboratory cultures (Wiedner et al. 2003, Gris et al. 2014). The gradient of lower light intensity was established in the same proportion as the nitrogen source (50, 25 and 5%), so that the irradiation evaluated was 50, 25 and 5 µmol photons m^-2 s^-1. The use of the experimental proportions of these two factors emulated the high concentration of nitrogen during mixing and lower radiation, while a lower concentration of nitrogen and high radiation during stratification.

The experimental test was performed in triplicate as batch cultures in 500 mL flasks with a Z8 mean volume of 200 mL. An initial cyanobacterial biovolume inoculum was 4 x 10⁴µm³ mL^-1 and the experiment were carried out for a period of 20 days, taking a sample in every two days. The cultures were maintained under the same growth conditions at temperature of 26 ± 2 °C, since the factor to be evaluated was light radiation. Likewise, the conditions of agitation and pH were kept the same as those of the maintenance cultures.

Cell density

From each culture, 1 mL sample was taken and it was fixed with Lugol solution at 2%. The cell number was determined by an improved Neubauer hemocytometer and the result was expressed as biovolume using a transformation of the data based on the geometric models (Sun and Liu 2003).

Quantification of NO₃ and MC-LR

For NO₃ determination 1 mL of sample and was taken by filtered in nitrocellulose membrane (0.45 μm. Millipore, USA) for obtained a cell free sample. The analysis was performed using a colorimeter (YSI 9500 photometer, YSI Inc, USA), with a dilution factor of 1:10, according to the manufacturer's specifications.

To determine MC-LR from the cultures of M. aeruginosa 1 mL culture aliquots were taken, centrifuged at 10,000 rpm for 5 min and the supernatant was filtered through nitrocellulose membrane (0.45μm, Millipore, USA) and was used for determine the amount of extracellular MC-LR, subsequently analyzed with a QuantiPlate Kit for MC-LR (EnviroLogix, USA) according to the protocol provided by the manufacturer. The analyses were done in triplicate and the results were expressed in μg L^-1 as equivalents of MC-LR.

Statistical analysis

We selected parameters that were recorded monthly in the reviewed works and that we related to the presence of cyanobacteria for analysis. We made combinations of the selected parameters with the presence of cyanobacteria to analyze them and establish their relationship. Data were grouped into the two seasonal seasons of the reservoir, stratification and mixing. Given the background mentioned in the publications on the relationship between these parameters, we carry out a statistical analysis to verify whether this relationship exists or if the data are independent of each other. Given the difference in numerical magnitude of each of these parameters, the data was transformed to a single magnitude using the equation Y=Ln(Y) for analysis and statistical comparison. We apply a D'Agostino & Pearson omnibus normality test to corroborate the uniformity of the data and choose the type of statistical test that relates the parameters. In each of the studies, according to the distribution of their data, under a normal distribution we use the Pearson test, while for those with a non-normal distribution, we apply the Spearman correlation test. Both statistical tests with an alpha equal to 0.05. Finally, to determine the association relationship between the selected parameters we apply a test of X2 with an alpha of 0.05. Los analisis estadisticos y gráficas fueron elaborados usando Origin Pro 2018 software (Origin Lab, Northampton, MA, USA).

In the review of the work at VB we found that the sampling periods were different, nine of them were 12 months and two 24 months. Within the nine mentioned, there were even two jobs that did not have a record in one or two months, particularly during the mixing season. We also observed that the parameter with the lowest record was DM, which appeared in only four studies. The results published within the studies did not show the same behaviour trend in any of the parameters. From the combinations we made between these parameters studied, we observed that within a same category there were both types of distribution of data, values which together had a normal distribution (P) or a non-normal distribution (NP). In the algal density stratification, 61% of the jobs were P and 38% were NP. Temperature was 58% for P and 42% for % NP. For NO3, 64% was P and 36% NP. In MC, 70% was P and 30% NP. In the mix, the studies with an annual monitoring cycle had insufficient data for their analysis, and only the two studies that recorded two annual cycles were considered. In the case of algal density all results had P. For temperature 80% was P and 20% NP. The NO3 showed 40% P and 60% NP. For MC the results were NP.

