Positive selection of digestive proteases in Daphnia: A mechanism for local adaptation to cyanobacterial protease inhibitors

Abstract

Due to the combined effects of global warming and eutrophication, the frequency of deleterious cyanobacterial blooms in freshwater ecosystems has increased. In line with this, local adaptation of the aquatic keystone herbivore Daphnia to cyanobacteria has received major attention. Besides microcystins, the most frequent cyanobacterial secondary metabolites in such blooms are protease inhibitors (PIs). Recently, it has been shown that a protease gene showed copy number variation between four D. magna populations that differed in tolerance to PIs. From that study, we chose two distinct populations of D. magna which had or had not coexisted with cyanobacteria in the past. By calculating FST values, we found that the two populations were genetically more distant in the protease loci than in neutral loci. Population genetic tests applied to the tolerant population revealed that positive selection was most probably acting on the gene loci of the digestive protease CT448 and CT802. We conclude that the selection of digestive proteases and subsequent reduction in copy number is the molecular basis of evolutionary changes leading to local adaptation to PIs.

Toward Disentangling the Multiple Nutritional Constraints Imposed by Planktothrix: The Significance of Harmful Secondary Metabolites and Sterol Limitation

“…Dietary protease inhibitors from M. aeruginosa strains have been shown to negatively affect Daphnia by hampering digestion and thus somatic growth rates (Rohrlack et al, 1999;Lürling, 2003;Schwarzenberger et al, 2010). However, it also has been demonstrated that Daphnia have specific means to cope with dietary protease inhibitors (Schwarzenberger et al, 2010(Schwarzenberger et al, , 2012(Schwarzenberger et al, , 2020Von Elert et al, 2012;, comprising physiological adaptations potentially resulting in population tolerance (Blom et al, 2006;Baumann and Jüttner, 2008;Schwarzenberger et al, 2017). Anabaenopeptins acting as carboxypeptidase inhibitors represent another group of harmful secondary metabolites produced by Planktothrix (Itou et al, 1999).…”

Draft genomes for one Microcystis-resistant and one Microcystis-sensitive strain of the water flea, Daphnia pulicaria

“…Genomic resources are key components to deepening our understanding of the contributions of genetic background on strain-specific responses to toxic algal blooms and other environmental stressors. These resources can be used for understanding the transcriptomic responses to toxins ( Asselman et al 2012 ; Orsini et al 2016 ; Giraudo et al 2017 ), identifying sequence variants under positive selection across the genome ( Bourgeois et al 2017 ; Schwarzenberger et al 2020 ), and comparative analysis across other Daphnia species ( Ravindran et al 2019 ). In this way, these genomic resources provide a promising avenue for future research as the effects of urbanization and global climate change continue to exacerbate the severity of these toxic algal blooms over time ( Carpenter 2005 ; Schmale et al 2019 ).…”

A Long‐Term Study on the Effect of Cyanobacterial Crude Extracts from Lake Chapultepec (Mexico City) on Selected Zooplankton Species

“…It has been documented that the interclonal variability evident in several cladoceran genera can be attributed to differences in their metabolism and, as a result, their sensitivity to stressors (Barata et al 2001). Some studies (Chen et al 2005;Barrios et al 2017;Schwarzenberger et al 2020) also show that cyanobacterial extracts sometimes promote zooplankton growth because of the detoxification by enzymes.…”

“…Cyanobacterial blooms are common in both natural and man‐made water bodies. Whereas most studies highlight the adverse effects of cyanotoxins, there are a few showing that zooplankton can develop resistance to cyanotoxins because of enzymatic activities (Chen et al 2005; Schwarzenberger et al 2020) or as a result of the ability of protists in decomposing cyanobacteria and increasing the available fatty acids (Luo et al 2015). Many urban lakes in Mexico City contain high densities of cyanobacteria.…”