Dataset Information

Disparate effects of antibiotic-induced microbiome change and enhanced fitness in Daphnia magna.

ABSTRACT: It is a common view that an organism's microbiota has a profound influence on host fitness; however, supporting evidence is lacking in many organisms. We manipulated the gut microbiome of Daphnia magna by chronic exposure to different concentrations of the antibiotic Ciprofloxacin (0.01-1 mg L-1), and evaluated whether this affected the animals fitness and antioxidant capacity. In line with our expectations, antibiotic exposure altered the microbiome in a concentration-dependent manner. However, contrary to these expectations, the reduced diversity of gut bacteria was not associated with any fitness detriment. Moreover, the growth-related parameters correlated negatively with microbial diversity; and, in the daphnids exposed to the lowest Ciprofloxacin concentrations, the antioxidant capacity, growth, and fecundity were even higher than in control animals. These findings suggest that Ciprofloxacin exerts direct stimulatory effects on growth and reproduction in the host, while microbiome- mediated effects are of lesser importance. Thus, although microbiome profiling of Daphnia may be a sensitive tool to identify early effects of antibiotic exposure, disentangling direct and microbiome-mediated effects on the host fitness is not straightforward.

SUBMITTER: Motiei A

PROVIDER: S-EPMC6941804 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Disparate effects of antibiotic-induced microbiome change and enhanced fitness in Daphnia magna.

Motiei Asa A Brindefalk Björn B Ogonowski Martin M El-Shehawy Rehab R Pastuszek Paulina P Ek Karin K Liewenborg Birgitta B Udekwu Klas K Gorokhova Elena E

PloS one 20200103 1

It is a common view that an organism's microbiota has a profound influence on host fitness; however, supporting evidence is lacking in many organisms. We manipulated the gut microbiome of Daphnia magna by chronic exposure to different concentrations of the antibiotic Ciprofloxacin (0.01-1 mg L-1), and evaluated whether this affected the animals fitness and antioxidant capacity. In line with our expectations, antibiotic exposure altered the microbiome in a concentration-dependent manner. However, ...[more]

PMID: 31899775

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Project description:Concerns are being raised that microplastic pollution can have detrimental effects on the feeding of aquatic invertebrates, including zooplankton. Both small plastic fragments (microplastics, MPs) produced by degradation of larger plastic waste (secondary MPs; SMPs) and microscopic plastic spheres used in cosmetic products and industry (primary MPs; PMPs) are ubiquitously present in the environment. However, despite the fact that most environmental MPs consist of weathered plastic debris with irregular shape and broad size distribution, experimental studies of organism responses to MP exposure have largely used uniformly sized spherical PMPs. Therefore, effects observed for PMPs in such experiments may not be representative for MP-effects in situ. Moreover, invertebrate filter-feeders are generally well adapted to the presence of refractory material in seston, which questions the potential of MPs at environmentally relevant concentrations to measurably affect digestion in these organisms. Here, we compared responses to MPs (PMPs and SMPs) and naturally occurring particles (kaolin clay) using the cladoceran Daphnia magna as a model organism. We manipulated food levels (0.4 and 9 ?g C mL-1) and MP or kaolin contribution to the feeding suspension (<1 to 74%) and evaluated effects of MPs and kaolin on food uptake, growth, reproductive capacity of the daphnids, and maternal effects on offspring survival and feeding. Exposure to SMPs caused elevated mortality, increased inter-brood period and decreased reproduction albeit only at high MP levels in the feeding suspension (74% by particle count). No such effects were observed in either PMP or kaolin treatments. In daphnids exposed to any particle type at the low algal concentration, individual growth decreased by ~15%. By contrast, positive growth response to all particle types was observed at the high algal concentration with 17%, 54% and 40% increase for kaolin, PMP and SMP, respectively. When test particles comprised 22% in the feeding suspension, both MP types decreased food intake by 30%, while kaolin had no effect. Moreover, SMPs were found to homoaggregate in a concentration-dependent manner, which resulted in a 77% decrease of the ingested SMPs compared to PMPs. To better understand MP-processing in the gut, gut passage time (GPT) and evacuation rate of MPs were also assayed. SMPs and PMPs differed in their effects on daphnids; moreover, the particle effects were dependent on the MP: algae ratio in the suspension. When the MP contribution to the particle abundance in the medium changed from 1 to 4%, GPT for daphnids exposed to SMPs increased 2-fold. Our results suggest that MPs and, in particular, SMPs, have a greater capacity to negatively affect feeding in D. magna compared to naturally occurring mineral particles of similar size. Moreover, grazer responses observed in experiments with PMPs cannot be extrapolated to the field where SMPs dominate, because of the greater effects caused by the latter.

Project description:BackgroundPiRNAs prevent transposable elements wreaking havoc on the germline genome. Changes in piRNA expression over the lifetime of an individual may impact on ageing through continued suppression, or release, of transposable element expression. We identified piRNA producing clusters in the genome of Daphnia magna by a combination of bioinformatic methods, and then contrasted their expression between parthenogenetically produced eggs representing maternally-deposited germline piRNAs of young (having their 1st clutch) and old (having their 5th clutch) mothers. Results from eggs were compared to cluster expression in three generations of adults.ResultsAs for other arthropods, D. magna encodes long uni-directionally transcribed non-coding RNAs consisting of fragmented transposable elements which account for most piRNAs expressed. Egg tissues showed extensive differences between clutches from young mothers and those from old mothers, with 578 and 686 piRNA clusters upregulated, respectively. Most log fold-change differences for significant clusters were modest, however. When considering only highly expressed clusters, there was a bias towards 1st clutch eggs at 41 upregulated versus eight clusters in the eggs from older mothers. F0 generation differences between young and old mothers were fewer than eggs, as 179 clusters were up-regulated in young versus 170 old mothers. This dropped to 31 versus 22 piRNA clusters when comparing adults in the F1 generation, and no differences were detected in the F3 generation. Inter-generational losses of differential piRNA cluster were similar to that observed for D. magna micro-RNA expression.ConclusionsLittle overlap in differentially expressed clusters was found between adults containing mixed somatic and germline (ovary) tissues and germ-line representing eggs. A cluster encompassing a Tudor domain containing gene important in the piRNA pathway was upregulated in the eggs from old mothers. We hypothesise that regulation of this gene could form part of a feedback loop that reduces piRNA pathway activity explaining the reduced number of highly-expressed clusters in eggs from old mothers.

Dataset Information

Disparate effects of antibiotic-induced microbiome change and enhanced fitness in Daphnia magna.

Publications

Disparate effects of antibiotic-induced microbiome change and enhanced fitness in Daphnia magna.

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