Regarding the correlations between the parameters, we found that during the stratification season there were positive correlations between cell density and MC, and this in turn with temperature. While the correlations between NO3 with algal density, temperature and MC were negative. The correlation between algal density and temperature was also negative (Table 1, part 1 and 2).

Unlike the previous season, during mixing the positive correlations were between temperature and algal density and MC. NO3 was not correlated with any of the other parameters and finally there was no correlation between algal density and MC (Table 2 part 1 and 2). The X₂ test, showed en ambas temporadas con the categories analyzed a total frequency of 34 negative correlations versus 26 positive correlations. Principalmente se encontraron correlaciones negativas entre el NO3 y la temperatura junto con la densidad cianobacterial; estando estas dos ultimas realcionadas. El resultado total de la prueba indicó que no hay asociación entre los parametros ambientales y biologicos relacionados a la proliferación de las cianobacterias y su MC-LR (Table 3).

By experimentally evaluating the effect of variation in light intensity and NO3 on M. aeruginosa, we observed that in cultures with optimal growth conditions (100% irradiation and 100% NO3) a total biovolume of 5.5 μm3 mL-1 was achieved. However, this was exceeded at 5.8 μm3 mL-1 when half of the nitrogen source (50% NO3) was supplied in the cultures. In this light intensity there was an increase in the total MC-LR as the proportion of NO3 decreased (3.7 μg L-1 in 100%, 4.4 μg L-1 in 50%, 4.6 μg L-1 in 25% and 4.7 μg L-1 in 5%). When recording the nitrogen assimilation, we observed that in the test, with the lowest proportion of NO3 supplied (5%), the utilization of this nutrient was more in the direction of the increase of the toxin (as a vertical change in concentration) than to the increase of the biovolume. By increasing the source of nitrogen (from 25 to 100%), the use of this nutrient was directed at the increase in biovolume rather than the increase in toxin (as a horizontal change in concentration). This inequality of the effect of nitrogen for biovolume and toxin showed that in the NO3 deficiency trials (25 and 5%), both biological parameters were more related than in the cultures with higher nutrient proportion (Fig. 1 a-d).

When the light radiation was reduced by half (50%), we found that the high availability of NO3 (100%) favored the growth of M. aeruginosa reaching a total biovolume of 4.5 μm³ mL^-1 and we observed a trend where the deficiency in the proportion of nitrogen in cultures negatively affected the total biovolume. On the contrary, we found that a decrease of 50% of NO3 in cultures had a greater effect on the increase of total MC-LR (4.6 μg L^-1), unlike the other proportions of NO3 evaluated (3.3 μg L^-1 at 100%, 3.7 μg L^-1 at 25% and 3.9 μg L^-1 at 5%). This difference between microcystin and biovolume results in the 50% NO3 assays was reflected as a lower relationship between both parameters compared to the three tested conditions (Fig. 1 e-h).

In cultures with 25% light radiation, the highest values recorded in the total biovolume of M. aeruginosa (3.7 μm³ mL^-1) and total MC-LR (4.5 μg L^-1) were presented in the cultures exposed to a high availability of NO3 (100%). Thus, as the nitrogen source decreased, both the total biovolume of cyanobacteria (3.0 at 50%, 3.1 at 25% and 2.3 μm³ mL^-1 at 5%) and the total MC-LR (3.7 μg L^-1, 2.8 μg L^-1 and 1.2 μg L^-1, respectively) decreased. We observed that in proportions less than 100, there was a recirculation of the concentration of nitrogen as the biovolume increased in each test. At this light intensity, the total relationship between biovolume and microcystin was closer in the studies with intermediate proportions of NO3 (50 and 25%), while it was distant in the extremes such as 100 and 5% (Fig. 1 i-l).

Under minimum conditions of light radiation (5%), we observed that the total biovolume achieved by M. aeruginosa was similar between the 100, 50 and 25% tests of NO3 (2.8, 2.4 and 2.4 μm3 mL-1). From these crops, only in high availability of NO3 (100%), a higher total MC-LR (3.2 μg L-1) was observed than the subsequent evaluated NO3 ratios (1.0 μg L-1 at 50%, 1.9 μg L-1 at 25% and 0.7 μg L-1 at 5%). Also in these trials, the relationship between the biovolume and MC-LR was closer. In this series of experiments, we also observed a recirculation of the nitrogen concentration, mainly when the total MC-LR had the highest values at 100 and 25% of NO3 (Fig. 1 m-p).

