Daphnia magna Exudates Impact Physiological and Metabolic Changes in Microcystis aeruginosa

Abstract

While the intracellular function of many toxic and bioactive cyanobacterial metabolites is not yet known, microcystins have been suggested to have a protective role in the cyanobacterial metabolism, giving advantage to toxic over nontoxic strains under stress conditions. The zooplankton grazer Daphnia reduce cyanobacterial dominance until a certain density, which may be supported by Daphnia exudates, affecting the cyanobacterial physiological state and metabolites’ production. Therefore, we hypothesized that D. magna spent medium will impact the production of cyanobacterial bioactive metabolites and affect cyanobacterial photosynthetic activity in the nontoxic, but not the toxic strain. Microcystin (MC-LR and des-MC-LR) producing M. aeruginosa PCC7806 and its non-microcystin producing mutant were exposed to spent media of different D. magna densities and culture durations. D. magna spent medium of the highest density (200/L) cultivated for the shortest time (24 h) provoked the strongest effect. D.magna spent medium negatively impacted the photosynthetic activity of M. aeruginosa PCC7806, as well as the dynamics of intracellular and extracellular cyanobacterial metabolites, while its mutant was unaffected. In the presence of Daphnia medium, microcystin does not appear to have a protective role for the strain. On the contrary, extracellular cyanopeptolin A increased in M. aeruginosa PCC7806 although the potential anti-grazing role of this compound would require further studies.

Cross talk: Two way allelopathic interactions between toxic Microcystis and Daphnia

“…Considering that the cyanobacteria and their genes responsible for toxin production are much older than complex organisms, such as their grazers, it has been suggested that an antigrazing role could have been obtained and kept over time due to grazing pressure (Wilken et al, 2010;Chislock et al, 2013). Increase of microcystin concentration in the presence of Daphnia infochemicals has been recorded in several studies (Jang et al, 2003(Jang et al, , 2007Izydorczyk et al, 2008;Kaplan et al, 2012;Pérez-Morales et al, 2015), as well as the higher export of microcyclamide 7806A (Sadler and von Elert, 2014a), and cyanopeptolin A (Bojadzija Savic et al, 2019) supporting this hypothesis. Cyanobacterial response seems to be strain dependant, as 4 out of 8 strains increased the production of microcystin in the presence of Daphnia medium (van Gremberghe et al, 2009).…”

“…Nevertheless, zooplankton often coexists with toxic cyanobacterial blooms, through co-acclimation, in mutual two-way interactions that are yet to be disentangled. It remains unclear whether Daphnia infochemicals could have negative impact on cyanobacterial growth and photosynthetic activity, due to contradicting results in the literature (Jang et al, 2007;Yang and Li 2007;Bojadzija Savic et al, 2019). Furthermore, whether cyanobacteria suffer from oxidative stress when exposed to daphnids requires further clarification.…”

“…Unraveling the natural role of microcystin and its dynamics for the cyanobacteria has been a topic of many studies with the emphasis on the influence of abiotic factors (such as light, nutrients, or temperature) (Gobler et al, 2007;Jähnichen et al, 2007;Schatz et al, 2007;Alexova et al, 2016). More recent studies focused on changes in the production of cyanobacterial metabolites mediated by biotic factors, such as the presence of grazers (Jang et al, 2003(Jang et al, , 2004van Gremberghe et al, 2009;Sadler and von Elert, 2014a;Harke et al, 2017;Bojadzija Savic et al, 2019). These studies suggest that the presence of Daphnia can trigger the production of cyanobacterial secondary metabolites via the substances they release in the water (infochemicals), which could be an antigrazing response.…”

“…Cyanobacterial response seems to be strain dependant, as 4 out of 8 strains increased the production of microcystin in the presence of Daphnia medium (van Gremberghe et al, 2009). On the other hand, the presence of Daphnia medium can also decrease microcystin concentration (Becker et al, 2010;Bojadzija Savic et al, 2019), as well as cyanopeptolin and aerucyclamide (Bojadzija Savic et al, 2019), leaving this role arguable. Furthermore, increase of microcystin has been associated with the intracellular protective role against oxidative stress, providing toxic strains advantage in stress inducing environments (Briand et al, 2008(Briand et al, , 2012Zilliges et al, 2011;Paerl and Otten, 2013).…”

Oxidative Stress, Programmed Cell Death and Microcystin Release in Microcystis aeruginosa in Response to Daphnia Grazers

“…Importantly, the use of spent medium or daphnid extracts allows only to study the effect of grazers on cyanobacteria while in situ a mutual interaction can occur, and possibly the array of molecules released by daphnids may be altered by the cyanobacteria presence. One should also note that the anti-grazing defense in Microcystis, including its non-MC producing strains, may also be attributed to other metabolites such as cyanopeptolin A or microcyclamide 7806A whose roles are much less studied (Sadler and von Elert, 2014;Bojadzija Savic et al, 2019, 2020. The present study employed only one strain of M. aeruginosa which was capable of MC-production.…”