The effect of hypoxia onDaphnia magnaperformance and its associated microbial and bacterioplankton community: a scope for Genotype x Microbial community interactions upon environmental stress ?

Abstract

The depletion of oxygen as a result of increased stratification and decreased oxygen solubility is one of the most significant chemical changes occurring in aquatic ecosystems as a result of global environmental change. Hence, more aquatic organisms will be exposed to hypoxic conditions over time. Deciphering the effects of hypoxia on strong ecological interactors in this ecosystem's food web is critical for predicting how aquatic communities can respond to such an environmental disturbance. Here, (sub-)lethal effects of hypoxia and whether these are genotype specific in Daphnia, a keystone species of freshwater ecosystems, are studied. This is especially relevant upon studying genetic responses with respect to phenotypic switches (G x E interactions) upon environmental stress. Further, we investigated the effect of hypoxia on the Daphnia microbial community to test if the microbiome plays a role in the phenotypic switch and tolerance to hypoxia. For this, two Daphnia genotypes were exposed for two weeks to either hypoxia or normoxia and host performance was monitored together with changes in the host associated and free-living microbial community after this period. We found G x E interactions for some of the tested Daphnia performance traits. The microbial community responded to hypoxia stress with responses in the bacterioplankton and in the Daphnia associated microbial community with respect to species richness and community composition and structure. The latter response was different for the two genotypes suggesting that the microbiome plays an important role in G x E interactions with respect to hypoxia tolerance in Daphnia, but further testing (e.g. through microbiome transplants) is needed to confirm this.

Genotype specific and microbiome effects of hypoxia in the model organism Daphnia magna

“…Possibly, the KNO genotype has a stronger intrinsic tolerance to hypoxia, or the KNO genotype is more efficient in the uptake of useful bacteria from its surroundings. The first explanation seems unlikely as a previous study on the same genotypes showed no strong significant difference in the survival probability between KNO and F in hypoxia (Coone et al, 2023). However it should be noted that in this study the Daphnia individuals were not made germ‐free, so priority effects in the microbial community may have masked host genotype dependent effects (Callens et al, 2020).…”

“…However, hypoxia‐induced microbiome shifts have been detected in the river prawn Macrobrachium nipponense (Sun et al, 2020) and fish Bostrichthys sinensis , where hypoxia alters the function of Clostridia and increases Gammaproteobacteria in the latter (Fan et al, 2020). In D. magna , it has been shown that a hypoxia exposure of 2 weeks induces a genotype specific shift in the gut bacterial community towards a lower species richness (Coone et al, 2023). This suggests a hypoxia‐induced gut microbiota adaptation, which we could not confirm in the donors of our experiment.…”

“…For example, rare taxa are primarily responsible for host genotype dependent alterations in the composition of the bacterial community upon parasite infection (Rajarajan, 2023). Interestingly in this context is that hypoxia‐induced shifts in the microbiome are associated with the loss of rare classes Polyangia , Acidimicrobiia , Armatimonadia and Kapabacteria (Coone et al, 2023). A final explanation could be the presence of Daphnia tissue and hormones that are likely transferred together with the gut microbiota in the surrounding water.…”

“…It has been shown that microbiome mediated changes due to an environmental stressor, such as mercury stress, temperature and toxic diets, can contribute to stressor tolerance in Daphnia (Akbar et al, 2020; Akbar et al, 2022; Fong et al, 2019; Frankel‐Bricker et al, 2020; Macke, Callens, et al, 2017). In a recent lab‐controlled experiment (Coone et al, 2023), it was shown that after an exposure of 2 weeks to hypoxia, D. magna individuals in general had an impaired reproduction, smaller body size and lower survival. However, only a genotype × environment interaction could be found for body size, indicating that the tested genotypes had a high hypoxia tolerance.…”

“…In association with the phenotypic changes, Daphnia 's gut bacterial communities were different between oxygen treatments with a decrease in species richness in hypoxic conditions. These host phenotypic and microbial responses varied between the tested genotypes (Coone et al, 2023).…”