Conventionally it was believed that phosphorus contributes to the proliferation of cyanobacteria. However, nitrogen takes an important role in the eutrophication process, also participating in the synthesis of microcystins (Søndergaard et al. 2017). The results of the parameters analyzed in VB showed that NO3 was not associated with cyanobacteria, MC-LR or temperature during the stratification or mixing season. The temperature was related to cyanobacteria only in the mixing season, while with MC-LR it was in both seasons, being lower during the mixing. Finally, we found that only during stratification did cyanobacteria become associated with MC-LR.

Our data are consistent with the hypothesis presented, in which VB NO3 is a secondary mediator of the presence of cyanobacteria, positioning temperature as the parameter responsible for the presence of cyanobacteria and their toxins. However, we note that studies with MC-LR records represent between 33 and 44% of the total reviewed. This means that increased studies in monitoring of dissolved MC-LR are required. So that water management and its potential risk of microcystins in the VB reservoir is not established based solely on these few studies or by effect juxtaposed to cyanobacterial density.

This leads us to consider that the different species of cyanobacteria have a particular susceptibility to temperature, which is related to the synthesis of microcystins and NO3. For example, M. aeruginosa and Planktothrix agardhii grown in crops at temperatures ranging from 18 to 20 °C (similar to the mixture) with minimal concentrations of NO3 (based on the concentrations in the culture medium BG-11), have shown slower growth rates but with higher intracellular microcystin production. By exposing cyanobacteria to higher concentrations of NO3, it does not increase the production of cyanotoxins. By contrast, when temperatures range from 22 to 26 °C (similar to the stratification season) and at optimal concentration of NO3 in the culture medium, cyanobacteria grow faster, but with a decrease in intracellular microcystin. At temperatures above 26°C with sufficient NO3, both cyanobacterial growth and microcystine synthesis decrease (Scherer et al., 2017; Peng et al., 2018; Walls et al., 2018).

The in vitro behavior of these cyanobacteria is suggested as an approximate representation in natural systems, such as VB. During mixing, temperature restricts the growth rate of cyanobacteria, directing their metabolism to toxin synthesis. Subsequently, when the temperature increases during stratification, cyanobacteria increase their growth rate rather than producing toxins. Given our results of association during the stratification season between cyanobacteria and MC-LR, we agree with the revised work of VB, in which the proliferation of cyanobacteria does carry a potential risk with the increase of MC-LR. However, temperature is the parameter which influences the cyanobacteria-MC-LR relationship, acting first on the growth rate and thus on the number of organisms, which contribute to the accumulation of microcystin in the medium, despite their reduced production capacity. This means that although cyanobacteria are less toxic in the stratification, their population increase translates into a proportional relationship with microcystin. This makes temperature, together with other parameters related to cyanobacteria, play a predictive role in the levels of microcystin in natural environments (Peng et al., 2018). When evaluating in vitro the effect of variation in light radiation, rather than temperature, and with different NO3 ratios on M. aeruginosa. We propose for VB a different dynamic than that established in the revised work with respect to cyanobacteria proliferation, and which may be mediated by environmental changes of light. Under optimal growth conditions, with the ratio of 100% light radiation and 100% NO3, M. aeruginosa did not reach its highest total biovolume, compared to the entire series of trials evaluated. It was in the cultures with the same intensity of light but with 50% of NO3 provided, that we recorded the maximum growth of cyanobacteria. We also observed that M. aeruginosa reduced its total biovolume each time the proportion of NO3 decreased. Under this light radiation intensity, M. aeruginosa cultures showed an increase in MC-LR as the proportion of NO3 decreased, becoming more evident when cyanobacteria grew in minimal concentrations of this nutrient (5% of NO3). We also observed a similar increase in MC-LR when M. aeruginosa was exposed to 50% decrease in both light and NO3 radiation. These experimental results, when transferred to the dynamics of the VB reservoir, could be linked to the stratification season, where the proliferation of cyanobacteria would result from the increase in the incidence of solar radiation, increasing the water temperature. On the other hand, a deficiency of NO3 supply at 50% in experimental crops would represent the decrease in nitrogen availability during this season and would explain the increase in microcystin in the reservoir. So the effect on the decrease of light radiation, in experimental tests, could exemplify when there is an environmentally decreasing of solar radiation due to weather variations.

