Abstract

BackgroundNutrient stoichiometry of phytoplankton frequently changes with aquatic ambient nutrient concentrations, which is mainly influenced by anthropogenic water treatment and the ecosystem dynamics. Consequently, the stoichiometry of phytoplankton can markedly alter the metabolism and growth of zooplankton. However, the effects of nutrient-imbalanced prey on the interplay between zooplankton and their gut microbiota remain unknown. Using metatranscriptome, a 16 s rRNA amplicon-based neutral community model (NCM) and experimental validation, we investigated the interactions between Daphnia magna and its gut microbiota in a nutrient-imbalanced algal diet.ResultsOur results showed that in nutrient-depleted water, the nutrient-enriched zooplankton gut stimulated the accumulation of microbial polyphosphate in fecal pellets under phosphorus limitation and the microbial assimilation of ammonia under nitrogen limitation. Compared with the nutrient replete group, both N and P limitation markedly promoted the gene expression of the gut microbiome for organic matter degradation but repressed that for anaerobic metabolisms. In the nutrient limited diet, the gut microbial community exhibited a higher fit to NCM (R2 = 0.624 and 0.781, for N- and P-limitation, respectively) when compared with the Control group (R2 = 0.542), suggesting increased ambient-gut exchange process favored by compensatory feeding. Further, an additional axenic grazing experiment revealed that the growth of D. magna can still benefit from gut microbiota under a nutrient-imbalanced diet.ConclusionsTogether, these results demonstrated that under a nutrient-imbalanced diet, the microbes not only benefit themselves by absorbing excess nutrients inside the zooplankton gut but also help zooplankton to survive during nutrient limitation.

Highlights

  • Nutrient stoichiometry of phytoplankton frequently changes with aquatic ambient nutrient concentrations, which is mainly influenced by anthropogenic water treatment and the ecosystem dynamics

  • The results indicate that the elemental composition of primary producers affects the growth, grazing behavior, and fecal parameters of herbivorous zooplankton, but it constrains ecological processes, such as food-web dynamics and the composition of fecal pellets, which are key for nutrient recycling [21, 22]

  • We investigated how microbiota, which were previously subjected to nutrient starvation stress, reacted to the nutrient-enriched D. magna intestinal environment; how the host and gut microbiota cooperated in the provision of nutrients; and how the gut microbiota mediated the properties of D. magna fecal pellets in a nutrient-imbalanced algal diet

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Summary

Introduction

Nutrient stoichiometry of phytoplankton frequently changes with aquatic ambient nutrient concentrations, which is mainly influenced by anthropogenic water treatment and the ecosystem dynamics. Primary producers usually experience dynamic fluctuations in the availability of nutrient resources; phytoplankton are more flexible in regulating their elemental composition (e.g., C:P, C:N and N:P ratios) than most heterotrophs [22, 23]. The results indicate that the elemental composition of primary producers affects the growth, grazing behavior, and fecal parameters of herbivorous zooplankton, but it constrains ecological processes, such as food-web dynamics and the composition of fecal pellets, which are key for nutrient recycling [21, 22]. Little is known about the effects of the nutrient-imbalanced algal prey on the metabolic interactions between zooplankton and their gut microbes, as well as the properties of the fecal pellets produced by the zooplankton

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