Cyanobacterial protease inhibitors lead to maternal transfer of increased protease gene expression in Daphnia

Abstract

Protease inhibitors (PIs) have frequently been found in cyanobacterial blooms and have been shown to affect the major herbivore Daphnia by decreasing growth and inhibiting gut protease activity. However, it has been shown that a clone of Daphnia is able to respond to dietary PIs by increasing its protease gene expression. Such an inducible response might be maternally transferred to the next generation. Therefore, we tested a tolerant clone for maternal transfer of protease gene expression. When exposed to the trypsin inhibitor-producing cyanobacterium Microcystis aeruginosa PCC7806 Mut, Daphnia mothers and their untreated newborns showed an increase in trypsin gene expression compared to naïve mothers grown on control food and their offspring. The maternally transferred increase in gene expression was accompanied by a higher somatic growth rate of the offspring generation from exposed mothers compared to offspring from naïve mothers. This higher growth rate compensated for the lower dry mass of newborns from exposed mothers and led to the same fitness as observed in the offspring of naïve mothers. In nature, clones that can maternally transfer increased protease gene expression should have an advantage over clones that cannot. The selection for such more tolerant clones by naturally occurring PIs might lead to microevolution of natural Daphnia populations, and to local adaptation in the long term. This is the first study to show an adaptive maternal transfer of increased target gene expression in an ecological context.

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

“…Nevertheless, it has been shown that Daphnia are able to respond to such inhibitors by an increase in protease gene expression (Schwarzenberger et al, ). This increased protease gene expression was demonstrated to be maternally transferred to the offspring of pre‐exposed mothers, which causes higher somatic growth rates of their offspring in comparison to offspring from naïve mothers (Schwarzenberger & Von Elert, ).…”

Deciphering the genetic basis of microcystin tolerance

“…Whereas adaptations to natural environments have been demonstrated in ecologically relevant organisms, the genetic basis of adaptation has mainly been investigated in genetic model organisms whose adaptations to environmental variability are of minor interest. In the case of Daphnia , studies identifying genes that account for adaptive traits are scarce, and are based on qPCR analyses of candidate genes which were identified on the basis of a-priori knowledge of their function [35, 36]. By using a transcriptome-wide approach, we have been able to answer the question as to which genes are involved in microcystin tolerance.…”

Clonal Variation in Growth Plasticity within a Bosmina longirostris Population: The Potential for Resistance to Toxic Cyanobacteria

“…Increased cyanobacterial densities can act as an important selection agent on zooplankton populations since cyanobacteria produce harmful compounds [9]. In the context of exposure to toxic cyanobacteria, daphniids either induce resistance within a life-time and pass it on to following generations [16–19], or evolve rapidly resistance over multiple generations [20–23]. Rapid evolution of organisms in response to environmental changes usually stem from selection on pre-existing genetic variation because beneficial alleles are already available and their probabilities are often higher than de novo mutation [40].…”

“…A short-time exposure to toxic cyanobacteria induces zooplankton defenses and enhances their fitness in cyanobacterial conditions [13–15]. These inducible defenses developed within one generation can be transferred to following generations via maternal effects and can contribute to neonatal success [16–19]. In addition to physiological adaptations, zooplankton can rapidly evolve genetically based resistance to toxic cyanobacteria [20–23].…”