Considering the records of the distribution of solar radiation in Central Mexico during the months of March and mainly April, the incidence of light increases due to the presence of clear without cloudless skies, which corresponds to the season of "dry" (Galindo et al. 1991, Matsumoto et al. 2014). This allows greater light penetration through the water column, thereby increasing the temperature, so cyanobacteria proliferate under this region of photosynthetically active radiation (unlike other phytoplankton groups), increasing its growth rate and reaching cell densities for the formation of blooms (cita…). In the following months from May to October, the intensity of light is not as high due to the presence of clouds, winds and rainfall, corresponding to the "rain" season (Galindo et al. 1991, Matsumoto et al. 2014, Hernandez-Escobedo et al. 2015, Gutiérrez-Trashorras et al. 2018). Then due to these weather variations the cyanobacteria continue to proliferate, but in an attenuated form and to a lesser extent compared with records in the months of higher temperature (Nandini et al. 2008, Ramírez-Zierold et al. 2010; Gaytan-Herrera et al. 2011, Valeriano-Riveros et al. 2014; Alcocer et al. 2020; Merino-Ibarra et al. 2021).

On the other hand, M. aeruginosa in cultures with 25 and 5% light radiation showed a reduction in its total biovolume, even in the presence of high availability of NO3 (100 and 50%). We observed that the combination of these parameters showed MC-LR values similar to those measured in crops with higher light radiation. With these experimental results, it is suggested that the dynamics in VB during the mixing season could be due to the decrease of sunlight in the cold months and that it would influence the low presence of cyanobacteria, although the amount of NO3 increases, due to the homogeneous distribution of nutrients in the water column (Gaytan-Herrera et al. 2011, Figueroa-Sanchez et al. 2014, Valeriano-Riveros et al. 2014, Alillo-Sánchez et al. 2015, Nandini et al. 2019, Arias-Rodriguez et al. 2020). The lower solar radiation translated as a reduction in temperature in this period, is explained due to latitudinal tilt of the axis of earth with respect to the position of the sun. In the geographic location of VB, the incidence of light is lower mainly during the months of December and January with temperatures around 17 °C (Galindo et al. 1991, Rivas et al. 2013, Matsumoto et al. 2014, Borunda et al. 2021). So that the decrease of solar radiation and lower temperature, would reduce the density of cyanobacteria but enhancing their ability to produce more microcystin (Scherer et al., 2017; Peng et al., 2018; Walls etc., 2018).

From a genetic perspective during mixing, genes responsible for MC-LR biosynthesis (microcystin synthetase, mcy: ABC and DEFGHIJ groups) are activated when there is nitrogen deficiency, increasing toxin production. In particular, the mcyHIJ genes are responsible for the elaboration and transport of microcystin molecules (Kaebernick et al. 2002, Pearson et al. 2008, Pineda-Mendoza et al. 2016, Bouaïcha et al. 2019). In addition, light limiting criterion acts on the mcyD gene, a fragment that codes for the formation of the molecule in the β-ketoacyl synthase and the acyltransferase domains, promoting the production of the toxin. These mcyD transcripts seem to overlap in their expression independently of the availability of NO3 and its associated gene mcyB (which adds l-Leu and d-Me Asp to the growing polypeptide chain of microcystin biosynthesis), which is activated by the temperature increase (Yang et al. 2012, Pimentel and Giani 2014, Chaffin et al. 2018, Chen et al. 2019).

Adding the monitoring of solar radiation as another environmental study factor to the various environmental parameters already studied in VB, would contribute to a better understanding of the dynamics of cyanobacteria and their blooms. For example, seasonal variation of solar radiation could be integrated into studies explaining the increase in cyanobacteria due to wind and wave in the reservoir during stratification (Ramírez-Zierold et al. 2010, Valeriano-Riveros et al. 2014, Merino-Ibarra et al. 2021). The displacement of water capable of vertically mobilizing NO3 and increasing its availability is not observed in our results as a direct relationship between NO3 and cyanobacteria density. In aquatic systems, the effect of nitrogen in conjunction with water temperature and this time as a consequence of solar radiation has been studied. Approximately 40% of water temperature is a direct consequence of solar radiation and the remaining 60% also depends on air temperature, which is mainly modified by factors such as wind speed and cloud cover (MacIntyre and Melack 2010, Schmid and Köster 2016, Shatwell et al. 2019). These clouds present intermittently during the stratification or rainy season, attenuate the intensity of solar radiation so that it would reduce the growth of the dominant species even if the amount of NO3 has been increased. These environmental conditions may also explain the wide variations in values recorded in the reviewed studies. So that for now it is not possible in VB to establish a generalization of the dynamics of cyanobacteria associated mainly NO3 and temperature.

