Freshwater zooplankton microbiome composition is highly flexible and strongly influenced by the environment

Abstract

The association with microbes in plants and animals is known to be beneficial for host's survival and fitness, but the generality of the effect of the microbiome is still debated. For some animals, similarities in microbiome composition reflect taxonomic relatedness of the hosts, a pattern termed phylosymbiosis. The mechanisms behind the pattern could be due to co‐evolution and/or to correlated ecological constraints. General conclusions are hampered by the fact that available knowledge is highly dominated by microbiomes from model species. Here, we addressed the issue of the generality of phylosymbiosis by analysing the species‐specificity of microbiomes across different species of freshwater zooplankton, including rotifers, cladocerans, and copepods, coupling field surveys and experimental manipulations. We found that no signal of phylosymbiosis was present, and that the proportion of “core” microbial taxa, stable and consistent within each species, was very low. Changes in food and temperature under laboratory experimental settings revealed that the microbiome of freshwater zooplankton is highly flexible and can be influenced by the external environment. Thus, the role of co‐evolution, strict association, and interaction with microbes within the holobiont concept highlighted for vertebrates, corals, sponges, and other animals does not seem to be supported for all animals, at least not for freshwater zooplankton. Zooplankton floats in the environment where both food and bacteria that can provide help in digesting such food are available. In addition, there is probably redundancy for beneficial bacterial functions in the environment, not allowing a strict host‐microbiome association to originate and persist.

Daily feeding rhythm linked to microbiome composition in two zooplankton species

“…In conclusion, our results are in contrast with prior zooplankton microbiome research indicating that microbe composition is predicted by the environment [8]. Moreover, the two species examined here were reared in the same environmental conditions, suggesting hosts may be able to maintain the microbial communities associated with their natural environment.…”

“…While most host-associated microbiomes are strongly associated with host phylogeny [21][22][23][24][25], the differences between these two species are striking, as these two distantly related species have been cultured in similar in-laboratory rearing conditions for years. While phylosymbiosis, the hypothesis that host-associated microbial communities of closely related host species are more similar to each other than to less related host species [26], has been observed in other invertebrate species, this pattern is not frequently observed in zooplankton species, as much of their microbiome is acquired from the environment [8,27]. The differences in community composition between D. dentifera and D. magna in this study, as well as the differences among other zooplankton species as demonstrated by Eckert et al [8], provide some evidence that zooplankton microbiomes are relatively distinct.…”

“…While phylosymbiosis, the hypothesis that host-associated microbial communities of closely related host species are more similar to each other than to less related host species [26], has been observed in other invertebrate species, this pattern is not frequently observed in zooplankton species, as much of their microbiome is acquired from the environment [8,27]. The differences in community composition between D. dentifera and D. magna in this study, as well as the differences among other zooplankton species as demonstrated by Eckert et al [8], provide some evidence that zooplankton microbiomes are relatively distinct. However, our results indicated that microbiome composition are not a result of environmental conditions.…”

“…Daphnia are dominant herbivores and serve as keystone species by linking primary producers with secondary consumers in freshwater systems [7]. Daphnia are an ideal system for addressing if and how feeding behavior and microbial composition are linked because (1) they have a relatively simple microbiome, which has been characterized in multiple species [8,9], (2) they have core clock genes and show circadian expression of feeding behavior, immune, and sensory genes [10][11][12][13], and (3) quantifying individual feeding behavior is straightforward [14].…”

Host Dependence of Zooplankton-Associated Microbes and Their Ecological Implications in Freshwater Lakes

“…The bacterial community associated with the same zooplankton population (Moina or Calanoids) also exhibits differences which may result from different characteristics of their ambient environment (Figure 2 and Table S1). Previous studies have demonstrated that the assembly of the ZA shows a strong environmental effect, suggesting that environmental variables also play an important role in shaping the zooplankton microbiome [40].…”