A dietary polyunsaturated fatty acid improves consumer performance during challenge with an opportunistic bacterial pathogen

Abstract

A dietary deficiency in polyunsaturated fatty acids (PUFAs) and/or sterols can severely constrain growth and reproduction of invertebrate consumers. Single nutrients are potentially assigned to different physiological processes, for example to support defence mechanisms; therefore, lipid requirements of healthy and pathogen-challenged consumers might differ. In an oral exposure experiment, we explored the effects of dietary PUFAs and cholesterol on growth, reproduction and survival of an aquatic key herbivore (Daphnia magna) exposed to an opportunistic pathogen (Pseudomonas sp.). We show that healthy and pathogen-challenged D. magna are strongly albeit differentially affected by the biochemical composition of their food sources. Supplementation of a C20 PUFA-deficient diet with arachidonic acid (ARA) resulted in increased survival and reproduction of pathogen-challenged D. magna. We propose that the observed benefit of consuming an ARA-rich diet during pathogen challenge is conveyed partially via ARA-derived eicosanoids. This study is one of the first to consider the importance of dietary PUFAs in modifying fitness parameters of pathogen-challenged invertebrate hosts. Our results suggest that dietary PUFA supply should receive increased attention in host-microorganisms interactions and invertebrate disease models to better understand and predict disease dynamics in natural populations.

Equal relevance of omega‐3 and omega‐6 polyunsaturated fatty acids for the fitness of Daphnia spp.

“…Furthermore, we observed an increase in the somatic growth rate of D. magna when ARA was supplied. This is in line with the results from Schlotz et al (), who observed higher growth rates of D. magna fed with an ARA‐enriched food mixture of A. obliquus and S. elongatus compared to a C 20 ‐PUFA‐free diet. Becker and Boersma () also observed an increase in somatic growth of D. magna when ARA was supplemented to P‐sufficient A. obliquus and provided an ARA threshold (lowest ARA concentration at which the growth of D. magna was not limited) of only 0.06 mg g −1 dry mass which corresponds to approximately 0.136 μ g ARA mg POC −1 when a conversion factor of dry mass to carbon of 0.44 is used (Becker and Boersma , ).…”

“…As both ARA and EPA serve as precursors for eicosanoids (Heckmann et al , b ; Schlotz et al ; Garreta‐Lara et al ), they play an important role for Daphnia ’s reproduction and the immune system (Martin‐Creuzburg et al ; Schlotz et al ; Fink and Windisch ). For example, ARA was shown to improve the survival and reproduction of D. magna exposed to an opportunistic bacterial pathogen (Schlotz et al ). However, in vertebrates, ARA‐ and EPA‐derived eicosanoids have partially opposing effects, where their proinflammatory and anti‐inflammatory activity, respectively, serves as the best example (Schmitz and Ecker ; Alcock et al ).…”

“…Furthermore, the survival and reproduction of D. magna when exposed to an opportunistic bacterial pathogen ( Pseudomonas sp.) were increased when ARA was supplemented to a C 20 ‐PUFA‐deficient diet (Schlotz et al ). Additionally, Schlotz et al () also observed an increased growth of D. magna when a C 20 ‐PUFA‐free diet mixture of Acutodesmus obliquus (formerly Scenedesmus ) and Synechococcus elongatus was supplemented with ARA, which is in contrast to the previous findings from von Elert (), Martin‐Creuzburg et al (), and Ravet et al ().…”

Resilience to changes in lake trophic state: Nutrient allocation into Daphnia resting eggs

“…Based on annual averages, the contribution of cyanobacteria to total phytoplankton biomass never exceeded 13.5% (1972), and regarding summer means (May–October), cyanobacteria never represented more than 25.6% (1972) of total phytoplankton biomass, though their relative contribution was presumably much higher during the peak of cyanobacterial blooms (Güde & Straile, ). Supplementation experiments with nontoxic cyanobacteria suggest that Daphnia are limited by sterols when at least 30% of the total provided carbon is represented by cyanobacteria (von Elert et al, ; Martin‐Creuzburg et al, ; Schlotz, Pester, Freese, & Martin‐Creuzburg, ). It is thus possible that phytoplankton in Lake Constance always provided enough phytosterols that could be metabolized into cholesterol to prevent a limitation by sterols and to ensure sufficient cholesterol allocation into the resting eggs.…”

Combined effects of dietary polyunsaturated fatty acids and parasite exposure on eicosanoid-related gene expression in an invertebrate model

“…It is well established that the fecundity of Daphnia can be increased by supplementing the eicosanoid precursors ARA and EPA, implying that eicosanoid biosynthesis is linked to reproduction (Martin-Creuzburg et al, 2010;Schlotz et al, 2013). Moreover, it has been shown recently that the dietary PUFA supply can improve the performance of Daphnia magna under pathogen challenge, suggesting a link between eicosanoid biosynthesis and immunity (Schlotz et al, 2013(Schlotz et al, , 2014. These latter studies also proposed that the presence of eicosanoid precursors (i.e.…”