If we consider the effect of sunlight on the environment, this is very useful for understanding the aquatic system. Light is transmitted in two ways in the water body, long wave radiation (+3000 nm) is absorbed and converted to heat mainly on the surface of the water and allows both stratification and mixing. Meanwhile, short wave radiation (400 to 700 nm) penetrates into the water column and has a direct influence on photochemical processes (Han et al. 2020, Talling 2020). Since cyanobacteria are photoautotrophic organisms, different species show a certain affinity in particular for the quantity and quality of solar radiation. Light radiation has been considered as the main growth regulator of cyanobacteria above the availability of nutrients. Both diazotrophic and non-diazotrophic cyanobacteria respond primarily to the intensity and wavelength of the radiation spectrum for their growth and secondarily to nutrients that it maintains their cellular functions (Walsby et al. 2004, Posch et al. 2012, Schmid and Köster 2016, Yao et al. 2017). In particular the nitrogen source seems to stand out metabolically due to its participation in the production of MC-LR over the other nutrients (Burson et al. 2018, Andersson et al. 2019, Wang et al. 2019). So the role of light during stratification and mixing would explain why some cyanobacteria are predominant under different conditions of solar radiation. The intensity or quality of light may also be acting as a selective criterion that favors its growth by creating protective pigments and light collectors that allow the exploitation of separate niches in terms of radiation and spectral composition, so light can modify or regulate the presence of cyanobacteria in the water column (Huisman et al. 2018, Lichtenberg et al. 2020).

Studies in temperate systems have established a theoretical basis for the interaction of cyanobacteria with nutrients, light and temperature, in which these parameters act together on marked seasonal changes (). However, in tropical aquatic systems such as the VB reservoir there are no studies integrating the effect of light with the other parameters. In addition, since solar radiation in temperate aquatic systems is lower, for example in Central and Eastern Europe they have mean values of 142 to 193 W m-2, between cloudy and clear skies respectively (Sanchez-Lorenzo and Wild 2012). In Mexico the average solar radiation fluctuates around 700 W m-2 in spring-summer and 500 W m-2 in autumn-winter (Rivas et al. 2013). This means that the effect of a higher incidence of solar radiation on the VB reservoir cannot be compared with temperate systems in terms of behavior and dynamics of cyanobacteria considering only temperature and nutrient availability.

In this work we proposed that in VB the high cell density of cyanobacteria and the increase in MC-LR is not a direct consequence of excess nutrients or temperature. Therefore, we suggest to implement in the monitoring and evaluation of water quality the records of light radiation, which would contribute to a better understanding of the seasonal dynamics of these organisms. Likewise, by relating these three factors, cyanobacteria, NO3 and solar radiation, it would allow the establishment of new strategies in the management, control and mitigation of harmful blooms in monomictic tropical waterbodies. Therefore, it is recommended to implement a permanent program to reinforce this hypothesis to corroborate if this happens in VB, so that from these findings those responsible for managing the body of water. In this work, light radiation and NO3 availability were used as two parameters that were considered responsible for the presence of cyanobacteria and their toxins in a eutrophic system such as the VB reservoir. Due to the complex relationship of these organisms with other environmental factors, it is suggested that further studies be conducted which include the effect of other nutrients in addition to NO3. As well as evaluating the dynamics of other diazotrophic cyanobacteria species at different wavelengths in both monocultures and mixed crops.

During stratification we found positive correlations of the density of algae with temperature and MC-LR, also NO3 with MC-LR. There was no correlation between NO3 with density and temperature, the latter with MC-LR. In the mixture we found a positive association of the density of algae with MC-LR and this with NO3. The negative correlations were between temperature and algal density and MC-LR. There was no association between NO3 and temperature and density of algae.

Disclosure statement

No potential conflict of interest was reported by the authors.

Funding

This work was supported by Project: FESI-PAPCA 2021-2022-54.

ORCID

Chicalote-Castillo David: https://orcid.org/0000-0003-2248-2162

Ramírez-García Pedro: https://orcid.org/0000-0003-1410-4495

Luna-Pabello Víctor M: https://orcid.org/0000-0001-8651-0295

Author Contribution

DCC: Participation in data collection from the field and conducting experiments PRG: Idea, data analysis, manuscript writingVMLP: Data analysis, manuscript writing

Acknowledgements

This work was carried out in accordance with the requirements of the Postgraduate Program in Biological Sciences, UNAM. The first author thanks CONACyT-225898 for a doctoral scholarship.

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Stratification season	Cyanobacterial density vs Temperature					Cyanobacterial density vs MC-LR					Cyanobacterial density vs NO₃
Author	N Test		n	C	W (%)	N Test		n	C	W (%)	N Test		n	C	W (%)
Author	Cd	T	n	C	W (%)	Cd	MC	n	C	W (%)	Cd	NO₃	n	C	W (%)

1	P	P	8	0.72	10	P	P	8	0.89	25	P	P	8	-0.82	11
2	NP	NP	16	0.97	20	NP	NP	16	-0.76	50	NP	NP	16	-0.53	22
3	NP	NP	16	-0.03	20	-	-	-	-	-	NP	P	16	-0.13	22
4	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
5	P	P	8	0.49	10	P	P	8	0.50	25	P	P	8	0.50	11
6	P	NP	8	-0.32	10	-	-	-	-	-	P	P	8	-0.24	11
7	P	P	8	-0.54	10	-	-	-	-	-	-	-	-	-	-
8	P	P	8	-0.36	10	-	-	-	-	-	P	P	8	0.52	11
9	NP	P	8	0.20	10	-	-	-	-	-	NP	NP	8	0.13	11

TC	NP	P	80	-0.03	100	NP	P	32	0.50	100	P	P	72	-0.56	100
CI	-0.25 to 0.20					0.18 to 0.73					-0.70 to -0.38

Table 1. Part 1. Comparative statistical analysis of the selected works for Valle de Bravo (VB) in the stratification season. Cd= Cyanobacterial density, T= Temperature, MC = MC-LR. P= Passed the normality test, NP= Not passed the normality test. C= Correlation index, W= Weight, TC= Total Correlation, CI= Correlation interval.

Stratification season	NO₃ vs Temperature					NO₃ vs MC-LR					MC-LR vs Temperature
Author	N Test		n	C	W (%)	N Test		n	C	W (%)	N Test		n	C	W (%)
Author	NO₃	T	n	C		NO₃	MC				MC	T

1	P	P	8	-0.78	10	P	P	8	-0.91	20	P	P	8	0.91	25
2	NP	NP	16	-0.56	20	NP	NP	16	0.80	40	NP	NP	16	-0.73	50
3	P	NP	16	-0.53	20	-	-	-	-	-	-	-	-	-	-
4	NP	NP	8	0.02	10	P	P	8	0.01	20	-	-	-	-	-
5	P	P	8	-0.26	10	P	P	8	0.96	20	P	P	8	-0.07	25
6	P	NP	8	0.18	10	-	-	-	-	-	-	-	-	-	-
7	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
8	P	P	8	-0.66	10	-	-	-	-	-	-	-	-	-	-
9	NP	P	8	-0.26	10	-	-	-	-	-	-	-	-	-	-

TC	P	P	80	-0.02	100	P	P	40	-0.18	100	P	N	32	0.29	100
CI	-0.24 to 0.20					-0.46 to 0.14					-0.07 to 0.59

Table 1. Part 2. Comparative statistical analysis of the selected works for Valle de Bravo (VB) in the stratification season. Cd= Cyanobacterial density, T= Temperature, MC = MC-LR. P= Passed the normality test, NP= Not passed the normality test. C= Correlation index, W= Weight, TC= Total Correlation, CI= Correlation interval.

Mixing season	Cyanobacterial density vs Temperature					Cyanobacterial density vs MC-LR					Cyanobacterial density vs NO₃
Author	N Test		n	C	W (%)	N Test		n	C	W (%)	N Test		n	C	W (%)
Author	A	T	n	C	W (%)	A	MC	n	C	W (%)	A	NO₃	n	C	W (%)

1	ID	ID	4	0.20	11	ID	ID	4	0.32	29	ID	ID	4	-0.40	13
2	P	P	8	-0.23	22	P	NP	8	0.55	57	P	NP	8	-0.64	24
3	P	P	8	0.09	22	-	-	-	-	-	P	P	8	-0.40	24
4	-	-	-	-		-	-	-	-	-	-	-	-	-
5	ID	ID	2	ID	5	ID	ID	2	ID	14	ID	ID	2	ID	6
6	ID	ID	3	0.50	7	-	-	-	-	-	ID	ID	3	-0.50	7
7	ID	ID	4	0.40	11	-	-	-	-	-	-	-	-	-
8	ID	ID	4	0.63	11	-	-	-	-	-	ID	ID	4	-0.77	13
9	ID	ID	4	-0.20	11	-	-	-	-	-	ID	ID	4	0.20	13

TC	P	NP	37	0.53	100	NP	NP	14	-0.02	100	P	NP	33	-0.39	100
CI	0.23 to 0.73					-0.56 to 0.53					-0.65 to -0.05

Table 2. Part 1. Comparative statistical analysis of the selected works for Valle de Bravo (VB) in the mixing season. Cd= Cyanobacterial density, T= Temperature, MC = MC-LR. P= Passed the normality test, NP= Not passed the normality test. C= Correlation index, W= Weight, TC= Total Correlation, CI= Correlation interval.

Mixing season	NO₃ vs Temp					NO₃ vs MC-LR					MC-LR vs Temp
Author	N Test		n	C	W (%)	N Test		n	C	W (%)	N Test		n	C	W (%)
Author	NO₃	T	n	C	W (%)	NO₃	MC	n	C	W (%)	MC	T	n	C	W (%)

1	ID	ID	4	-0.80	11	ID	ID	4	-0.63		ID	ID	4	-0.80
2	NP	P	8	0.07	22	NP	NP	8	-0.89		NP	NP	8	-0.89
3	P	P	8	-0.90	22	-	-	-	-	-	-	-	-	-	-
4	ID	ID	4	0.63	11	ID	ID	4	-0.32		-	-	-	-	-
5	ID	ID	2	ID	5	ID	ID	2	ID		ID	ID	2	ID
6	ID	ID	3	-1.00	7	-	-	-	-	-	-	-	-	-	-
7	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
8	ID	ID	4	-0.63	11	-	-	-	-	-	-	-	-	-	-
9	ID	ID	4	0.89	11	-	-	-	-	-	-	-	-	-	-

TC	P	P	37	-0.29	100	NP	P	18	-0.28	100	P	P	14	0.13	100
CI	-0.56 to 0.03					-0.67 to 0.23					-0.43 to 0.62

Table 2. Part 2. Comparative statistical analysis of the selected works for Valle de Bravo (VB) in the mixing season. Cd= Cyanobacterial density, T= Temperature, MC = MC-LR. P= Passed the normality test, NP= Not passed the normality test. C= Correlation index, W= Weight, TC= Total Correlation, CI= Correlation interval.

Environmental and biological parameters	Positive Correlation			Negative Correlation
	Stratification season	Mixing season	TOTAL	Stratification season	Mixing season		TOTAL
Cyanobacterial density vs Temp	4	5	9	4	2	6
Cyanobacterial density vs MC-LR	2	2	4	1	0	1
Cyanobacterial density vs NO₃	3	1	4	4	5	9
NO₃ vs Temp	2	3	5	6	4	10
NO₃ vs MC-LR	3	0	3	1	3	4
MC-LR vs Temp	1	0	1	2	2	4
TOTAL	15	11	26	18	16	34
X²	3.803
p	0.0512

Table 3. Comparison of the frequency between positive and negative correlations of environmental and biological parameters related to the proliferation of cyanobacteria, found in the nine works selected in VB.

No competing interests reported.

Consideration of solar radiation as a relevant parameter associated with cyanobacteria in a tropical monomictic aquatic system

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